Cephalove

The Big Move

2010-08-07T00:12:00.001-04:00

This week, I was graciously invited to join the Southern Fried Science blog network. I accepted, and so will be relocating to www.cephalove.southernfriedscience.com . All of the old posts have been copied to that site, and no new posts will show up here. I'm sorry if this is a hassle for all of you generous souls who link to me, but please continue to link to me at my new and improved location!

Thanks so much to all of my readers, and those of you who put up with my rambling comments on your own blogs. If there is one reason I have enjoyed blogging, it's your feedback and encouragement.

Memory, observation, and consciousness in Octopus Vulgaris

2010-08-05T12:35:00.000-04:00

          A while back, I wrote a post about short and long term memory processes in cephalopods. I wrote then that there is good evidence for a dissociation of short and long term memory process in cephalopods, but that this isn't a good basis (alone) for inferring the presence of consciousness, or in the case of arguments about animal's rights, the capacity to suffer (which, I guess, usually comes along with being conscious.) I stand by this; I just want to cover a neat study that I missed while writing that post: Lesions of the vertical lobe impair visual discrimination learning by observation in Octopus vulgaris by Fiorito and Chichery (1995). This uses an observational learning task that Fiorito and Scotto used in their 1992 article on observational learning in the octopus, where the test octopus watches another octopus perform a visual discrimination, and then is tested on that discrimination. Octopuses can (apparently) learn a simple task by watching another octopus do the task pretty well, and so in their 1995 paper, Fiorito and Chichery examine the effect of brain lesions to the vertical lobe of O. vulgaris on their retention of this task, as well as a discrimination learned through the more traditional method of reward and aversion (in the case of the octopus, some fish for a correct answer and a small electric shock for an incorrect answer, usually.)

          The vertical lobe is one of many lobes in the cephalopod brain. It sits above the oesophagus, and receives input from the sensory systems of the arms and visual information from the optic lobes. It is classically associated with learning, so that removal of the vertical lobe results rather reliably in deficits in the learning of a discrimination task. When asking questions about the presence of short and long term memory processes, one has to differentiate between the two. Thus, Fiorito and Chichery test their animals at two time points, 1.5 hours after training and 24 hours after training. It's important to note that this 24 hours would not nearly qualify as long-term in human memory, where memories can be stored for many years. In the octopus, tactile memories have only been shown to be retained for up to 50 days, although interestingly enough, the removal of the vertical lobe after a task has been learned appears to improve memory retention (Sanders, 1970.) I'll get back to this.

          On to the procedure! Fiorito and Chichery trained one group of octopuses to disciminate between a white ball and a red ball - specifically, to attack the white ball and not the red ball. Then, another group (which had been operated on, some having their vertical lobe partially removed and others having a sham surgery) watched the first group perform the discrimination for 4 trials. They were then tested, to see if they could remember the discrimination at 1.5 hours after training and at 24 hours after training. The results are shown below:

          This is a bit of an odd way of showing the data (I would have done a line graph, myself.) First of all, the bars in each graph show how many of the tested octopuses chose which ball, the red (R) or the white (W). NA is used for trials in which the octopuses did not make a valid response (ie. did not attack either ball.) The white ball can be thought of as the "correct" choice. The top row of graphs shows animals with the vertical lobe removed, and the bottom row shows animals who received a sham surgery. The first column of graphs shows the 1.5 hour test, and the second column shows the 24 hour test. The sham-operated group looks much as one might expect them to - they learn, and they retain the learning. The lesioned group is strikingly impaired. At 1.5 hours, it's clear that the removal of the vertical lobe has hurt performance, as these animals are performing at chance levels. By 24 hours, however, they seem to have improved! This is odd. If we explain this by analogy to human learning processes, we would have to say that these octopuses formed a long-term memory of the task without forming a short-term memory of it first. This indicates that "short-term" and "long-term" memory like what we talk about in mammals is not readily applicable to the description of learning in cephalopods.

          Consider for a moment the results of Sanders (1970), who found that octopuses who learned a task and had their vertical lobes removed (unfortunately, I cannot find the full text of the paper at the moment and so I don't know the exact procedure) retained it better than those who had intact vertical lobes - that is, they retained it for a longer period of time. If Fiorito and Chichery had tested their octopuses at longer intervals, we might expect that they would find the same results, with vertical lobe remove leading to a greatly delayed acquisition of the memory as well as a slower decay of the memory. This strikes me as odd, as I do not believe that this can be shown to be the case with people. In general, if people cannot remember something for a short time, they cannot thereafter remember it better after a long interval - it is simply gone from the system. I may be wrong about this point (and please point out any counter-examples you know), but it seems to me that the memory of cephalopods doesn't correspond very cleanly to the "working memory-consolidation-long term memory" model that is used to describe human memory.

          And why should it? Cephalopods may not have memory that looks like ours, but they have highly developed memory systems that serve them well enough. If anything, we should be excited that our theories of human memory cannot explain cephalopod memory very well; the more varieties of memory systems we have to study, the more we can learn about learning, period.

          This paper is a big deal (theoretically speaking) for a reason besides its illustration of the role of the vertical lobe in the time course of memory. Did you catch it? The authors used an observational learning task. That is, the octopuses being tested did not receive fish for the correct answer and shocks for the incorrect answer in the task. They did the task (correctly, at that) without ever being rewarded or punished for it; instead, they learned how to do the task by watching another animal perform it. When Fiorito and Scotto published a paper on observational learning in the octopus in 1992, people had a hard time swallowing it. It simply did not make sense, critics contended, that octopuses, being such loners, would have the capacity for observational learning. Why would they have evolved the capacity to be cooperatively social? The fact that they can learn by observation is one of the arguments that proponents of cephalopod consciousness (that is, the idea that cephalopods have some form of conscious awareness) often cite this as evidence of their general powers of cognitive representation. The octopuses are not being social, they're just being smart. At some level, they appear to have a representation of themselves and other beings, enough that they can learn a simple task by observing another octopus do it. In any case, replicating this finding adds some weight to Fiorito and Scotto's argument that octopuses can learn by observation.

Thanks for reading!

Fiorito G, & Chichery R (1995). Lesions of the vertical lobe impair visual discrimination learning by observation in Octopus vulgaris. Neuroscience letters, 192 (2), 117-20 PMID: 7675317

Fiorito, G., & Scotto, P. (1992). Observational Learning in Octopus vulgaris Science, 256 (5056), 545-547 DOI: 10.1126/science.256.5056.545

SANDERS, G. (1970). Long-term memory of a tactile discrimination in Octopus vulgaris and the effect of vertical lobe removal Brain Research, 20 (1), 59-73 DOI: 10.1016/0006-8993(70)90154-X

Cephalopod Links Number 4.5

2010-08-02T10:00:00.002-04:00

At National Geographic, you can check out some footage and a story about the successful attachment of a critter cam to a Humboldt squid. I'll have to get ahold of their television show somehow, seeing as I don't have TV, and it was last Friday, anyways.

Although it's an old piece, I want to point out this article on the expansion of the Humboldt squid's range. It's a very interesting topic, and one that is still (as far as I know) ripe for investigation and theorizing.

PZ Meyers points out a video claiming (among other ~~things~~ fallacies) that the fossil record of coleoid cephalopod ancestors provides evidence against "macroevolution". Of course, the alternative, and so presumably correct, theory is "Intelligent Design". Wow.

Folks in Delaware can head down to the Delaware Seashore State Park and dissect a squid for $8, among other great activities. Now that's good use of public facilities!

Departing from cephalopod-related links for a moment, Virginia Heffernan has written this piece over at the New York Times that's gotten science bloggers in a tizzy, and which I can't help but feel a wee bit offended by. While most of the article is spent blasting ScienceBlogs in particular (which I find catty and off-topic much of the time, too,) she has a few cracks at science blogging in general, including this gem:

"...science blogging, apparently, is a form of redundant
and effortfully incendiary rhetoric that draws bad-faith
moral authority from the word “science” and from
occasional invocations of “peer-reviewed” thises and
thats."

Please, stop me the next time I start throwing around "incendiary rhetoric"on Cephalove.

Check out this cool video of giant octopus kites.

And then this one of S. latimanus in an agonistic encounter, complete with some great changes in coloration.

Circus of the Spineless #53, that virtual periodical on all things invertebrate, is up at The Birder's Lounge. Make sure to check it out for an interesting assortment of writing on all sorts of spineless wonders.

I'll be back later in the week with some more cephalopod photographers, and a few science-y posts. I'm thinking about tackling the "cephalopod consciousness" issue, although it will take a bit of work to get ahold of the literature, read it, and then work out where I stand. Nonetheless, I'll see what I can get up here.

Thanks for reading!

Cephalopod Photography: Barry Fackler

2010-08-02T00:07:00.000-04:00

Today's cephalopod photographer of note is Barry Fackler, a physical therapist originally from Pennsylvania who lives and dives in Hawai'i. All of the photos in this post are his, and they're all click-through-able, so check out the larger sizes. It turns out that octopods (mostly O. cyanea) are the only cephalopods in his Flickr portfolio, so I'm sorry to disappoint the squid and cuttlefish lovers out there. I promise they are all wonderful photos, though!

Here is an O. cyanea showing a mostly white color pattern while jetting, a behavior often associated with defensive flight.

Here is another gorgeous octopus of the same species, giving the camera an inquisitive look. This was taken at at Keone'ele Cove in Honaunau (another place to add to my "List of incredible spots to visit when I get money" spreadsheet.)

I always love to see octopuses express dramatic papillae. In this next shot, we see an octopus who is apparently trying to look like just another chunk of coral, even if he's not doing a terribly good job.

This next one shows an octopus (O. cyanea again) in a defensive posture. Notice the high contrast color pattern, the curled arms, and the spread interbrachial web. The point of this behavior is to look big enough to make a potential predator think twice before he eats you - it's a common strategy among prey species. According to Barry, the animal adopted this pose when approached by some fish.

I like this next shot simply because you can see right into the octopus's mantle. It's somehow fascinating to me to see the inside and outside of an animal at the same time like this.

These next two photos show some behavior that I had never heard of before reading the photographer's description. Apparently, the fish (a peacock grouper) was following this octopus around to feed on small prey that the octopus stirred up as it foraged over the reef. According to Barry, they usually follow eels, but he found this one hanging around a hunting O. cyanea. I'd argue that it is probably not cooperative hunting per se, as it's unclear how the octopus would benefit from it, but it's fascinating behavior nonetheless.

I'll finish up with two gorgeous portraits of O. cyanea just sitting on the reef. I love the colors of these octopuses.

Thanks for reading! Make sure to click on over to Barry's photostream and check out his other underwater photos.

Serotonin in the octopus learning system.

2010-08-01T10:00:00.001-04:00

          (Note: I apologize if this post seems jargon-ey. I've tried to explain or reference any hard to get terms, but I do assume that readers know the very basics of neural functioning. If you need a primer on this, check out wikipedia's page on neurons or this great tutorial. Feel free to post in the comments if there's anything you want explained more thoroughly, and I'll give it a crack.)

          The Octopus research group in Jerusalem is back with a paper in the August issue of Neuroscience about the function of serotonin in the octopus vertical lobe, Serotonin is a facilitatory neuromodulator of synaptic transmission and “reinforces” long-term potentiation induction in the vertical lobe of Octopus vulgaris. I'm very excited to blog about this paper - it's the very first time in my short blogging career that I've gotten to cover a study as it was coming out! You can read my other posts about their work here and here (that second one has a basic description of the technique of stimulation-induced LTP, which I'll be very brief with here.)

          Basically, LTP (long-term potentiation) is one of the mechanisms by which neurons are thought to adjust how they connect to each other during the process of learning - specifically, they become stronger (or potentiated,) meaning that signals are carried across the synapse more effectively. The authors of this paper use a technique by which they induce LTP in synapses in the octopus vertical lobe (a structure thought to be involved in learning and memory) and study the effects of serotonin (also called 5-HT, which is short for 5-hydroxytryptamine, the terminology I'll be using from now on) on the properties of the induced LTP. Presumably, this can tell us something about the function of 5-HT in the normal functioning of the vertical lobe, although this point is very debatable.

          Why look at 5-HT? Well, for starters, it's one of the big neurotransmitters these days (along with such illustrious nearly-lay-term chemicals as dopamine, norepinephrine, GABA and glutamate.) You hardly need to have a specific reason to study it these days because it's involved in pretty much every process that contemporary neurobiology cares about: consumptive behavior, mood and depression, social cognition, the action of addictive drugs. More than that, though, it's conserved across all bilaterians, the group of bilaterally symmetrical animals including people, the rest of the vertebrates, the insects, and, among many others, the molluscs! If there is any neurotransmitter that is interesting to study comparatively, it's 5-HT, as it's been shown to be involved in learning in animals as distantly related to each other as sea slugs, rats, humans, and (now) cephalopods. If we learn how 5-HT does its job in a wide variety of animals, it will help us understand how neurotransmitters function within nervous systems in general. This is, we will hopefully agree, a Good Thing.

          The authors begin with the hypothesis that, as has been shown in Aplysia (a beautiful little sea slug who is relatively widely studied in neuroscience,) 5-HT probably has a role in the modulation of LTP rather than inducing it directly, making it a putative neuromodulator. It is not hard to imagine how this might be a good thing to have in a memory system. Let's pretend that our animals has just been injured, or that it has just found a great big source of food. All of these events call for a general upregulation in the formation of memories, since remembering what happened around these events will help the animal repeat or avoid them in the future, depending on whether they were good or bad. If a chemical can increase the amount of LTP (a process thought to be involved in learning,) it would make sense that it might be selectively secreted or expressed during times when the animal's memory system needs to pay attention to what's going on, and not when there is nothing of consequence happening. This is an extremely limited view of the role of neuromodulators in learning, but it illustrates the principal as well as I know how to. In short, neuromodulators, while not responsible for neurotransmission and plasticity themselves, have some effect on it. This sort of effect is one of the things that allows the great flexibility of neural systems, one of their key features.

          In the first part of their study, the authors stained slices of the octopus vertical lobe for 5-HT, and then described what they say - this is good old fashioned neuroscience. They found that 5-HT shows up in fibers from the medial superior frontal lobe (MSF) that innervate large areas of the vertical lobe. The MSF is thought to be one of the main sources of input of sensory information to the vertical lobe, and this tract of fibers (known as the MSF-VL tract) is thought to be involved in the formation of sensory memories in the octopus, as per J. Z. Young's early lesion experiments in the octopus. The authors note that this wide spread of 5-HT is typical of neuromodulators, supporting the idea that MSF neurons use 5-HT to modulate LTP in the vertical lobe.

          In the second part of the study, the authors use a technique where they induce LTP in live slices of octopus brain (cool, right?) by repeatedly stimulating the axons running from the MSF to the vertical lobe. They measure the "strength" of neurotransmission as fPSP's, or synaptic field potential, which is roughly an indicator of how much electrical activity is generated by activity in many synapses within a small area of the tissue. I'll only summarize one of their several experiments here, because it is the one that really illustrates the neuromodulatory effect.

          This figure shows the results of an experiment using induced LTP in octopus brain slices. The experimenters stimulated the brain slices along the MSF-VL tract and recorded the resultant electrical activity in the VL. Let's start with the first graph. The y-axis shows the amount of activity recorded in the vertical lobe after a very small electrical stimulation (this is what each data point is.) The x-axis shows the time from the beginning of the experiment. At about 30 minutes, MSF-VL neurons were stimulated with a "triplet", which consisted of three pulses in quick succession. As we can see in the control preparation (the blue line,) this w pas not enough to induce LTP, which would be evident as an increase in the field potential. In a preparation treated with 5-HT, however, this stimulation was enough to elicit some LTP, which is apparent as a stable elevation of the recorded field potential at times 50 and 60 minutes. After 60 minutes, each preparation was subject to high-frequency stimulation, which caused maximal LTP in both cases.   The bar graph next to it (B) shows the results of multiple experiments, showing that before high-frequency stimulation, the treatment with 5-HT caused an increase in the LTP resulting from the triple-pulse, indicating that the presence of 5-HT made MSF-VL synapses prone to undergo LTP. The second line graph (C) shows the results of a set of similar experiments, except that the stimulation was done once per minute. As is apparent, treatment with 5-HT (shown by the red bar) increased the rate of LTP; however, as indicated in the adjacent bar graph (D), it did not increase the maximum amplitude of LTP.

          It's important to remember that in the active nervous system, it's unlikely that synapses are ever stably at a maximal strength. That increase in the rate of induction of LTP, modest though it may seem in this experiment, could be crucial in affecting the functioning of a memory system in a behaving animal. In the "real world", the stimuli involved in learning are often only present for a short time, and the state of any particular synapse in the nervous system is determined by an incredibly complex set of chemical factors. Neuromodulatory activity (like that argued for in this paper) provides a sensitive mechanism by which the functioning of a neural system could be finely coordinated, allowing the integration of a variety of information into one system that can make a timely decision about whether an action was good enough to repeat or bad enough to avoid in the future.

          For convenience's sake, I skipped a variety of other interesting experiments that the authors did, and I encourage you to get the paper yourself and read it, if you can. I very much like this type of research, and I like the challenge that blogging about it presents. Anyways, I hope you've enjoyed this as much as I have!

Thanks for reading!

Shomrat T, Feinstein N, Klein M, & Hochner B (2010). Serotonin is a facilitatory neuromodulator of synaptic transmission and "reinforces" long-term potentiation induction in the vertical lobe of Octopus vulgaris. Neuroscience, 169 (1), 52-64 PMID: 20433903

Cephalopod Photography: Klaus Stiefel

2010-07-30T23:51:00.001-04:00

Next on my (long and growing) list of cephalopod photographers to feature here is Klaus M. Stiefel, a neurobiologist who currently works in Okinawa. All of the photos in this post were taken by him. He was cool enough to release them under a creative commons license, so feel free to use them, just don't use them for anything commercial and make sure to give him credit (lots and lots of it.) You can click through on all of the photos to access them on Flickr, including larger versions (which I always recommend - they make great desktop wallpapers.) Let's dive right in, shall we?

To start off, a portrait of an adorable cuttlefish of unknown species (if anybody can tell, please post it in the comments - I'm embarrassed to admit it, but I'm very bad at identifying species):

Moving right along, we have these two lovely photos of the flamboyant cuttlefish, Metasepia pfefferi. Klaus calls this posture a "threat display", although I'm pretty sure it is used both as a defensive behavior and during hunting, especially for shrimp and prawns. My favorite thing about pictures of M. pfefferi is that they always look so relaxed, just because of the shape of their pupils.

Last in our illustrious lineup of cuttlefish is an unidentified individual who is expressing its papillae beautifully and showing off its ability to use binocular vision by looking at the camera with (count 'em) two eyes.

You want squid? We've got squid! Well, a squid. This is a juvenile squid (species unknown, though one of the commenters on Flickr suggests that it's a bigfin reef squid, Sepioteuthis lessoniana) floating among the fronds of a sea lily.

Here is an octopus (again, species unknown) expressing a very striking white ring around its eye. This looks to me like it might be related to the eye-bar body pattern component, which is used during defensive behavior by adult octopuses to obscure the shape of the eye or make it appear larger than it really is.

Here's a great shot of some octopus arm suckers, showing various degrees of flexion of the suckers themselves. I wish I knew the species of octopus that these belonged to.

I just love pictures of octopuses peeking out of things! Here is the obligatory inquisitive-octopus-eyes shot:

In this series of photos, Klaus captured a dramatic color change in an octopus. It looks to me like the octopus tried to camouflage itself, then decided that wasn't going to work and began to hide under the rocks.

Finally, we'll close with a gorgeous photo of a cephalopod that is too often ignored: the Nautilus.

Thanks for reading!

Cephalopod Photography: Lawrence Tulissi

2010-07-30T01:20:00.001-04:00

I stumbled upon the Flickr group: Cephalopods , and decided that it was about time to put up some more eye candy on the site. I've gotten in touch with some of the photographers whose cephalopod photos are in the group, and I'll be doing a series of posts with each post featuring the work of a single photographer.

First on the list is Lawrence Tulissi. All of the photos in this post are click-through-able if you want a larger image - which I highly recommend - and are his property (so don't steal them.)

First is an octopus (looks like it could be O. cyanea to me, but I'm not the best at species identification) in a neat posture, with a very striking pattern of coloration. This was taken at Truk Lagoon, which sounds like an incredible place to dive.

This next one shows the suckers of a giant Pacific octopus. I like that you can see suckers in various states of contraction, showing the great flexibility that having multiple sets of muscles in each sucker affords the octopus.

This next one is of O. briareus, the Caribbean reef octopus, showing off its long arms and exhibiting some great body patterning. This posture is probably defensive, judging by how conspicuous its coloration is and the fact that the interbrachial web is spread.

This picture shows the eye of a giant Pacific octopus. The description of the photo says that the octopus was in its den, and the closed pupil slit indicates that it was likely resting. In a neat case of functional homology, octopuses, like many vertebrates, tend to close their eyes when they rest - it's just that, since they have no eyelids, they do this by closing their pupils. If you don't believe me check out Brain and behavioural evidence for rest-activity cycles in Octopus vulgaris by Brown et al. (2006).

Moving on from octopuses (as much as it pains me), we'll finish up with two wonderful shots of Carribean reef squid, Sepioteuthis sepioidea:

Thanks for the photos, Lawrence!

Everybody else, thanks for reading. I'll be writing on some brand-spanking-new research on the role of serotonin in the octopus learning system next week, so I'll see you then!

Pass the clams, please: A strategy for object retrieval in the octopus.

2010-07-27T19:05:00.000-04:00

          I recently blogged about a line of research on octopus reaching movements, but I left out an important study for time's sake. I promised to cover it promptly, and so I'm making good on that promise here. To recap:

          It has been shown that reaching movements by octopuses are controlled by the nervous system of the arms relatively autonomously from the central nervous system; that is, a severed arm can complete these movements on its own, given the proper stimulation of the base of the nerve cord of the arm. This is all well and good, as the movements being studied were rather simple, involving the extension of an arm. This reaching movement was found to consist of a propagating wave of muscle activity down the arm, a solution to the control of such a flexible appendage that greatly reduces the amount of neural computation that is needed to make such a movement.)

          The study I'll look at today is Octopuses Use a Human-like Strategy to Control Precise Point-to-Point Arm Movements by Sumbre et al (2006). In it, the authors study a more complicated movement: retrieval of an object using a single arm. This is a problem of interest to neuroscientists and roboticists, because understanding how the octopus generates controlled, precise movement using an appendage with so many possible movements might give us some insight into the optimal solution of this problem. This could help reveal general rules of efficiency in neural programming.

          Beginning (as is advisable) at the beginning, the authors videotaped reaching movements in O. vulgaris that were elicited by touching a piece of food to the animal's outstretched arm. Their observations revealed that octopuses create joints in their arm during this movement, around which they move stiffened segments of the arm much the same way that animals with a skeleton (notably, humans) do. A series of stills from one of their videos and a lovely diagram of the arm "joints" of an octopus who is about to eat an unhappy-looking fish are shown below:

          It turns out that most of the distance covered in this movement sequence comes from the arm's rotation about the medial joint (the yellow one), much as most of the effective range of human retrieval movements come from flexion of the elbow. After some more detailed analysis of the kinetics of this movement (which I'll skip here - but please check out the paper if you're interested) the authors go on to probe the pattern of muscle activity that is responsible for this movement as they did in their earlier studies (for a brief explanation of their methods, see my earlier post; for a longer one, see the paper reference therein.) They found differences in patterns of muscle activity depending upon where in the arm recordings were being made. When they looked proximally to the medial joint (eg. in arm segment L1 in the above diagram,) they found that a wave of muscle activity propagated away from the body, as it does in reaching movements. When they recorded from a portion of the arm distal to the medial joint (eg. in arm segment L2,) they found that muscle activity was propagating in the opposite direction - from the tip of the arm towards the base.

          Using these results, the authors offer an elegant explanation of the neural control of this behavior. They suggest that the initiation of a retrieval movement involves the initiation of two waves of muscle activity, one starting from the tip of the arm and one from the base. Where these waves meet, the medial joint is formed. In this way, the octopus nervous system simplifies the problem of finding an efficient way to retrieve an object, a problem which would be hard to solve on the basis of proprioception or neural control contingent on a direct representation of sensory space due to the flexibility of the octopus's body.

          In case you were wondering (I sure was), an experiment that was reported in the supplementary material (though it seems pretty important to me) revealed that retrieval could not be elicited in denervated arms in the way that arm extension can. Therefore, it appears that some input from the central nervous system is required to initiate this more complicated movement, although it is still possible (and seems likely) that, once initiated, the movement is driven primarily by peripheral mechanisms local to the arm performing the movement. The authors found that ablation of the anterior basal lobe left octopuses unable to initiate object retrieval, confirming its suspected function as a motor center in the octopus.

          The authors finally put forth a hypothesis of convergent evolution of reaching movements between octopods and vertebrates:

                    It is especially surprising that of all possible
                    geometrical structures and motor control strategies
                    with which a flexible arm can bring an object to the
                    mouth, the octopus generates a quasi-articulated structure
                    with a striking morphological and kinematic resemblance
                    to the multijoint articulated limbs of vertebrates.
                    Because the hypothetical common ancestor of cephalopods
                    and vertebrates dates back to the beginning of
                    Cambrian era (about 540 million years ago), fetching
                    appears to be a genuine and rare case of evolutionary
                    functional convergence, where two independent attributes
                    (morphology and neural control) coevolved to
                    achieve a common goal.

          I have no particular problem with this hypothesis. I'd be interested to see if these types of movements are present in other species of cephalopods, both decapods and other octopod varieties. I think that the case for convergent evolution in this instance will always be a hard sell, because (unlike, for example, the eye) the anatomy of the body parts executing the movement in question are so different. In addition, the movements studied in this paper were elicited in very specific conditions using octopuses that were trained to extend their arms and wait for food to be pressed to them, leaving it unclear what other types of movements they might make in retrieving an object as well as the relative importance of the aforementioned quasi-articulated arm movements in the ethogram of the octopus. Those criticisms aside, I'm willing to accept the idea that articulated movement really does represent a good solution to the problem of controlling movement, because it shows up across animalia so often and in so many forms. Why wouldn't we expect the octopus to get in on the action?

          Thanks for reading!

Sumbre, G., Fiorito, G., Flash, T., & Hochner, B. (2006). Octopuses Use a Human-like Strategy to Control Precise Point-to-Point Arm Movements Current Biology, 16 (8), 767-772 DOI: 10.1016/j.cub.2006.02.069

Do octopuses play?

2010-07-27T08:00:00.011-04:00

         I was recently pointed to this article on "octopus intelligence". I like the article (which features quotes from such cephalopod research all-stars as Roger Hanlon and Jennifer Mather,) although I am a bit let down by the brief, incomplete explanation that is given to the various "intellectual" abilities of the octopus such as "problem solving" and "play". Both of these behaviors are difficult to define precisely, and are often understood in vertebrates by analogy to human experience. For example, one of the criteria that is used to define play in animals (as stated in Kuba et al. 2003, a study on play-like behavior in octopuses) is that it is "spontaneous and pleasurable ('done for its own sake')". This is one of the central features of play - that it appears to serve no other immediate purpose than to entertain or occupy the animal expressing the behavior. I take some issue with the use of the term "play
to describe octopus behavior, at the very least because the implications of play-like behavior in the octopus are not very well studied yet. It's much harder to determine the motivational significance of an activity in an octopus than it is in, say, a rat. This is because we know the brain and behavior of the rat much more thoroughly than we know those of octopuses, and since they are structurally similar to ours we can relatively easily design valid measures of motivation in rats. In contrast to the vast (though still incomplete) neurological and behavioral description of pleasurable and aversive states in the rat that we have generated, we have only a very crude measure of the possible hedonic characteristics of an activity in the octopus; that is, we can assume that the octopus will do "pleasurable" things and will avoid aversive things, but we have little more to go on when we are talking about the motivation of an octopus. Because of this limitation, I think that it may be too early to say for sure what processes play-like behaviors in the octopus actually represent, and so the touting of play as evidence of the impressive mental powers of the octopus also seems premature.

         Whoa, now! Before I go making assertions like this, I should look at the research, right? Good call. Let's see what the vast scientific library that is the internet can teach us about the play-like behavior of octopuses.

         I'll focus on Kuba et al. (2006), a recent study that was done to examine putative play behavior in O. vulgaris. In this study, the authors exposed octopuses to stimuli made out of Lego blocks for half an hour at a time repeatedly over a period of 7 days and scored the octopuses reactions to the objects. The authors' scoring system is illustrated below (this if Figure 1 from the paper.)

         As you can see, level 3 (which the authors describe as "play-like") and level 4 (which the authors call "play") involve repeatedly manipulating non-food objects in complex, non-stereotyped ways for a significant amount of time. Out of 14 (wild-caught) subjects, object manipulation that was scored at level 3 was observed in 9 subjects, and object manipulation that was scored at level 4 was observed in one subject. There was no difference of age or hunger state in this behavior (young and old octopuses showed the same sorts of behavior, as did hungry and sated octopuses.) Play-like behaviors tended to occur after several days of presentation of the stimulus, suggesting that this was not merely exploratory behavior, which appeared to decrease during the first few days of exposure (as the octopuses presumably got used to the presence of the stimuli in their tanks.)

         By this point, I tentatively buy the characterization of these behaviors as "play" - they don't appear to serve any purpose for the octopus, who is clearly not simply confusing the objects with food. They are exhibited after the octopus has presumably had ample time to learn that they do not represent a threat. The behaviors do not appear to clearly belong to any other class of behavior (except perhaps tactile exploratory behavior.) As I said before, however, using the existence of these behaviors to argue for the intelligence of the octopus seems premature to me. For one, the significance of these behaviors in the wild is not well understood - they must confer some survival utility, but they do not appear to be disproportionately expressed in young, rapidly developing octopuses as they are in mammalian young, and so are unlikely to contribute to neurodevelopment in the same way that play in mammals (especially social mammals) is thought to. We know that play in social mammals (like humans, some apes, and rats) serves a variety of functions in development - to establish dominance hierarchies, to develop skills for living within social organizations, to learn hunting and food-gathering behaviors, to help develop motor coordination, etc. We have comparatively little sense of the importance of play in the life of an octopus, and so it is hard to know what play-like behavior means in the context of octopus cognition.

         Because we know that play is very important to the cognitive function of mammals I mentioned previously (more properly, we know that disrupting play behavior causes deficits in behaviors that depend on play to develop,) we can claim that play is part of a group of behaviors that make manifest the intelligence of these animals. Without knowing what play-like behavior does for an octopus, it's hard to say whether it implies an analogous intelligence in these animals. It might be explained in many cases as a simple extension of exploratory behavior. As a foraging predator, it makes sense that O. vulgaris would be served well by repeated, thorough explorations of the same object, which mobile and semi-mobile prey would presumably periodically be found on. This behavior might be explained as part of a foraging strategy that is somewhat impervious to associative learning, and so violate the criteria that we use to classify a behavior as play all together.

         My discussion thus far has accepted the hypothesis that behavior classifiable as play occurs regularly in the octopus, and thus needs to be explained in terms of its adaptive utility to the animal. Based on the previously summarized paper, however, clear play-like behavior in the octopus appears to be pretty rare. On the 5th day of the experiment, when play-like behavior peaked, 444 interactions with the stimuli were observed. Out of these, 13% qualified as level 2 (they involved manipulation beyond very basic exploration of the object with the arms,) 0.9% were scored as play-like, and a single observation (0.02% of the total observations) was scored as being definitively "play". I think this was a well-designed study, but the results don't convince me that play (as defined by the authors) is terribly important in the lives of octopuses, and might just as well represent a rare, specific type of interaction that they have with unusual stimuli in a laboratory environment.

         I realize that I have been sort of hard on this study. I don't want to imply that octopuses are not remarkable animals that are capable of many things one wouldn't expect from a mollusc. I do think, however, that it pays to be very skeptical about the use of the terms "play" and "intelligence". Both of these are concepts that we understand primarily by analogy to our experience of them as humans. We know that social play in vertebrates is indeed play (even the scientists among us) because we know what a play fight feels like, and understand intuitively how it differs from a real fight. We can extend this to behaviors that we see in animals (with more or less accuracy, depending on the situation.) We know what intelligence means (or we think we do) because we have expectations of how people should function, and we can draw analogies to other vertebrates who have the same sort of behavioral flexibility and environmental demands that we do. One might dismiss this as unscientific, but we have pretty good evidence that the neural structures that are responsible for a variety of emotions and types of behaviors are conserved in some form across species (in mammals at least.) Thus, we can be somewhat comfortable in our understanding of the role of play in a rat's cognitive life because, at a pretty complex level of structure and function, they have essentially the same machinery in their head that we do. It's a bit less convincing to use the same anthropomorphic logic to justify associating what looks like play behavior in an octopus with the "intelligence" that we suspect goes along with play behavior in vertebrates. This is because the existence of analogous neural substrates and their accompanying cognitive functions (emotions, hedonic value, etc.) is not clear. It strikes me as somewhat mistaken that we would use psychological constructs that were created to describe human behavior such as "play" and "problem-solving" to describe cephalopod behavior, though we do it even when they appear to be a poor fit to the behavior in question.

         As Jennifer Mather points out in her quote in the Boston Globe article: “We’re smart and the octopus is smart, but octopus intelligence just can’t be related to our intelligence.” This I have to agree with. Just because we can call a behavior something that sounds familiar (in this case, "play") doesn't mean that we've explained it, even though it might appear this way. I think that octopuses are fascinating and astounding creatures that exhibit very interesting behaviors; I'm just not quite convinced that they play.

Thanks for reading!

Kuba, M., Byrne, R., Meisel, D., & Mather, J. (2006). When do octopuses play? Effects of repeated testing, object type, age, and food deprivation on object play in Octopus vulgaris. Journal of Comparative Psychology, 120 (3), 184-190 DOI: 10.1037/0735-7036.120.3.184

M Kuba, D V Meisel, R A Byrne, U Griebel, & J A Mather (2003). Looking at Play in Octopus Vulgaris Coleoid cephalopods through time, 163-169

Neuromuscular Dynamics of Octopus Arm Movements

2010-07-23T01:01:00.000-04:00

I was planning on writing an article about cephalopod statocysts (and I still am; I've just had trouble deciding which pieces of research I want to cover and which I want to leave out) to continue on the theme of cephalopod sensory systems. I've stumbled upon a line research that I just had to blog about, though, so I'm putting off the statocyst post even further. The research in question is a series of studies by The Octopus Group at the Hebrew University of Jerusalem on the biomechanics and neural control of reaching movements of octopuses. I read this research some months ago (before I was blogging,) and I was reminded of it while watching Twister (the resident E. dofleini at the Niagara Falls Aquarium) groping about in his enclosure. I noticed that, as he moved his arms about, the movements almost always started with a bend near the base of the arm, which traveled out to the tip, becoming sharper and moving faster as it proceeded. It looked for all the world like the way a wave travels through water (or, more geek-ily, the way one imagines spontaneous activity propagating in a spatially extended nervous system.) The series of studies I will talk about here shows that this is generally the case, and characterizes the way that this happens with some detail, although we still do not know this system in nearly as fine detail as we know the vertebrate neuro-muscular system. I'm getting ahead of myself, though.

Why do we care about the details of how octopuses move their arms? First, it's just plain cool - who, upon looking at an octopus moving, hasn't wondered how it can possibly keep track of all those arms? Second, the octopus arm provides a unique model nervous system for a few reasons. It is a muscular hydrostat - that it, having no bones, it is a system of muscles that run perpendicularly to each other that maintain a roughly constant total volume; this property of an octopus arm allows it to function like a very flexible vertebrate limb because the muscles can pull against each other to form temporary, semi-rigid structures that allow the arms to bear weight. As such, it is a novel motor system (in terms of research, that is,) with most of the well-characterized motor systems we know of (ie. human, primate, reptile, etc.) are composed of skeletal muscles, which pull against bones. Besides this, the task of coordinating the movement of eight almost infinitely flexible arms is a herculean task in terms of neural processing, and it would be very informative (as well as a triumph of systems neuroscience) to understand how this is done. It has been thought, since the early days of octopus neuroanatomy, that much of the movement of the octopus's arms (and probably those of other cephalopods) is encoded in the nervous system of the arms rather than in the central nervous system (Graziadei, 1971). This is evidenced by the fact that there is no straightforward representation of the arms in the brain of the octopus, as there is in humans and most other vertebrates, as far as we know, and so it is unlikely that fine motor control comes from the central nervous system. Supporting the importance of the distributed nervous system of the arms is its incredible scale: the nervous system of the arms is much larger than the central nervous system of octopus, containing around 2/3 of all of the neurons in the animal. The octopus arm, then, is a unique example of a highly complex, distributed motor system that stands in contrast to the centrally controlled motor systems we are most familiar with. As with almost every topic in comparative neuroscience (I'm a big sucker for it), I think that the octopus motor system is important because by understanding it, we will understand more about vertebrate nervous systems; that is, we will (pretending for a moment that we could actually solve both systems) understand which features of them are critically related to the specifics of vertebrate and invertebrate neural functioning, physiology, development, and ecology. We would come closer to understanding why each system evolved the way it evolved. Finally, we would exercise our tools of modeling neural computation in a way that would allow us to figure out how generalizable they are. My final verdict: this is a good thing to study.

So now you're bored. You want to hear about some research! Well, I won't disappoint; at least, I hope I won't. We'll start with Gutfreund et al. (1998), one of the early papers out of this research group, which kicked off this line of research by examining the neuromuscular dynamics of octopus reaching movements. I should note that (presumably for simplicity,) this group generally only studies reaching movements in a single arm - it is not know exactly how their findings might relate to more complicated movements, including those involving multiple arms. As a disclaimer I am going to leave out description of a large portion of their study, which I encourage you to read in full, for my own convenience, and only present the results that I think are most relevant to the topic at hand.

This authors in this study used electromyography (a method of measuring the electrical activity of muscles) in O. vulgaris to determine how arm muscles are activated in sequence to produce octopus reaching movements. Briefly, they put electrodes through two points in a single arm of their (anesthetized) test animals, then allowed the animals to wake up and elicited reaching movements by tempting the octopus with either a crab or a target that was associated with food. They videotaped the reaching movement, which allowed them to compare the electromyogram to the behavior of the octopus. Reproduced below is their first figure, showing the gross cross-sectional anatomy of the octopus arm, as well as their electrode placement:

The white arrows indicate the position of the electrode, which is the white line running through the muscle. The striated outer portions of the arm are the muscle, and the round shape in the middle is the nerve cord of the arm.

They found that reaching arm movements usually start with a sharp bend near the base of the arm, which travels outwards until it reaches the tip, accelerating somewhat throughout the extention and then slowing as the arm reaches its target. Here's a series of images showing the behavior:

The authors found that this type of arm extension occurs virtue of a propagating wave of muscle contraction traveling down the arm, from the base to the tip. Shown here are examples of the type of data they used to confirm this:

The left panel shows two electromyograms from a single trial, the top one from the electrode nearer to the arm tip, and the bottom one nearer to the base of the arm. The arrows indicate when the bend in the arm reached each electrode. As is apparent, neuromuscular activity at the proximal site started earlier than that at the distal site, coinciding approximately with the timing of the movement of the bend in the octopuses arm. The graph shows the correlation between the lag in the electromyogram record between the two sites and the time it took for the bend in the arm to move between the two sites. It's clear that the propagation of the wave of electrical activity down the arm is highly correlated with the motion of the arm. The authors continue on to characterize some of the properties of these arm movements in more detail and propose a mathematical model for the movement of the octopus arm, but I'll leave those results out, here. I recommend this article for it's methodological clarity - too seldom do authors take such pains to make their method so clear and so thoroughly address their research question.

Moving on, the same reearch group (with a different first author) published a paper in Science describing their experiments with isolated arm preparations (Sumbre et al. 2001). This is where it gets really interesting to me, because this experiment really gets at the distinction between central and peripheral motor control. The authors made their preparations by either denervating one arm of an octopus that had already been decerebrated (a procedure somewhat akin to an octopus lobotomy) by severing its connection to the brain, or by severing an arm completely. They then attached the base of the arm to a surface, and stimulated the nerve cord at the base of the arm. It was found that, in a large percentage of cases (46%, to be exact,) the movement resembled the reaching movement seen in an intact animal. The figure below (taken from the paper) shows the reaching movement of a normal animal (on the left) and that elicited by stimulating the nerve cord of a denervated arm in a decerebrate animal:

Importantly (for reasons I'll explain in a second,) it appears that the arm movements were initiated, but not sustained by the stimulation. We can tell the difference because the "reaching" movement continued through to completion even when it began slightly after the experimenters stopped stimulating the arm. This shows that the brief stimulation started a motor process that was maintained by the intrinsic neuromuscular system of the arm. The authors also found that similar movements could be elicited in amputated arms by "tactile stimulation of the skin or suckers." After a brief analysis of the kinetics of the evoked movements, the authors conclude that they, like those of intact animals, are caused by a propagation of muscle activity down the arm.

The authors' conclusion:

          "The division between the central and
          peripheral levels of the octopus motor control
          system resembles the hierarchical organization
          of motor control systems in other
          invertebrates and vertebrates, even
          though in the octopus it uniquely serves as
          an important component in a goal-directed
          voluntary movement rather than in rhythmical
          or reflexive behaviors."

The peripheral nervous system of the octopus appears to play a much greater role in the programming of movement that does the peripheral nervous system of vertebrates (which can only independently control simple reflexes and some other involuntary movements like peristalsis), even to the extent that it can execute complex movements (like reaching as if to grasp) all by itself. That propagating wave of muscle activity isn't coordinated by the central nervous system, like coordinated movements are in humans; rather, it's coordinated by the nervous system intrinsic to each arm. This is convenient for the octopus because it means that it generally does not need to keep track of its arms (that is, it's central nervous system doesn't have to spend a lot of resources monitoring and controlling them) because they largely take care of themselves. It's a good solution to the problem of having a large number of incredibly flexible appendages.

The exact extent of the arm's abilities to coordinate their own motor activity, as well as activity between arms, remains to be uncovered by more and more detailed experiments on a variety of types of movement, but the general conclusion seems pretty solid to me, and fits nicely with what we know about the neuroanatomy of the octopus. It would also be interesting to see the results of similar studies in other cephalopods. I have a sneaking suspicion that one could relate the extent of the peripheral nervous system's "motor autonomy" from the central nervous system to the complexity of arm movement required by a given species' lifestyle. It would be a neat idea to explore (if I had a laboratory on the Italian coast and a million-dollar grant to study squids. I can dream, right?)

There's one more article I wanted to cover here, but I don't have time at the moment, and I want to get this up tonight. It's by the same group, and it applies what the previous studies showed to explain the way that octopuses retract their arms after they have grasped their target. Hopefully I'll have a shorter post on that before the end of the weekend.

As always, thanks for reading!

Sumbre, G. (2001). Control of Octopus Arm Extension by a Peripheral Motor Program Science, 293 (5536), 1845-1848 DOI: 10.1126/science.1060976

Gutfreund Y, Flash T, Fiorito G, & Hochner B (1998). Patterns of arm muscle activation involved in octopus reaching movements. The Journal of neuroscience : the official journal of the Society for Neuroscience, 18 (15), 5976-87 PMID: 9671683

Graziadei, P.P.C. (1971). The nervous system of the arms. pp. 44-61 in Young, J.Z. The Anatomy of the Nervous System of Octopus vulgaris. Oxford : Clarendon Press.

So, enough about me...

2010-07-21T00:54:00.001-04:00

I've been writing this blog for about 3 months, and it has been an immensely rewarding experience. I've learned a great deal about all sorts of topics, had a chance to develop my writing skills, and enjoyed the virtual company of many wonderful science bloggers (almost all of whom are far more qualified than I, and whom I am very grateful to be able to observe and learn from.)

I assume that I've developed a small regular readership, as my traffic-tracking service indicates that I have between 5 and 20 returning visitors each day (depending on how recently I've posted.) I figured I'd take this opportunity (as sleep doesn't seem to be working out for me, at the moment) to probe your minds for a minute, both to satisfy my own curiosity and to help me figure out how I should be running this thing. If you have a second, please leave your responses to these questions in the comments:

Who are you? Why do you read this blog? What do I do right as a blogger, and what do I do wrong?

Thanks in advance for your help!

I'd also like to use this post to offer to trade articles with anybody who might be interested. I'd love to have some guest posts on here. I'd also like to try my hand at writing about something besides cephalopods (I have lots of other interests, I promise!), but I am not ready to maintain more than one blog at the moment, and I've decided to keep Cephalove firmly on topic. Send me an email or leave me a comment if you're interested.

Links: 3rd Edition

2010-07-20T11:36:00.002-04:00

It's time for some links! I'm working on some posts about cephalopod statocysts (to continue my coverage of sensory systems,) but in the mean time, here's what's going on (cephalopod-wise, mostly) on the web. There are some really funny news items this week.

An article at Deep Sea News makes the argument that Paul the octopus is actually psychic; at least as far as we can tell by current statistical standards.

Speaking of our friend Paul, he has officially reached internet stardom: Parry Gripp has written a song about him.

Another brand-spanking-new article from the same site addresses the possibility that pharmaceutical waste can alter marine ecosystems.

I recently lam-blasted the way popular media talks about the Humboldt squid. Over at Thoughtomics, this article exposes another sciency media frenzy for what it is: crap.

A burglar in Reno, Nevada decided to mess with his victims in a very creative way: by microwaving a squid. Seriously.

A new Syfy channel original movie, Sharktopus, gives us a vivid picture of what life would be like if half-shark, half-octopod monsters roamed the sea. And I though Lifetime movies were bad...

Apparently, email spammers are trying to sell people squid now. Does this mean that Viagra and pornography are no longer profitable? Let's hope that this ushers in a new, more creative era of spam marketing.

North Korea has started leasing squid fishing rights to China. The arrangement brings income to North Korea and supplies the strapped squid market in China. I find fishery management interesting, if only because it's so critical to ocean ecology.

Finally, this UK man is charged for possessing squid pornography (and child pornography, but that's not interesting enough for a tabloid headline.) It's apparently a criminal offense in the UK to have photos of somebody having sex with a dead squid. My favorite line of this story: "Prosecuters amended the charge when it was admitted it could have been an octopus in the picture." Oh, it was an octopus? That's a different story.

I wish I could make this stuff up.

The Myth of the Humboldt Squid

2010-07-20T02:27:00.001-04:00

I recently got a request (thanks to arvindpillai at Fins to Feet) to do a post on the shoaling and predatory behavior of Humboldt squid, Dosidicus gigas (also known as the Jumbo squid, and by those who don't know any better, the giant squid.) I decided that this would be a good thing to do, because I hadn't read much about the predatory behavior of D. gigas. So I spent a week searching the literature for scientific studies on Humboldt squid predatory behavior, and guess what? I still haven't read much about it!

It turns out that there is very little known about the behavior of these squid. The paucity of our ethological knowledge of them is shocking to me, given the disproportionate attention to this species in popular media. I've seen at least one budding cephalopod enthusiast become intrigued by stories about this species to the extent of obsession, and it's not hard to see why. Somehow, these squid have gained a reputation as fierce predators that are so bloodthirsty as to be regularly deadly to humans. As such, popular TV shows and news magazines have run numerous stories about them, usually finding one or two divers who have (presumably) had experience with these squids (or at least heard stories about them) to expound on just how ferocious and aggressive they are. Invariably, some sensational quip (that is almost always unsupported by scientific literature because, well, that literature does not exist) is used to drive home just how scary these squid are:

"It has probing arms and tooth-lined tentacles, a raptor-like beak and an insatiable craving for flesh -- any kind of flesh, even that of humans," says Pete Thomas in "Warning lights of the sea".

Mike Bear, an otherwise anonymous diver from San Diego is quoted in this article as saying "I wouldn't go into the water with them for the same reason I wouldn't walk into a pride of lions on the Serengeti."

“The Humboldt squid is a voracious predator that will eat anything it can get its tentacles on,” says Kelly Benoit-Bird, an oceanographer, quoted by Mark Floyd in this piece.

With all the hubbub, these guys must be pretty dangerous, right? The stuff of nightmares, even! I mean, just look at this bloodthirsty monster!

Oh wait, it's kind of cute, isn't it?

This is the myth of the Humboldt squid: that they are first and foremost dangerous, indiscriminate killing machines. This is, frustratingly, the first (and often only) piece of information that is repeated about them in any given article. But what's the real story?

Let's put this in perspective by considering the case of sharks, another predatory ocean-dweller that has been sensationalized as being imminently dangerous to humans (remember "Jaws"? It was pretty silly, but a lot of people took that era's shark scares seriously.) Fatal shark attacks on humans are documented somewhat regularly, and are discussed (albeit infrequently) in the scientific and medical literature (ie. this study on fatal shark attacks.) I cannot find a single verifiable record of a fatal squid attack on a human in the medical literature (admittedly, I have only searched 3 online databases and Google scholar - I might be missing something.) The closest thing I can find are fisherman's accounts in popular media of other fisherman's stories about hearing about people being killed by Humboldt squid. Keeping in mind the D. gigas is a rather common animal, is fished for sport by casual fishermen, and is usually encountered in large groups (the commonly cited size is 1000-1200 animals per shoal, but I can't find anything peer reviewed to support this,) it looks like these squid are all but harmless, given how often it is encountered by lay-people and how few (if any) fatal encounters there have been.

This is not to say that I don't think it's possible that a Humboldt might kill a human someday; they are clearly aggressive, as several documented, non-fatal "attacks" on humans show. I have to say, though, that the media attention that is payed to them (which is probably the reason why so many people are "interested" in them) is really a nuisance. By making inflated claims about a species that we have little behavioral research about, media outlets encourage people to accept hearsay and horror stories as if they were biological fact. These stories also draw attention away from other squid species whose behavior is very well characterized (ie. L. Pelalei) which might be better used to teach the public basic information about cephalopods. Finally, by attempting to catch people's eye using gorey stories, such articles serve to blind people to really learning about these animals by focusing on how "bloodthirsty" and "horrifying" they are - an effect that can't be any good for conservation effforts. I recognize that most people want an entertaining story rather than a dissertation out of their media, but this obvious bias in popular media coverage on this particular variety of cephalopods just bugs me because it is so pervasive and one-sided.

Now that I'm done ranting and raving, and have hopefully convinced you that D. gigas might not be the single-minded killers that they are often portrayed to be, I'll try to get at the facts (that is, our very limited scientific knowledge) of this species. Most of the research that has been done on them has been about their interactions with predator and prey species and their movement through their habitat, rather than their ethology. This is because they are an important species in the study of ocean ecology. They can be caught regularly in relatively large numbers throughout their range with little risk of damaging populations - this is uncommon among large predators, which tend to be much more rare than those lower on the food chain. They are also suitable to be tracked using remotely monitored tags (as per Markaida et al. 2005) which are difficult to attach to less robust cephalopod species. As such, they are convenient and informative to study when trying to learn about how oceanic food chains work.

So, what do we know about their feeding habits? For one, we know that, as Dr. Benoit-Bird was trying to point out, that Humboldts are active, generalist predators, eating (according to Nigmatullin et al.) all manner of prey including "cepepods, hyperiid amphipods, euphausiids, pelagic shrimps and red crabs... heteropod molluscs, squid, pelagic octopods and various fishes." The authors also note that D. gigas is commonly cannibalistic, a facet of their predation that has probably contributed to their mythological status. They are especially cannibalistic during squid jigging sessions, when they are excited by bright lights and surrounded by their injured conspecifics. They feed near the surface mostly during the night, especially at dusk and dawn, and spend their days deeper in the water column (200-400m deep), as was shown by a radio tracking study by Gilly et al. in 2006. They can vary their diet depending on changes in their environment, showing an adaptability that no doubt contributes to their great abundance (Markaid and Sosa-Nishizaki, 2002). Interestingly, recent ecological research has shown that their range has recently expanded from its historical locus in the equatorial Pacific ocean off of Central and South America to extend to the Pacific Northwest (as described by Cosgrove and Sendal, 2005, Zeidberg and Robison, 2007, and Field et al., 2007), possibly due to their unique ability to deal with hypoxic conditions that other predatory species cannot. The squid can retreat into deep water with very little oxygen in between daily trips to feed at the surface, and thus avoid predation by other species such as Mako sharks (Vetter et al, 2008).. On an unrelated note, if I were a squid researcher named Zeidberg, I'd just go ahead and change it to "Zoidberg". It's too perfect.

There is dissappointingly little to say about the shoaling and predatory behavior of D. gigas. If there are any glaring omissions in my coverage of the topic, please let me know; however, I think I found most of what's in the scientific literature. Basically, we know that they form large shoals, and that they are generalist predators. More detailed information than that on the behavior of this species will have to wait for a new generation of adventurous ethologists. Until then, I'll be turning back to those species of cephalopod about which we have enough information to draw useful conclusions about behavior. Perhaps someday the sort of experiments that have been done in smaller, more easily handled species will be done in D. gigas, but until that happens, I will probably stay mostly silent about them in favor of covering studies on less glamorous species in detail.

Please excuse me if it seems like I've rained on the proverbial parade. Excuse me also for not getting into the methods of the studies that I've cited. I encourage you to peruse them, but I opted to cover a greater area of research superficially rather than getting in depth about any specific finding in this post, so that I could adequately sum up the state of scientific knowledge of the Humboldt squid. To lighten the mood, I'll leave you with one more quote about the Humboldtl, by the realtively famous undersea cameraman, Scott Cassell, who has spent much of his professional career filming these squid (including a documentary titled "Humboldt: the Man-Eating Squid") and is quoted in this piece by Tim Zimmermann: "They are one of the most beautiful creatures, and they just happen to be lethal... There is no life form on this planet more alien than a Humboldt squid." I guess I didn't realize that any life form on this planet was "alien", given that they all evolved here. Oh well - what do I know?

Thanks for reading!

Gilly, W., Markaida, U., Baxter, C., Block, B., Boustany, A., Zeidberg, L., Reisenbichler, K., Robison, B., Bazzino, G., & Salinas, C. (2006). Vertical and horizontal migrations by the jumbo squid Dosidicus gigas revealed by electronic tagging Marine Ecology Progress Series, 324, 1-17 DOI: 10.3354/meps324001

JOHN C. FIELD, KEN BALTZ, A. JASON PHILLIPS, & WILLIAM A. WALKER (2007). RANGE EXPANSION AND TROPHIC INTERACTIONS OF THE JUMBO SQUID,
DOSIDICUS GIGAS, IN THE CALIFORNIA CURRENT CalCOFI Rep., 48 : http://swfsc.noaa.gov/publications/FED/00859.pdf

James A. Cosgrove, & Kelly A. Sendall (2005). First Records of Dosidicus gigas, the Humboldt Squid
in the Temperate North-eastern Pacific Archives of the British Columbia Royal Museum

Unai Markaida, Joshua J. C. Rosenthal, & William F. Gilly (2005). Tagging studies on the jumbo squid
(Dosidicus gigas) in the Gulf of California, Mexico Fisheriy Bulletin, 103, 219-226

Markaida, U., & Sosa-Nishizaki, O. (2003). Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico Journal of the Marine Biological Association of the UK, 83 (3), 507-522 DOI: 10.1017/S0025315403007434h

Nigmatullin, C. (2001). A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) Fisheries Research, 54 (1), 9-19 DOI: 10.1016/S0165-7836(01)00371-X

RUSS VETTER, SUZANNE KOHIN, ANTONELLA PRETI, SAM MCCLATCHIE AND HEIDI DEWAR (2008). PREDATORY INTERACTIONS AND NICHE OVERLAP BETWEEN MAKO SHARK,
ISURUS OXYRINCHUS, AND JUMBO SQUID, DOSIDICUS GIGAS, IN THE CALIFORNIA CURRENT CalCOFI Rep., 49

Zeidberg LD, & Robison BH (2007). Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proceedings of the National Academy of Sciences of the United States of America, 104 (31), 12948-50 PMID: 17646649

Byard RW, Gilbert JD, & Brown K (2000). Pathologic features of fatal shark attacks. The American journal of forensic medicine and pathology : official publication of the National Association of Medical Examiners, 21 (3), 225-9 PMID: 10990281

I know these citations are sloppy - for some reason, I'm having some trouble working with the ResearchBlogging citation generator. I promise I'll fix it before next time.

Short and long-term memory in cephalopods

2010-07-13T00:03:00.002-04:00

          I've heard the assertion that octopuses have short- and long-term memories several times in the past few days, mostly in discussions of the ethics of eating octopuses prompted by ethical questions raised about Paul, the famous German octopod. It's interesting to me what these people don't say - that they think that having a multiphasic memory process makes octopuses worth not eating (because, well, people have multiphasic memories, and you wouldn't eat them, would you?!? Sicko.) While I don't think that memory capacity of an animal is associated in an uncomplicated way with its ability to suffer or its moral status, it seems to me like a nonetheless interesting question. I'm almost sure that most of the people who use (read: copy and paste) this bit of information to support their beliefs have very little idea of what sort of research is behind it. Let's face it: developing a working knowledge of behavioral research on cephalopods is something that just isn't on most of the public's mind. In fact, until I began writing this blog, I had very little knowledge of the subject. I plan to set the record straight, so that internet users need never make an unfounded or unqualified statement about memory processes in cephalopods again (a lofty goal, huh?)

          If you don't know octopus neuroanatomy very well (and who does?) you might want to check out the figures in this post. I'll be talking about the vertical and superior frontal lobes of the octopus brain, and I know it sometimes helps to be able to visualize things like that when you're reading about them. Just so that it's clear: the term "biphasic memory" means that the memory system in question has two discrete parts or processes (ie. short-term and long-term memory.) A monophasic memory would have only one process, so that memories would last for a certain amount of time and then fade similarly in all circumstances. A multiphasic memory system (which could be biphasic, triphasic, or more) is a general term to describe memory systems that are clearly more than monophasic, but are not completely characterized yet - and no memory system is. Now, on to the research!

          J. Z. Young, that demigod of cephalopod neurobehavioral research, published one of the few papers I could find on this topic back in 1970, following up on his earlier work on the subject. In it, he investigated the development of short and long term memory in O. vulgaris (I assume - he doesn't actually mention what species he uses in this paper, but he almost always used O. vulgaris) as well as the role of two brain areas in memory, the median superior frontal lobe (MSF) and the vertical lobe (VL). To do so, he performed surgeries to remove one of these two areas of octopuses' brains and put them through a learning task. In this task, octopuses were trained to either attack a rectangle (rewarded with a piece of fish) or withhold attacking a crab (which was punished with electric shock.)

          It turned out that octopuses whose vertical lobes had been removed were greatly impaired in learning to attack the rectangle. Young explains this by claiming that the vertical lobe is involved in short-term memory, and that the acquisition of stable behavior day-to-day was impaired because the animals without vertical lobes could not remember events long enough for the training to be effective. The animals without median superior frontal lobes, however, learned the task just fine, but were impaired in their long-term retention of it., suggesting that the MSF lobe might have some role in retaining learned information. Interestingly, Young also found (in other experiments) that removing the vertical lobe after a task was learned resulted in a greater retention of the task. These results suggest that the vertical lobe plays a role in the updating of memory stores, but is not absolutely essential for the recall of memories.

          His results from the attack-withholding task were less clear, but they suggest that animals with lesions, especially those with vertical lobe lesions, were less consistent than intact animals in learning not to attack a crab after being shocked each time they attacked it.

          Basically, Young argues (on the basis of this and some of his other experiments) that octopuses have a memory system that can be disrupted in more than one way; that is, it is possible to dissociate memory acquisition from long term retention, just like in vertebrates. For the most part, more current research has agreed with his position, as we'll see in this next paper.

          Moving forward (past a lot of great research that I'll skip over for the sake of brevity) to 2008, Shomrat et al. used electrophysiological methods to test this hypothesis. Before we get into their methods, let's look a bit more closely at the system that we are talking about (this figure is from Shomrat et al. (2008)):

          On the left is a sagittal slice of the supraoesophageal (over-the-oesophagus) mass of the octopus brain. On the right is a diagram of the memory system in question. Sensory information flows into the MSF from the arms and eyes before being sent along to the VL. The VL neurons in turn send out information encoding attack. It's been established that long-term potentiation (LTP) can occur in this area of the octopus brain, and this is a likely mechanism for the formation of memories in octopus (I blogged about this here - check it out if you need a little more background.)

          The authors' procedure went as so: O. vulgaris who had already been trained to attack a white ball either had their MSF tract cut (at the dashed line in each image,) severing the sensory input to the vertical lobe, or this tract was stimulated, causing LTP at the synapses indicated in the figure. Shortly after the procedure, the animals were trained to avoid a red ball through electric shock. It was found that animals with severed MSF tracts were slower than controls to learn to withhold attack, while animals in whom LTP was induced were quicker. This is all well and good - it confirms what we already thought about the role of the vertical lobe in acquiring memories in the octopus. The really important result from this paper came when the authors tested the octopuses a day later. It was found that both MSF tract transection and LTP induction impaired recall after 24 hours. So even though stimulation of the MSF tract improved short-term memory (presumably by hyper-activating the memory system in the vertical lobe,) it impaired long-term memory. This suggests that these two processes are not identical; that is, that octopuses have discrete and dissociable short- and long-term memory circuits. This general finding has been replicated in cuttlefish (see my post on cuttlefish memory) and nautiluses (Crook and Basil, 2008).

          Unfortunately, that's just about all that we know at this point: that cephalopods appear to have biphasic memories, meaning that the behavioral evidence of short-term memories can be dissociated from that of long-term memories. This is hardly (by itself) a basis on which we can imply any sort of consciousness or advanced cognitive capacity, as animal-rights supporters who mention this fact seem to imply.

          In interpreting these results in the context of our knowledge of cephalopods as a whole, we should keep in mind what is meant by short- and long-term memory in humans. Short-term memory is what happens when newly learned information is bouncing around the cortex somewhere, being continually processed but not permanently encoded somewhere. These memories will disappear if they are not rehearsed (or otherwise actively retained). Long-term memory has been (relatively permanently) encoded into neural circuits, so that it can be retrieved after periods when it has not been actively processed in short-term (or working) memory circuits. These processes have been studied intensely in humans, and can be precisely because we have a complex cognitive system build around them (or on top of or parallel to them, depending on who you ask) that we can access. As of yet, we don't have the experimental techniques to assess exactly how "human-like" or "vertebrate-like" cephalopod memory systems are, because we can't study them in nearly as much detail as language-based and other cognitive tasks allow us to in humans. Thus, making any strong conclusions about the nature of cephalopod memory other than that it appears to be multiphasic (with no implied "and-so-cephalopods-are-smart-like-people") is untenable.

          Lastly, I find it frustrating that animal rights activists use our (very primative) knowledge of cephalopod memory systems to try to support their position that eating cephalopods is wrong. Not only is it an inconclusive (what does memory have to do with suffering and morality?) and nonspecific argument (did anybody think that ungulates, swine and birds don't have complex memory systems?), but it misses some of the big points that the animal rights movement has taught us. First of all, it implies that cephalopods are somehow special because they are intelligent and human-like. However, having compassion for animals explicitly demands that we not judge their worth by analogy to our own abilities - this has proved to be an attitude that encourages cruelty to animals simply because we are ignorant of them and their behavioral and cognitive capacities. If we didn't know about cephalopod memory systems, would they still be worth defending from fishing and consumption as food? Hopefully, the answer is yes - so why try to use this (admittedly inadequate) argument now that we conveniently have information that appeals to one's emotional predispositions? I find this to be irresponsible and counter-productive, as it diminshes the credibility of other, more valid arguments against the consumption of cephalopods (or any animal, for that matter) that animal rights activists might use.

          Sorry if this was a bit heavy on editorial material. Being very concerned about animal welfare myself, I get annoyed when people make the cause look stupid by saying things that are ill-informed, ill-reasoned, or just plain wrong. Although I wish that people would stop killing cephalopods for food, spinning information to try to get people to agree with a point is dishonest, and at best a very poor strategy for debate, as there's bound to be at least one attentive person on the other side who will point out that you're not being true to the facts - and nobody will listen to you after that.

Thanks for reading!

SHOMRAT, T., ZARRELLA, I., FIORITO, G., & HOCHNER, B. (2008). The Octopus Vertical Lobe Modulates Short-Term Learning Rate and Uses LTP to Acquire Long-Term Memory Current Biology, 18 (5), 337-342 DOI: 10.1016/j.cub.2008.01.056

J. Z. Young (1970). SHORT AND LONG MEMORIES IN OCTOPUS AND THE INFLUENCE OF THE VERTICAL LOBE SYSTEM Journal of Experimental Biology (52), 385-393

Crook, R., & Basil, J. (2008). A biphasic memory curve in the chambered nautilus, Nautilus pompilius L. (Cephalopoda: Nautiloidea) Journal of Experimental Biology, 211 (12), 1992-1998 DOI: 10.1242/jeb.018531

Antarctic octopus venom

2010-07-10T01:22:00.002-04:00

In my recent quest to find new, cutting-edge research on cephalopods, I've come across some neat stuff (check out this post on the perception of polarized light by cuttlefish - it's one of my favorite new cephalopod research topics!) The study I'll review here is outside of my field of relative expertise, but it's so neat and so new that I couldn't resist writing about it. It's good to step out of one's comfort zone every once in a while, right?

An international team of researchers hailing from Norway, Australia, and Germany has published a study on the venom of Antarctic octopods (more accurately, it is being published, though it hasn't hit the presses yet.) The team investigated the biochemical properties of extracts from the salivary gland of four Antarctica octopus species and wrote up their results in Venom on ice: First insights into Antarctic octopus venoms (2010).

Here is their image of the posterior salivary glands of an octopus, from which the authors collected all of their specimens:

These glands produce a variety of compounds, notably venom and digestive enzymes. The venom of temperate-water octopuses has been studied in the past. Never before, however, has venom been studied in an octopus that lives in below-freezing temperatures, conditions under which the enzymes in most venoms work very poorly if at all. To begin to understand the role of venoms in the lives of Antarctic octopuses, the team collected and tested venom from four octopus species collected off the Antarctic shore: Adelieledone polymorpha, Megaleledone setebos, Pareledone aequipapillae, and Pareledone turqueti. Here are images of some of their specimens:

Cute, aren't they? Octopods always are! Anyways, back to the biochemical assays.

First, the authors tested the extracts for alkaline phosphatase (ALP) activity. ALP is an enzyme that is in spider and snake venom that is thought to help immobilize prey items. Second, they tested for Acetylcholinesterase (AChE) activity. AChE breaks down acetylcholine, a neurotransmitter, potentially acting as a toxin by disrupting neuromuscular function. Third, the extracts were tested for general proteolytic activity using casein. Fourth, an assay for secreted phospholipase A2 (sPLA2) was performed. sPLA2 is found in cone snail and snake venome, and contributes to the effects of venoms in a variety of ways. Finally, the researches assessed whether the venoms showed haemolytic activity, which is a common marker of the general toxic activity of venoms. Taken together, these results should begin to characterize the putative venom of each octopus species. After all of this, the researchers reviewed what is known about the morphology of the mouthparts of the octopuses, as well as their feeding habits, and tried to relate these to their biochemical findings.

Whew.

So, after all of that, what did they find? Here are their results(takes another deep breath):

Venom from all of the species had some ALP activity. Interestingly, however, when ALP activity was tested at 0 Celsius and at 37 Celsius, venom from 3 species of octopus (A. polymorpha, M. setebos, and P. turqueti) had higher ALP activity at the lower temperature! This is a significant finding because it suggests some sort of modification of the proteins responsible for this activity to function optimally at a lower temperature. This lends some weight to the theory that the use of venom has been important enough to the survival of Antarctic octopus species that they have evolved enzymes to work under conditions where most enzymatic toxins would not. In the other tests, an essentially similar pattern of results were found, except for the AChA activity assay. Little AChA activity was found in any of the species, although the results of the assay were poor enough (that is, inconsistent) that they were not included in the paper. Interestingly enough, although all of the species had a few potentially functional toxins in their venom, most of them showed only weak haemolytic activity. Only one extract (from P. turqueti) showed strong haemolytic activity.

The relation of venom activity to morphology and diet that the authors attempted to point out appears to be weak (or at least difficult to point out given their sample,) as it is mentioned that few clear venom-related adaptations in diet or anatomy were present in these octopus species. A. polymorpha is noted to have a very large salival gland and a narrow beak, which the authors suggest might be an adaptation associated with the use of venom as a primary means of catching prey (as opposed to having powerful jaws to physically overpower the prey.) This species feeds mostly on amphipods and polychaete worms, and so it's unclear why it would rely on venom to subdue such (relatively) easy going prey instead of retaining a more varied diet. In any case, though, this is one of those papers that, being exploratory, raises many more questions than it answers - that's the kind I like!

What I find most interesting about this work is that it begs questions about the evolution of octopus venom. How quickly could the octopus populations move into cold water? Was this limited by the evolution of venom enzymes, or did that evolution occur after some quicker relocation of the species which left their warm-water-adapted enzymes useless? Did A. polymorpha's ancestors have a specialized diet before they became Antarctic, or is that only a successful feeding strategy in the Antarctic environment? The world may never know (although I hope we do, someday!)

Thanks for reading!

Undheim, E.A.B., et al. (2010). Venom on Ice: First insights into Antarctic octopus venoms Toxicon

Kissing an octopus and other diversions

2010-07-09T22:25:00.001-04:00

In Washington, a Pacific Giant Octopus is released into the wild with a kiss! I don't know that I'd kiss a cephalopod, but the picture of science center directer Patrick Mus doing it is pretty darling.

The German branch of PETA released a statement demanding that Paul the (psychic) octopus be released into the wild, claiming that octopuses are "capable of complex thought processes, they have short- and long-term memories, use tools, learn by observation, show different personalities and are particularly sensitive to pain." I'd argue that their first point is highly dependent on the definitions of "complex" and "thought processes", their second point says little about the intellectual capacity of an animal, their third point is contentious even among those who care, being supported by a very few examples, their fourth point is based on one study that (as far as I know) has not been replicated, their fifth point is only supported by anecdotal evidence (and "personality" is a very loosely defined term,) and their last point (again, as far as I know,) has never been specifically investigated. Nonetheless, it makes good news.

In the town of Whyalla (where our heroes from the last link post were arrested for stealing cuttlefish,) cuttlefish are an important tourist trap, as well as possibly being a special, isolated genetic pool. If I were in Australia, I'd go see them.

In the most exciting recent news story (in my opinion, at least,) a deep sea squid's penis is seen in action. Really. No, I'm not joking. Just click it.

Partially in response to the whole Pepsi-blog incident at Science Blogs (which seems to have mostly resolved pretty quickly,) Adam Bly, CEO of SEED Media Group has started a new blog, Science is Culture. In response to the fiasco, I've updated my blogroll to link to the new locations of those who left Science Blogs.

I've also updated my format and added some new folks to the blogroll. I'm working on a few posts at the moment (including a cephalopod reading list with reviews,) so stay tuned!

Getting to know some squids

2010-07-08T13:23:00.001-04:00

Time for a treat! The last post was about the ecological significance of retinal organization in coastal and oceanic squids. The study I reviewed used 5 species of squid, and I thought it would be nice to take a moment to get to know the research subjects.

Euprymna morsei

This little guy is commonly known as a Mimika bobtail squid. E. morsei is benthic (meaning bottom-dwelling,) and forages for crustaceans in sandy and muddy seafloors all around western Asia and Indonesia.

Sepioteuthis lessoniana

Also known as the bigfin reef squid, S. lessoniana is a coastal squid that is found throughout the South Asian and Australian coastlines. In this video, we see a group performing courtship rituals and laying eggs.

Todarodes pacificus

Also known as the Japanese flying squid, this oceanic squid is an important fishery in the pacific. I'm not sure where this video clip is from, but they sure are cute!

Eucleoteuthis luminosa

I could not find a video of this guy, but here's an image (by Michael Vecchione, originally uploaded on www.TOLweb.org.) The distinctive feature of this squid is the photophores (which look white in this image,) especially the two long ones that run the length of the mantle.

Thysanoteuthis rhombus

T. rhombus (also called the diamondback squid) is a large squid that is found throughout the world. This (slightly depressing) video shows two specimens in a tank. Note the large, muscular fins on either side of the mantle.

Thanks, Youtube, for bringing squids to us all.

Squid Visual Ecology

2010-07-08T12:46:00.000-04:00

Keeping with the theme of sensory systems, I thought I'd review some newer research on squids.

While searching for recent cephalopod neurobehavioral research (which is pretty scant) to blog about, I came upon Makino and Miyazaki's study on the distribution of retinal cells in the retina of squids. I have a soft spot for visual neuroscience that I picked up from working with my first research advisor, who works on the visual system of frogs. In any case, this is a good paper (although it was a bit hard to get my hand on,) and I'll review it here.

The study aims to look at the distribution of retinal cells in the retinas of a variety of squid species. This has been done in several vertebrates, with the general finding that animals have retinas that perform well for their lifestyle. Seems pretty simple, right? For example, fish who live in "closed" environments have dense retinal ganglion cells (RGCs) in the area of the retina that sees light from directly ahead, while oceanic fish have a strip of high-density RGCs that stretch laterally across the whole visual field. Thus (to make a horribly crude generalization,) cave and reef dwelling fish have focused binocular vision, while oceanic fish largely lack this but have a greater ability to monitor their whole visual field, ie. for predators or food items.

In vertebrates, retinal ganglion cells are often mapped in this sort of study. By the time RGCs exit the retina, they are carrying visual information that is already processed into the very basic components of visual perception (namely, hue and tone contrast.) As vertebrates have complex retinas, it is also possible to map photoreceptors in vertebrate retina, or a variety of other types of cells (which might be more or less informative.) Cephalopods, however, only have one type of visual cell in their retina - the retinal cell (or rhabdomere.) So, the authors chose to map this. It is useful to keep in mind that this is not directly comparable to the mapping of retinal ganglion cells in vertebrates - it could be the case that the density of visual cells in an animal's retina is not always correlated with the importance of that piece of the visual field in further levels of visual processing. This problem is partially solved in studies on vertebrates by the use of RGCs, in which the processing of information from photoreceptors is already underway. With cephalopods, however, there is currently no way to probe this any deeper, and so for now it remains an assumption - albeit a pretty noncontroversial one - that rhabdomere density is correlated well with the relative importance (behaviorally and neurophysiologically) of portions of the visual field. (For more on cephalopod visual anatomy, check out my earlier post on cephalopod eyes.)

The image to the left shows cell counts (in retinal cells per mm) across the retinas of the 5 species of squid. I added color to this image to make it easier to see the distribution of cells. It's important to not that the colors are relative within each figure, and do not represent absolute cell density, which is shown as (difficult to read) numbers on the boundaries of regions. Also note the scale bars, which are 10mm in every image.

In terms of orientation, keeping things straight gets a little tricky (as it does with all cephalopods.) Dorsal-ventral orientation is pretty easy - remember that the lens of the eye inverts the light coming through it, so that the ventral part of the retina forms the top part of the visual field and the dorsal part of the retina forms the bottom part of the visual field. Anterior is the direction the squids' arms point in, so the anterior retina forms the posterior part of the visual field. The posterior retina is the part that forms the anterior part of the visual field. This is the part that is used when squids look forward to form a binocular image.

Using this data, the authors estimated the visual axes of the squids, based on the location of the highest density of photoreceptors. The visual axis is the general point of focus, which is known to be of utmost behavioral importance in vertebrates. When you follow a moving object with your eyes, you are keeping it in your visual axis. The location of an animal's visual axis is key to its visual ecology - many predators have forward facing visual axes so that they can see their prey accurately, while prey species often have very laterally oriented visual axes (think of rabbits and deer) so that they can monitor more of their environment at any given time. Thus, we'd expect that squids with different lifestyles have different visual axes, because they will be looking for food and predators in different places.

In coastal squid (E. morsei and S. lessoniana), the visual axis is directed downwards, presumably reflecting the importance of monitoring activity on the substrate that these species live on. In oceanic squid (T. pacificus, E. luminosa, and T. rhombus,) the visual axis is directed upwards, and the eyes have a much greater density of photoreceptors overall. I think the retinal cell density map of E. luminosa is especially interesting, because the concentration of cells on the extreme posterior edge of the retina suggests that binocular vision is disproportionately important to this species. The authors conjecture that this eye may be specialized to detect and track bioluminescence in the open ocean, but this is purely speculation.

These findings are important because they expand our knowledge of cephalopod eyes, which are a model evolutionary system. If we can begin understand the impact of ecology on the organization of visual systems (which is part of the emerging field of visual ecology,) we can generate a wealth of testable hypotheses about the ecological conditions that occurred during the evolution of differnt species eyes, as well as the other sorts of adaptations we might see in sensory systems as they diverge (or converge) during evolution. It's also a nice piece of evidence that our rather basic theories about visual ecology and the structure-function relationship of the visual system are largely correct. This is good to know, as we base an incredible amount of more complicated neuroscience research on these theories.

Thanks for reading!

Akihiko Makino, & Taeko Miyazaki (2010). Topographical distribution of visual cell nuclei in the retina in relation to the habitat of five species of decapodiformes (Cephalopoda) Journal of Mulluscan Studies, 76, 180-185 : 10.1093/mollus/eyp055

Cephalopod Links

2010-07-05T02:39:00.000-04:00

First things first: a few recent cephalopods in popular news media:

Paul, the German octopus, successfully predicted yet another World Cup match. An aquarium in Oberhausen, Germany had its animals place their bets on World Cup matches as a promotion, and the world discovered that Paul is the luckiest octopus to ever live.

In Australia, three men are arrested for stealing cuttlefish from a protected area of ocean. The town police consider selling the catch as food - failing this, they will bury it. I couldn't make this up.

In Oregon, researchers try to recruit fishermen to help them understand Humboldt squid population dynamics off the Oregon coast.

And some topical blog posts:

Marine Biologist William Gilley updates us on the progress of an expedition to study Humboldt squid in the Gulf of California.

A recipe for char-grilled baby octopus salad at Food Stories (this makes me sad, oh so sad, but I had to post it for the weirdness.)

Richard Ross gets very excited about a pair of Metasepia pfefferi getting it on (with video!) I have to say, of all the animal mating rituals one could watch, cuttlefish are pretty easy on the eyes. In all seriousness, though, culturing cephalopods is notoriously difficult, so this is probably a huge deal.

The Carnival of Evolution #25 is out at Culturing Science - take a moment learn about empathy in crows and all the other amazing things that the evolutionarily-minded blogosphere finds fit to write about. You'll be glad you did.

What the cuttlefish sees that you don't

2010-07-05T01:10:00.004-04:00

I thought I'd mix things up a little bit and take a look at some research on the sensory abilities of cuttlefish. Specifically, I'd like to take a look at an aspect of cuttlefish vision that has shown up in the literature recently (it's actually one of the few threads of cuttlefish research that seems to be active at the moment - the other ones I've noticed are memory and fishery ecology and management): the ability of cuttlefish to perceive polarized light. Polarized light is composed of photons that are all oscillating in the same plane - we cannot sense the polarization of light, but it seems to play some role in the lives of cephalopods and some other animals. For more info on polarized light, check out this explanation of polarization.

It has been known that cephalopods can respond to polarized light for some time - Wells did the work showing that octopuses can detect polarized light in the 1960's, and it's been studied in fits and spurts since then. In the late 1990's and early 2000's (from what I can tell,) it became a relatively hot topic among researchers who study animal communication, because it appeared as if cuttlefish might be able to use polarized light for some sort of intraspecific communication. A good though somewhat dated review of the topic is Shashar et al's Polarization Vision in Cuttlefish - a Concealed Communication Channel? (1996).

How can cephalopods see polarized light? It turns out that their photoreceptors are orientated at a variety of angles, so that incoming light will cause the most stimulation in photoreceptors that are oriented the "right" way. In unpolarized light, all of the cells would be pretty much equally stimulated - nothing unusual happens here. Upon being hit by polarized light, though, a specific population of retinal cells (those that are oriented in the proper direction) will be activated, and the animal will be able to see the polarization of light.

This is an image of cuttlefish (S. officinalis) photoreceptors (From Shashar et al 1996.) The lines are folds in the photoreceptor cells called microvilli. Notice how the two adjacent cells have microvilli at a right angle to each other - this is what allows cephalopods to see the difference between polarized and non-polarized light.

Detecting polarization can help a creature in a lot of ways. In a basic sense, it almost always helps an animal (especially one who, like the cuttlefish, is both a predator and a prey item) to have as much information about the environment. If sensing polarization allows the cuttlefish to know more about its environment at any given time, it's already a huge advantage. In fact, it has been shown that the perception of polarized light probably helps cuttlefish to catch certain prey that is difficult to see otherwise (see Shashar et al 2000.) But I mentioned the possibility of communication through polarized light - how does that work?

It turns out that iridophores, organs in the skin of cephalopods that reflect light, polarize that light to some extent. The anatomy of iridophores is such that they preferentially reflect light polarized in a certain plane. It is known that cephalopods, especially cuttlefish, have wonderful neural control over the pigment organs in their skin, which allows them to display such a dazzling array of colors and patterns. Cuttlefish might be able to manipulate the polarizing properties of their iridophores, adding another layer of complexity to their body patterns. Importantly, however, this would be a type of display that not everybody in the sea could perceive. Shashar's theory is that cuttlefish might use polarized light as a type of social signal, while still being able to maintain the camoflauge which is key to avoiding being eaten.

Shashar and friends did a few experiments to test this hypothesis: first, they observed cuttlefish during a variety of behaviors, and found that the polarization of light being reflected from the cuttlefish's arms varied with different behaviors in much the same way as their patterns of coloration. Polarized light is reflected from stripes on the arms and the area around the eye, as seen in this image from a review on the use of polarized light by cuttlefish by Mathger et al (2009):

The top image is a cuttlefish as seen by the human eye. The bottom image has been given false color, so that areas which reflect polarized light show up as green. On an unrelated note, cuttlefish sure are cute.

In addition to discovering the patterns of reflection of polarized light by cuttlefish skin, the authors found that cuttlefish respond differently to their own reflections when they view them through a filter that screens out polarized light. Specifically, they found that cuttlefish responded less noticibly to the disrupted image. While the authors declare that these findings are "fully consistent with the hypothesis that cuttlefish use controllable polarization patterns for intraspecific communication," they are also consistent with the more parsimonious explanation that cuttlefish don't respond to any stimulus made of non-polarized light as strongly as they do when it is at least partially polarized. While the theoretical argument presented in this paper is interesting, I think it's a bit too eager for what the data show.

Fast-forward to 2004: Boal et al. published a study called Behavioral evidence for intraspecific signalling with achromatic and polarized light by cuttlefish. In this study, they exposed cuttlefish (S. officinalis) to conspecifics (that is, other cuttlefish) through either a clear or a polarized light-blocking barrier. They found that only females responded differentially to conspecifics behind the polarization-distorting barrier, not responding to them at all (cuttlefish confronting each other unexpectedly often show some sort of postural and color change.) This was the only significant result that they found, and it is ambiguous in its interpretation. Again, it might simply be that a non-polarized stimulus is not very interesting to an animal who is used to seeing a world of polarized light.

So, do cuttlefish use polarized light to communicate? I'm not convinced. It seems as if everybody's hoping that it's true, but there's not any good data showing it to be so. I can't sum it up any better than Mathger et al. did in their 2009 review:

                 The fact that cephalopods can detect polarized light
                  and can also produce changeable polarized light
                  patterns in their skin begs the question whether
                 cephalopods communicate using polarized light signals.
                 The likely answer is that they do. Unfortunately, we
                 have little evidence to support this statement.

Thanks for reading!

Shashar N, Rutledge P, & Cronin T (1996). Polarization vision in cuttlefish in a concealed communication channel? The Journal of experimental biology, 199 (Pt 9), 2077-84 PMID: 9319987

Mathger, L., Shashar, N., & Hanlon, R. (2009). Do cephalopods communicate using polarized light reflections from their skin? Journal of Experimental Biology, 212 (14), 2133-2140 DOI: 10.1242/jeb.020800

Boal, J., Shashar, N., Grable, M., Vaughan, K., Loew, E., & Hanlon, R. (2004). Behavioral evidence for intraspecific signaling with achromatic and polarized light by cuttlefish (Mollusca: Cephalopoda) Behaviour, 141 (7), 837-861 DOI: 10.1163/1568539042265662

Shashar N, Hagan R, Boal JG, & Hanlon RT (2000). Cuttlefish use polarization sensitivity in predation on silvery fish. Vision research, 40 (1), 71-5 PMID: 10768043

Octopus Sensory Systems: Part 2.5

2010-07-03T02:02:00.002-04:00

This will be a quick one - I'll get back to the meat of my series on octopus sensory systems soon, but I wanted to write a post on this article because it struck me as cool (although it has a sort of sensational title.)

The article I'm talking about is Octopuses (Enteroctopus dofleini) Recognize Individual Humans (2010) by Anderson et al. in the Journal of Applied Animal Welfare Science.

The authors used an apparently elegant experimental design to test whether octopuses can tell people from one another across a long period of time - specifically, this is operationally defined as meaning that they could learn an association between a person's features and a good or bad stimulus. The experiment was conducted thus: eight octopuses were captured and habituated to their aquaria. Then, for 2 weeks, the octopuses had daily interaction with two people, one of whom fed them and one of whom (I'm not joking) poked them with a "bristly stick" (more specifically, "a length of PVC pipe with one end wrapped in Astroturf.") Then, the octopuses were tested to see if they reacted differently to the two individuals - presumably, if they remember who is who, they should show anticipatory behaviors related to eating or defensive behaviors in response to the appropriate person.

To get a better feel for the task, here are the experimenters, shown in an image taken from the octopus's point of view:

My problem with this experiment is that the term "individual" is usually used in cognitive research to mean some entity who is known to persist despite changes in their appearence in one specific sensory modality. When we get a haircut, our friends (and, usually, our pet dogs and cats) still recognize us - thus, we are individuals to them. However, if the visual stimulus of the two keepers didn't change from day to day (and they took pains to make sure that it didn't,) then this seems like little more than a complex visual discrimination task. It seems, judging from this image, that it would be pretty easy for an octopus to learn an association between, say, a shiny bald head and being jabbed with a stick, regardless of any ability she might have to recognize "individuals" in the cognitive sense. In any case, we are still a ways away from knowing whether octopuses can recognize individuals, and not just their constant visual features. With this in mind, let's consider their results.

It turns out that the octopuses learned to move away from the irritator and towards the feeder within two weeks. In addition, the octopuses showed fewer defensive coloration responses to the feeders than to the irritators, as well as changes in their respiration rate and the orientation of their bodies relative to the people. In sum, it looks like (in this test, at least) the octopuses succeeded in learning basic traits about the people interacting with them. I don't think that the title of the paper is fully supported, however - it's hard to make the case that this single study proves that octopuses can identify individuals in any sort of robust way.

This paper is pretty solid (besides its unfounded title,) although it begs a few questions:

1. How fine of a discrimination can octopuses make? Would they treat two bald men of similar stature the same? What if the subjects wear different clothes? How is this piece of research fundamentally different from Wells' experiments using simple visual cues? These are all important questions if we're actually going to claim that octopuses can identify "individuals" as opposed to simple visual stimuli.

2. What does this mean functionally to the octopus in the wild? Is this sort of ability actually used to identify predators and prey items? Do octopuses remember individuals of any species in the wild? Unfortunately, there is not much literature on the development of behavior in the octopus, so we can't know how much of octopus behavior is "instinct" and how much of it is based on learning (like that shown in this study.)

3. How does this generalize to other species of octopus? This study used Enteroctopus dofleini, the giant pacific octopus, because it is often kept in public aquaria. However, practically the whole body of research on octopus learning and vision has been done using O. vulgaris and, to a lesser extent, O. cyanea. We know that cephalopods have a pretty wide diversity of life-styles, so it seems important to me to know how these behaviors occur in different species if findings like this are going to be relevent to the rest of cephalopod research.

If nothing else, this study keeps alive my childish hope that Twister, the resident E. dofleini at the Niagara Falls Aquarium (which I visit almost weekly these days) will someday get to know me, if only in the most basic way.

Anyways, I hope this has been as fun for you as it was for me. Thanks for reading!

Anderson, R., Mather, J., Monette, M., & Zimsen, S. (2010). Octopuses (Enteroctopus dofleini) Recognize Individual Humans Journal of Applied Animal Welfare Science, 13 (3), 261-272 DOI: 10.1080/10888705.2010.483892

Octopus Predatory Behavior

2010-06-30T23:50:00.000-04:00

Having finished the last post with a short discussion of hunting/foraging behavior in the octopus, I figured I should do a lighter post with some fun video examples of cephalopod predatory behavior.

This is a short video of an octopus hunting (I don't know the species) by For the Sea Productions. The octopus catches a fish, apparently by spreading its web and feeling around. There's some great color-changing behavior here, too. It's hard to know how typical this behavior is, though, as it's obviously influenced by the presence of the person filming.

This is a clip from Deep Sea 3D (I think - I haven't seen the IMAX film, but that's what the caption says) showing a visually-provoked attack on a crab. I believe that the octopus here is a Pacific giant octopus.

Let's not leave out the other cephalopods! In contrast to octopuses, cuttlefish are primarily visual predators, who shoot out two long tentacles (these are tentacles proper - they are distinct from arms, which octopuses also have) to grab their prey.

This video was made by the California Academy of Sciences, and shows some adorable cuttlefish attacking crabs. I'm not sure what species they are. Again, you can see dramatic color changes as the animals become aroused.

This one, also by the CAS, shows a great slow-motion shot of the cuttlefish tentacular strike.

I'll end with one of my favorite videos of cephalopod predation:

Notice how the octopus turns mostly white and spreads its arms when the cuttlefish (most likely Sepia apama, although I'm not sure) approaches. This is called the deimatic display, and it's a defensive behavior seen in adult octopuses.

I feel obligated to warn anyone reading this that when you search "octopus eating" or similar strings on youtube, you are much more likely to find videos of people eating octopuses than octopuses eating anything. : (

Octopus Sensory Systems: Part 2

2010-06-30T22:58:00.002-04:00

In this post, I'll be talking about octopus tactile sensation. M. J. Wells and J. Z. Young did the classic experimental work on touch discrimination and learning in the octopus, although a bit of recent work has been done on the neurochemical basis of touch learning in the octopus (which I won't get into here.)

We'll focus on Tactile Discrimination of Surface Curvature and Shape by the Octopus (1964) by Wells. This was one of his later papers in a series on tactile learning in the octopus. Prior to this paper, Wells had already determined that octopus do not use proprioception to discriminate between objects (as a blindfolded person might do when trying to feel what an object is with his hand,) but rather use (almost exclusively) tactile cues about the object's shape. Let me explain.

It had been found that a blinded octopus could discriminate, on the basis of touch, between a sphere and a cube. This could be explained by the presence of some sort of proprioception that monitors the relative position of the octopus's arms in space - a system like this is known to exist in most vertebrates. However, Wells carried out a series of experiments that show that this is, if anything, a very subtle factor contributing to the octopus's ability to perform tactile discriminations. He found that octopuses learn to recognize the corners of a cube as variations in texture, which are encoded in reference to the extent that the suckers contacting the object are deformed. For example, a sucker that is on the corner of a cube will wrap around the corner, bending itself along a sharp angle. This information is encoded as some sort of distinct textural component, and sent along to the brain where it can interact with learning centers (which I'll discuss in a later post, hopefully) that will allow the octopus to remember what a particular texture means. Thus, if you teach an octopus to respond to a cube (meaning that you reward it with food when it grabs the cube, and punish it with electric shock when it grabs another object, say, a sphere,) this theory would predict that it would also respond to any object which induces a similar deformation of the suckers that contact it, such as a rectangular prism, or a thin rod. This is called a transfer experiment, because it tests the extent to which a learned task transfers to situations other than the one it was learned in. Indeed, Wells found that he could substitute a thin rod for the cube, and the octopus will respond to it as if it is a cube, presumably because the suckers contacting the rod are bent into a relatively sharp angle, as are those contacting the edges of the cube.

This evidence alone didn't quite clear up the question of how octopus performed touch discriminations, though - specifically, Wells' experiment with the cube, sphere, and rod did not use enough variations of form and dimension to really probe the mechanism of touch discrimination. Thus, Wells decided to conduct a number of transfer experiments between differently sized and textured cylinders in order to figure out the characteristics that octopuses use to identify objects by touch. The stimuli he used are shown here:

The numbers under the cylinder cross-sections indicate their diameter in millimeters. Wells notes that the octopus he is working with have suckers that are 10mm or less in diameter. Knowing this, one can gauge the approximate deformation of a sucker that the different cylinders would produce. For example, a 6mm wide cylider would induce a significant curvature in the sucker, whereas the 38mm cylinder would produce a very slight curvature, and thus would appear essentially "flat" to the octopus, if Wells' theory is correct.

Wells quantified this difference, and generally found that the greater the difference in curvature between two cylinders, the easier the discriminate was. This is great, but it doesn't rule out the proprioception theory. What if the octopus was actually "feeling" the position of the arm as it bent around the cylinder?

To solve this problem, Wells used the two cylinders shown at the bottom of Figure 1, those labeled 8* and 6*. These are "composite cylinders" were made of 7 small cylinders attached together, parallel to each other. If the sucker-distortion hypothesis is correct, then these objects should be treated as equivalent to small cylinders, because they create equivalent deformation of the suckers contacting them. If there is some mechanism that determines the shape or position of the grasping arm as a whole, then they should be treated as equivalent to the large cylinders, as they would require the same arm position and curvature to grasp as the 24mm and 18mm "simple" cylinders, respectively. In fact, this is what Wells found, although the experiments with compound cylinders did not adhere quite as closely to his proposed model regarding differences in curvature as did those with the simple cylinders. This might be expected, as the actual curvature experienced by the suckers is more variable with a more complex object.

Wells tested his idea further, by offering already trained octopuses P1 (which was grooved) and P4 (which was smooth.) Other than their texture, these objects did not differ at all. If sucker deformation is the basis of discrimination, we would predict that P1 feels most like a small-diameter rod to an octopus, as it would deform the suckers touching it greatly. P4, on the other hand, would feel like a large-diameter cylinder, because, well, it is. In fact, this is what Wells found - octopuses who were trained to take the larger diameter cylinder transfered this learning to the P1/P4 discrimination, and tended to take the smooth one. Animals who were trained to take the smaller diameter cylinder tended to take the grooved one.

Wells goes on to consider discrimination using a cube with rounded corners (which proves difficult for an octopus) and a cube/rectangular prism discrimination (which is also difficult,) but I'll let him tell you about those, as the point is amply made already.

What about the neuroanatomy of this system? Wells provides us with a figure showing the cross-sectional structure of a single sucker, including the receptors that putatively monitor mechanical distortion of the sucker (in the area labeled "2" at the rim of the sucker, towards the bottom of the diagram.

These receptors detect the mechanical forces from the object deforming the rim of the sucker, and then send this information to the ganglia of the arm. It seems likely (although I don't know that it has been tested) that these mechanoreceptors don't send their information the whole way to the central nervous system, but rather input into some processing system in the nervous system of the arms first. It would be interesting to know the minimum number of steps that information from the suckers might go through before it gets to the brain, because this would give a rough idea of how "processed" the sensation is before it gets to brain areas involved in learning. J. Z. Young's "Anatomy of the nervous system of Octopus vulgaris" didn't seem to have a clear answer for this question, so for the time being, I'll assume that it's unanswered (though, if I'm wrong, please point me to the literature.)

All in all, this might seem like a poor way to distinguish two things from each other. When you keep in mind the fact that octopus can't discriminate objects based on weight, either, even though it can adjust its posture and muscle tone to hold a heavy object, it would seem that the octopus has a sort of crappy tactile sensory system. We should ask, then: what does the octopus use this for?

When octopuses hunt, they often use a "blind" foraging strategy. They will pounce on an area where prey is likely to be with their arms and web spread open and then feel for prey. Alternatively, in rocky areas, an octopus might feel around in cracks for prey items. If the octopus feels a prey item, she grabs it, moves it towards her mouth, and eats it. It seems likely to me that the sort of touch discrimination that Wells trained octopuses with is not anything like what is demanded of them under ecological conditions. For one, it is likely that octopuses are sensitive to movement as well, as they must be able to discriminate between rocks and prey, both of which might be similarly textured. While hunting, an octopus also has other sensory systems to rely on. They're not primarily visual predators, but they can be, spotting prey and then attacking it (as they do when shown a live crab in an aquarium.) They also probably have chemoreceptors on their arms which could help them identify objects under their web. It doesn't seem to me as if lacking proprioceptive input to the central nervous system is at all a deficit to the octopus in its natural habitat.

Thanks for reading!

M. J. Wells (1964). Tactile Discrimination of Surface Curvature and Shape by the Octopus Journal of Experimental Biology, 41, 433-445

Octopus Sensory Systems: Part 1

2010-06-24T23:12:00.000-04:00

I've been reading M. J. Wells' book "Octopus", one of the "classic" works on the octopus. It was published in 1978, and is an essentially complete review of research on octopuses (primarily O. vulgaris, the common octopus) up until that time. It must have been fun to write the book, because he had done much of the research he cites (he cites at least 45 of his own papers in the book.)

Wells has published a large number of experimental studies on octopuses, and I've become very interested in his series of experiments dealing with the sensory capabilities of the octopus. In this series of posts (there will be 3 or 4, I anticipate, over the next week or two) I'll relate his findings, as well as others, about the sensory systems of the octopus. Forgive me if I write brief posts, as I'm rather busy writing other things at the moment.

I'll jump right into the octopus visual system. It's a good place to start, I think, because it's relatively easy for us to imagine what it's like to see, and so to think about octopus visual perception by analogy. It's relatively harder to imagine what it's like to control eight boneless arms (just like it's hard to think about what lateral line perception is like in fish - we simply do not have the anatomy to do it.) We'll move on to other senses in the next few posts. For now, though: vision! (For a brief look at the anatomy of the octopus visual system, check out my earlier post on that topic.)

Vision in octopus has been studies mostly through the technique of visual discrimination tasks. Simply put, an octopus is taught (via food rewards for correct answers and/or electric shocks for incorrect answers) to attack one visual stimulus and not another. The visual stimuli are then varied, and it can be discovered what stimuli the octopus can discriminate between. If two shapes are not discriminated between, they can be said to be perceptually identical (or at least perceptually similar) to the octopus. These experiments were widely done (well, as widely done as anything in octopus neurobehavioral research) throughout the 1950's, 60's and 70's, with some research still going (albeit at a slower pace and with shifting foci) today.

Octopuses, it turns out, can see pretty well. They can reliable learn to discriminate a variety of shapes, and can even tell the difference between rectangles that are identical except that one is rotated through a small angle relative to the other. An interesting deficit showed up after a variety of experiments were carried out, however - Octopuses are unable to recognize the difference between certain mirror images! For example, an octopus does very poorly when discriminating between two diagonally oriented rectangles, even though they are perpendicular to each other. This result is not too surprising, as this is the case to a greater or lesser extent with many vertebrates (to whom the octopus is often compared in its sensory abilities.) It is, however, remarkable in its extent - it seems like a big deal not to be able to make such a discrimination at all.

In any case, these experiments gave theorists of visual perception a lot of things to think about (I'll write about their theories later in the series.) What I find interesting about the whole series of experiments, however, is that they laid the groundwork for the investigation of the role of statocysts in octopus visual perception. Statocysts in cephalopods are like the vestibular systems in our ears: they are tiny, fluid filled chambers that contain hair cells which detect the movement of this fluid (see The Fine Structure of the Octopus Statocyst (1965) by V. C. Barber for a more complete description.) It appears that the main function of the statocysts is to help the octopus maintain its equilibrium by detecting changes in velocity as well as the direction of gravity. For example, an octopus whose statocysts have been surgically removed will move unsteadily and fail to make normal eye movements in response to the movement of its environment.

Under normal conditions, an octopus will keep its pupil slit horizontal, relative to the pull of gravity. However, when the statocysts are removed, the octopus will no longer be able to do this; her pupils will be fixed relative to her body position, and will not adjust to remain horizontal. This is a figure from Proprioception and Visual Discrimination of Orientation in the Octopus (1960) by Wells, showing this effect:

So what happens when you test these octopuses on orientation discrimination tasks? It turns out that they can no longer discriminate between differently-oriented bars. This is a big deal, because it can tell us something about the way that the visual system of the octopus processes shapes. Specifically, it reveals that there is something important about the orientation of the retina that makes it possible for the octopus to discriminate shapes. When the octopus cannot keep its retina level, it cannot discriminate between long shapes and tall shapes. Thus, we know that the circuitry processing visual information in the octopus is relying on the input from the eye always being in the same orientation.

This can be contrasted with the way that people (and probably other vertebrates, although I don't know this for sure) determine orientation in their visual field, which is determined partly by non-visual cues but also largely by the presence of some sort of horizon line in the visual field (see A Horizontal Bias in Human Visual Processing of Orientation and its Correspondence to the Structural Components of Natural Scenes (2004) by Hanson and Essock for a neat demonstration of this.) If there is no available horizon line, orientation is gathered from other parts of the context, such as common or known objects. This means that in humans, even when the orientation of retina is perturbed, the visual processing system can use what it knows about the visual environment to adapt to the new orientation. As long as the input is otherwise normal, it doesn't matter which way the retina is turned - that is, one can still make orientation discriminations when one's eyes aren't on the level.

This might seem puzzling or maladaptive on the part of the octopus, but a little thinking about the visual ecology of humans and octopuses reveals that it's perfectly sensible. Octopuses, living in the ocean, don't often have very clear horizon lines or reliably-oriented objects around them. Their strongest clue about orientation is the pull of gravity. People, living on land, have reliable horizon lines almost all the time, so they can take advantage of this to orient themselves. In addition, octopus eyes have muscles that can rotate the eyeball around any which way relative to the body - human eyes do not. Octopuses never needed to evolve the complex orientation-correcting systems that vertebrates did, because they can just hold their eyes level. They can, in a sense, afford this apparent deficiency in their visual processing system, because they compensate for it easily. If this was the case with people, every time we laid down, bent over, or leaned to one side, the world would be full of novel objects that we couldn't make sense of!

I hope this was informative. I can't wait to write the next one, about octopus touch and proprioception. See you next time!

Notes on the Argonaut

2010-06-21T01:51:00.002-04:00

(Photo by Bernd Hofman.)

One of my favorite parts about reading the research on any topic is reading very old research on that topic. Today, I came across this paper on the argonaut, Notes on the Argonaut (1869), by W. H. Dall, published in The American Naturalist, volume 3. The argonauts are a neat genus of pelagic octopods (Argonauta,) the females of which secrete a thin shell from specialized areas on their arms (pictured above in ecological conditions, inside the shell, and drawn below without the shell.)

(Lithograph by Arthur Bartholomew, ~1870)

Almost 150 years ago, this guy put together a pretty good description of argonaut behavior, although it was brief. Reading his work renews my faith in the power of good old observation, as well as flowery phrasing in otherwise dry writing. For example, Dall comments on the argonaut's sexual dimorphism, with a healthy dose of Victorian sexism:

The Argonant shell is formed, curiously enough, by the females only;

as among more highly organized beings sometimes, the gentler sex

outshine their brothers in the splendor of their apparel, and the

extent it occupies. Unlike many, however, the Argonaut toils not,

neither does she spin.

The last sentence of that quote is genuinely confusing to me. What exactly does he mean? What evidence is there that argonauts do not "toil"? What does it even mean for an octopod to toil? Without being accustomed to the zoological vernacular that Dall is writing in, it's hard to get what he means by this.

Another gem is his description of argonaut mating habits. Unlike today's biological authors (fortunately or unfortunately, it's your call,) Dall doesn't shy away from anthropomorphism:

When the tender passion seizes him, as he rocks on some sunny wavelet,

far from female society, he does not go in search of a wife, but with

Spartan courage, detaches one of his eight hands (or arms) and consigns

it to the deep, in the hope that some tender hearted individual of the other

sex will fall in with it and take it under her protection. Thus for a long time

the male Argonaut was unknown, the arm (which does not die when

detached, but lives an independent worm-like life) was, when found in

the gill-chamber of the female, supposed to be a parasite, and was called

Hecto-cotylus.

Interestingly enough, although this name was given to the organ because it was thought to be a parasite, the modified arm that octopus and squid use to mate is still called a heteroctylus.

In closing, Dall acknowledges the unique contributions of one Madame Jeannette Power (a pioneer of the use of aquaria) to the study of the argonaut with a quaint tone of amazement:

It is pleasant to add that our first detailed account of the Argonaut and its

development, was published by a lady, Madame Power, who made her

observations in the Mediterranean, having a sort of marine enclosure

made, where she kept these animals and observed their habits from life.

I know this was a short one. I couldn't help it - I can't resist dusting off a few of the old chestnuts in the scientific literature and reveling in my own fantasies of some lost scientific world, where it's considered adequately professional to use the term "tender passions" when describing the behavior of a mollusc in a leading biology journal.

Thanks for reading!

Prawn-in-the-tube (More Cuttlefish Memory)

2010-06-17T11:51:00.000-04:00

For several years, a group of researchers in France have been studying the neural correlates of learning in cuttlefish (recently focusing on, among other things, oxytocin-like neuropeptides in the cuttlefish CNS - I'll review this in a later post.) I reviewed some of their work in an earlier post. Although this is a fascinating concept, their method has been criticized because they use a single learning task to elicit what they claim are learning-induced neural changes, generally. Importantly, it is questionable whether their method causes associative learning or habituation. Associative learning involves the formation of a mental or neural (depending on your conceptual preference) association between some behavior and a consequence of that behavior, such as finding food or feeling pain. This form of learning has long been thought of as one of the hallmarks of adaptive behavior, and it is certainly central to any claims about cephalopod intelligence - if we could not demonstrate associative learning in cuttlefish, we would have very little ground on which to call them intelligent. Habituation occurs when we are exposed to some stimulus for long enough that we just stop responding to it. In the case of habituation, we haven't learned much about the stimulus - simply that it is generally unrelated to any reward or punishment we might get.

So what is this controversial procedure? The group has given it the obscure name of the prawn-in-the-tube procedure. It is essentially what is sounds like. A cuttlefish is presented with a prawn enclosed in a clear plastic tube. Cuttlefish, being visual predators, will attack the prawn, but their tentacles will hit the tube, and their attack will fail. Over subsequent presentations, they learn not to attack the tube. The difficulty is that it is hard to tell whether the cuttlefish are simply habituating to the prawn-in-the-tube stimulus, or whether some sort of sensory feedback from failed attacks is causing them to suppress their attacks - a type of associative learning known as passive avoidance learning.

In this group's research on cuttlefish learning (as well as in an older line of research by J. B. Messenger that used the same procedure) it is vital to know what sort of learning they are inducing in order to interpret their results. Specifically, they work under the assumption that their procedure induces passive avoidance learning. This is a pretty big assumption. As such, they decided to settle this problem with a series of experiments, which they published as The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning? (2006) by Agin, Chichery, Dickel, and Chichery.

This study uses two techniques. The first is called dishabituation. In these experiments, a strong competing stimulus is presented alternatively with the "habituated" stimulus. If this elicits a greater response, the it is likely to be the case that the animal has habituated rather than learned by association. If the response is still suppressed after the novel stimulus is presented, it must be that the familiar stimulus is repressing behavior, and that passive avoidance learning has taken place. The logic is that the effects of habituation will decrease if the animal becomes generally aroused by some other stimulus. Their results show, however, that this is not the case. Novel stimuli did not dishabituate the cuttlefish to the prawn-in-the-tube assembly. Strike on against the habituation theory.

The second test that they used involved showing the cuttlefish a piece of bait (a live prawn,) and then removing it from the tank as the cuttlefish attacked, preventing them from ever catching it. In this test, the cuttlefish never received any sort of tactile feedback when they attacked. If the prawn-in-the-tube procedure causes habituation, we would expect attacks to decrease in this condition, as there is no reward or punishment to shape the behavior. If the prawn-in-the-tube procedure works mainly by passive avoidance learning, we would expect that, as there is no negative sensory feedback following unsuccessful strikes, the cuttlefish would not change their response at all during this version of the procedure. As it turns out, the procedure was almost completely ineffective in inducing any sort of learning in this condition. The cuttlefish continued to strike regularly at the prawn, and their latency to strike actually decreased. This experiment clearly does not support the habituation hypothesis. Strike two!

Where's the third strike? Oh, yeah, Purdy et al found similar results using a variation of this procedure in their paper Prawn-in-a-Tube Procedure: Habituation or Associative Learning in Cuttlefish? (2006). Strike three, and the habituation hypothesis is out!

Actually, these results could presumably be overturned by some more sensitive or definitive test in the future. For the moment, however, these studies allow the cuttlefish memory research community to investigate the neural bases of memory in the cuttlefish with a reasonable amount of certainty that they are studying associative learning. They also make a nice general point about the sort of fine-grained analysis that's needed in order to study complex psychological processes like learning and memory, as well as emphasizing the importance of being critical of the assays that one uses to study these things.

Thanks for reading!

(Sepia apama. Photo by Nick Hobgood, used under a Creative Commons license.)

Octopus ethology: the case of Abdopus aculeatus

2010-06-15T12:10:00.002-04:00

Ethology is a discipline that I have been enamored of ever since I first discovered it.
The field started with the studies of animal behavior by Konrad Lorenz, who was interested in "instinctive" behaviors in a variety of species, most of them birds (for a good review of history, see http://apophenia.wdfiles.com/local--files/start/tinbergen.pdf). The goal of ethology is stated in a deceptively simple way: to study the behavior of animals. It seems to me to straddle the junction of zoology and psychology, studying behavior from the perspective of animal biology, much as biological psychology studies human behavior in reference to human biology.

It turns out that ethologists do, in essence, the legwork that allows comparative psychologists to study animal behavior with the hope of generalizing across species. Ethology generates the systematic, cross-taxon descriptions of behavior that comparative psychologists rely on. If you don't know what an animal does, how in the world are you supposed to study it?

The basic structure of an animal's behavior is referred to as an ethogram. Ethograms have been developed for a wide variety of species. These are essentially attempts to create a complete catalogue of a species' behavior. Ethograms can be quantitative (that is, quantify how much an animal does each activity in its repertoire) or merely descriptive. In some commonly used laboratory species (take the rat, for example) ethology has been largely left by the wayside, due in part to a focus on generalizing experiments to human psychology or biology. This appears, to me, to be very unfortunate, as we risk losing our perspective on what the behaviors we study mean to the animal performing them.

For example, consider the classical learning experiments in rats that use the lever press as an operant response. Ethologists would never have tried to study learning in the rat using a lever-pressing behavior. Rats, if left to their own devices, simply do not tend to press levers! More recently, nose-poking (a very common and easy thing for a rat to do) has gained some popularity as an operant response, and has made this research much easier to conduct as well as more flexible. Knowing the behavioral repertoire of an animal is a prerequisite to understanding any particular behavior in that animal, let alone using it to draw inferences about behavior across species.

The take home point: I like ethology.

I didn't bring up ethology just to rave about it, though. I've been reading a number of cephalopod ethograms, and wanted to spread them around. Ethograms are interesting to read because they provide a snapshot of a species - they provide some understanding of its biology, its ecology, and its psychology, all in one.

In Ethogram of Abdopus aculeatus (d'Orbigny, 1834) (Cephalopoda: Octopodidae): Can behavioural characters inform octopodid taxomony and systematics?, Christine Huffard lays out an ethogram of Abdopus aculeatus, a species of small octopus that lives in indonesia (for videos and a press release on her findings, see this link) In this press release, she mentions how much of our information about octopus behavior comes from a few, rather old sources, and not a diverse and current range of ethological studies, as one might hope for. I find this to be frustratingly true - when you look at the literature on octopus behavior, it seems like many experimental biologists quickly jumped on the octopus as a system to study something (vision, motor control, learning) largely without taking to trouble to investigate and re-investigate its behavior in ecological conditions. The sources that exist on this topic are mainly books, not journal articles - both less accessible and less stringently peer reviewed. Huffard's articles are like a breath of fresh air in the world of octopod behavior.

Here's a few pictures of the pretty little guy:

(Figure 2 from Locomotion by Abdopus aculeatus (Cephalopoda: Octopodidae): walking the line between primary and secondary defenses (2006), also by Huffard. The supplementary material for this paper also has a few good videos of A. aculeatus moving about.)

Now comes the big question: what did the study find?

Well, the study does a very good job answering the question: what does this animal do? Huffard found that A. aculeatus is diurnal, both mating and foraging primarily during the day. Like other octopuses, they forage using mainly their tactile sense (although sometimes visually,) groping the substrate to locate prey.

A. aculeatus shows a great variety of body patterns, including really impressive papillae (bumps on the skin that can be made larger or smaller as part of a body pattern) and a variety of color patterns, mainly used for camouflage.

Perhaps the most striking findings are about the social and sexual behavior of A. aculeatus. Octopuses are known for being solitary creatures, but Huffard describes the presence of specific male-male aggressive interactions, usually in the presence of a female. Sometimes, it even appeared that one octopus would try to strangle its opponent by "[wrapping] one arm around the mantle opening of another individual, presumably cutting off ventilation." It was also found that males actively guarded their mate females from other males, whom they often mated repeatedly with over a few days. This is in contrast to the relatively simple meet-and-mate behavior that has been described in other octopus species.

Huffard ends the paper with a discussion of the use of skin components and other behaviors to clarify octopus systematics. She makes the argument that O. cyanea shows certain behavioral similarities to A aculeatus, as well as being closely phylogenetically related, demonstrating that behavior can inform phylogeny. While this is suggestive that behavior might be useful in classifying organisms, I think that it remains to be seen whether this is a reliable way to do it (at least, more reliable than molecular phylogenetics, upon which her argument appears to rest.) The case for this seems like it would fall prey to the problem of convergent evolution, as it appears relatively easy to evolve nearly identical behaviors and morphologies independently, but harder to evolve identical nucleotide sequences independently. Frustrating this issue, she mentions, is the fact that there are no published ethograms for cogeners of A. aculeatus.

Thanks for reading!

Cuttlefish Chromatophores

2010-06-12T09:44:00.002-04:00

I'd like to take a minute to talk about chromatophores. These are the pigment organs that allow cephalopods to change their color and body pattern, like this pretty little guy is doing:

(Photo by Nick Hobgood)

Neuroscientists (at least some of them) seem to get pretty excited about cephalopod chromatophores, because they are neurally controlled instead of hormonally controlled - this makes them unique among chromatophores, which are found in a wide variety of animals including fish, reptiles, and some invertebrates. Each of a cephalopod's chromatophores is innervated directly, which allows it to change color quickly to make a huge variety of patterns. Besides allowing cephalopods to exhibit remarkable color-changing behavior, chromatophores give us a chance to study a unique neural system whose operation probably sits somewhere between autonomic or reflexive activity and voluntary control, and which has no clear homolog in vertebrate neurvous systems.

Chromatophores themselves are interesting structures. They consist of a central area of pigment surrounded by radially organized muscles. When these muscles contract, the chromatophore widens from its usual contracted state. By coordinating the movement of the muscles of many chromatophores, cephalopods can create a variety of body patterns. Here is a diagram of the organ:

(Figure from Peptidergic Regulation of Chromatophore Function in the European Cuttlefish Sepia Officinalis by Loi et al. (1996).)

When one considers that even a small cuttlefish has hundreds of these organs, all controlled via neurons emanating from the central nervous system, the chromatophore system and the behaviors it makes possible become very impressive.

To bring this post back towards the topic of brains, let's consider the innervation of chromatophores. I should point out that chromatophores are mostly studied in Sepia (that is, in cuttlefish,) because this species has very densely placed chromatophores and some of the most conspicuous patterns of coloration. Some work has been done in squid and octopus, but the vast majority of the literature on cephalopod chromatophores is restricted to cuttlefish. As such, while I work under the assumption that most cephalopod chromatophore systems are similar to what's been described in the cuttlefish, this is only an assumption on my part, and remains to be seen.

In Peripheral innervation patterns and central distribution of fin chromatophore motoneurons in the cuttlefish Sepia officinalis by Gaston and Tublitz (2004), the authors present data illustrating the pattern of innervation of chromatophores in the fin of cuttlefish. What they find is that the fin nerve is highly branched and innervates the fin muscles and chromatophores in an apparently efficient manner. Here is a photograph of their preparation, showing the branching fin nerve:

While this is cool, I'm more concerned with their findings regarding of the source of the neurons that innervate the chromatophores. The authors used a method called retrograde labeling to investigate this. In this technique, nerves are dyed somewhere in the periphery (in this case, the fins), the dye is given time to fill the whole neuron, and the it can be located in the central nervous system by slicing the brain and looking at it microscopically. Gaston and Tublitz found that most of the neurons innervating chromatophores originated from the posterior suboesophageal mass (in the following image, found towards the bottom right - one of the lobes of the posterior suboesophageal mass, the pallidovisceral (pv.) is labeled.) This is perhaps not surprising, because it has been known since Young's work in Octopus in the 1960's that much of the innervation of the mantle organs and musculature arises from the posterior suboesophageal mass.

The cuttlefish brain is pretty similar to the octopus brain in its organization. The following figure is a sagittal section of a cuttlefish brain and buccal mass from "The Brains and Lives of Cephalopods" by Nixon and Young (which is a wonderful book, by the way.) In terms of orientation, the mouth is to the left of this figure (the beak and lip are labeled,) the supraoesophageal mass is towards the top of the image, and the suboesophageal mass is towards the bottom of the image. I like this image because it situations the brain in the context of the larger structure of the head of the cuttlefish.

Although there is a growing literature on the subject, there are still lots of questions to be asked about chromatophores. I would personally love to see more research on the representation of the skin's surface within the neural system controlling the chromatophores. It would be neat to see if somatotopy was present, and in what forms. Also, the possibility of the systems that control chromatophores working as part of some sort of generalized stress- or motivation-related system is very interesting to me.

For the interested reader, here are some other free, full-text resources on chromatophores:

Neural regulation of a complex behavior: body patterning in cephalopod molluscs by Tublitz, Gaston, and Loi (2006, Integrative and Comparative Biology)
Cephalopod chromatophores: neurobiology and natural history by Messenger (2001, Biological Reviews)
Neural Correlates of Colour Change in Cuttlefish by Messenger and Miyan (1986, Journal of Experimental Biology)

Thanks for reading. See you next time!

A View of the Octopus Brain.

2010-06-09T18:27:00.002-04:00

In this post, I am going to outline octopus neuroanatomy, to the best of my ability. It's a complicated subject that I am only beginning to have a grasp on, but I want to post more about specific research papers regarding cephalopod brains, so I figure I should review this first. Let's get right to it.

This figure is from J. Z. Young's "The Anatomy of the Nervous System of Octopus Vulgaris" (1971, which I was fortunate enough to come across recently. If you're familiar with looking at mammalian brains (like me,) you'll be utterly lost. This is a view of the octopus brain from above - imagine that the octopus is lying on a table, it's mantle away from you and its tentacle towards you, it's eyes looking longingly into yours. Its brain would be oriented as shown. The two big swellings on either side are the optic lobes, which sit just underneath the eyes. The rest of the octopus brain is wrapped around the esophagus. The brachial nerve (labeled "n.br." and seen towards the bottom of this figure) travels out to innervate the arms (more precisely, we might say, to connect the nervous system of the head and the nervous system of the arms, which is hugely complex in its own right.) See this diagram of octopus general anatomy to get an idea of the size of the brain relative to the octopus's body, as well as the nervous system of the arms.

This is a figure from the same work showing a section of the octopus brain from the side. In this figure, the mouth and tentacles would be off to the left, with the mantle off to the right. The big white hole in the middle of the brain is at the level of the oesophagus, although I'm not sure if it is actually the oesophagus in this section. The brain is thus divided into supraoesophageal and suboesophageal masses (the former being above and the latter below the oesophagus.) This image does not include the optic lobes.

While the octopus brain is smaller than that of birds or mammals when adjusted for body weight, it is still a highly-developed, centralized brain with specialized substructures within it. Within the next few weeks, I'll try to cover some of the research that has been done to map the functionality of the cephalopod brain, as scant as it is in comparison to the literature on mammalian brains. For now, though, I'll go through it briefly.

It is misleading, actually, to focus only on the brain if we're trying to understand the nervous system of octopus - most of the neurons in an octopus (roughly 2/3 of them, actually) lie in the nervous system of the arms, which is thought to control some aspects of movement with little input from the brain.

Young divides the octopus brain into 5 functional areas: Lower, intermediate, and higher motor centers, receptor analyzers, and memory centers. We'll go through them all briefly.

Lower motor centers are those which contains the neurons controlling muscles directly. These neurons effect muscle contraction, and so make possible the movement of the animal. These are analagous to some neurons in human motor cortex, as well as those in the spinal cord. In the octopus, these are located in the nervous system of the arms.

Intermediate motor centers (located in the anterior suboesophageal mass in the pre- and post-brachial lobes (br.pr. and br.po.), as well as others) coordinate movements between the arms in a way that is beyond that of the lower motor centers. These areas are comparable to some neurons in mammalian motor and premotor cortex that, when stimulate, produce complex patterns of movements, but which generally fall short of that seen when an organism is behaving freely.

Higher motor centers, located (for example) in the basal lobe (b.l.) control complex behaviors that involve the animal's whole body. I am not sure that these have a parallel in the mammalian brain, but my guess is that it would lie somewhere in premotor cortex, coordinating the activities of the motor units further down the chain of command.

Receptor analyzers are those parts of the brain that interpret incoming information from sensory receptors. Notable, in the octopus, they include the optic lobes (opt.) which analyzes incoming visual information, and the buccal system (buc.s.) which analyzes information from touch receptors in the arms and buccal mass (the area at the convergence of the arms, where the beak is located.) The mammalian brain has lots of these as well, for example the inferior and superior colliculi, which analyze incoming auditory and visual information, respectively.

Last, but certainly not least, are the memory centers. The memory system in octopus (and in cuttlefish, as I'll post about later on) is distributed among the superior frontal (f.sup.med.), vertical (v.), and subverticle (subv.) lobes, as well as the buccal system, and the inferior frontal (fr.i.med.) lobes. J. Z. Young has made the argument that the organizations of this system show analogy to circuits in the human hippocampus (see Computation in the Learning System of Cephalopods, 1991). I do not know enough about the two systems to agree or disagree with him at this point, but it is an interesting idea, nonetheless.

I hope this has been as informative for you as it has for me! You can count a few more posts on memory research in cuttlefish soon.

Cuttlefish Memory

2010-06-06T09:38:00.002-04:00

Image by David Sim, used under a Creative Commons License.

Being, up to this point, rather octopus-centric in my posts, I decided to dig into the literature on cuttlefish behavior. Cuttlefish are (relatively) easily kept in aquaria, and have been extensively studied in terms of their complex color-changing behavior (see A review of cuttlefish camouflage and object recognition and evidence for depth perception by Kelman, Osorio, and Baddeley for more information on this area of study) as well as their predatory behavior learning abilities, and possible social behavior.

The first paper I want to talk about in this post is Evidence for a specific short-term memory in the cuttlefish by Agin, Dickel, Chichery, and Chichery (1998).

Agin et al's experiment ran as follows: cuttlefish of various ages were shown a prawn or shrimp sealed inside of a glass tube during a training phase. As one might expect, the cuttlefish attacked the glass tube, but learned to suppress their attacking as they learned that the prey was inaccessable. Then, after a 5 minute break, the cuttlefish were tested to see how well they could remember not to attack the prey in the tube. There were 3 groups - the first got 20 minutes of training, the second got 5 minutes of training, and the last was exposed to the empty glass jar for 20 minutes as a control group.

In a nutshell, here are their results: Juvenile cuttlefish (15-30 days old) learned to suppress attack in the 20-minute condition only, while for older cuttlefish, a 5 minute exposure was enough for them to learn the lesson and almost completely suppress attack.

This is all well and good by itself. We would more or less expect that cuttlefish should be able to retain this simple memory, knowing how good cephalopods are at that sort of thing. What makes this story more interesting is this groups follow-up paper.

In Effects of learning on cytochrome oxidase activity in cuttlefish brain by Agin, Chichery, and Chichery (2001), the group subjected cuttlefish to the same learning task and then measured cytochrome oxidase levels in their brains at different time points after learning. Cytochrome oxidase expression is increased in metabolically active cells, putatively indicating (in neurons, at least) the overall activity level of the cell (with rather poor spatial resolution, of course.) What this experiment revealed was that the pattern of cytochrome oxidase staining changed depending on how long it had been since the cuttlefish did the learning task. In other words, it looks rather like different populations of neurons are involved in the early stages of memory than the late stages of memory. A similar effect was found using a marker of acetylcholine synthesis in this study, Central acetylcholine synthesis and catabolism activities in the cuttlefish during aging by Bellanger et al .

This is notable because it suggests that cephalopods, like birds and mammals, may have dissociable short- and long-term memory systems. According to the generally accepted theory of human memory, the short-term and long-term memory systems are comprised of distinct but overlapping neural circuits. It would be very interesting if the same dissociation had developed in cephalopods (in fact, this same group has gathered more behavioral evidence supporting this hypothesis since these studies were published, ie. their study Developmental study of multiple memory stages in the cuttlefish, Sepia officinalis, 2006 .) While it seems that the study of cephalopod memory processes is still in its infancy (compared, at least, to the study of human memory processes) and no strong assertions about this system can be made yet, it's a tantalizing thought that we might be able to find and understand such a striking example of the convergent evolution of neural systems as this.

Cephalopod Consciousness

2010-06-02T22:34:00.001-04:00

In their paper Identifying hallmarks of consciousness in non-mammalian species (2005), Edelman, Baars, and Seth put forth the idea that research on consciousness needs to expand beyond methodologies which rely solely on the ability of organism somehow report their concious awareness of something (that is, behavioral tests) and encompass neuroanatomical and neurophysiological investigation. To my delight, they chose to focus on birds and octopuses as examples of animals whose possible consciousness might be probed via non-traditional methods of inquiry.

Citing evidence related the neuroanatomical and functional bases of consciousness in humans and other mammals, the authors eventually conclude that it there is a good case for avian consciousness, and the possibility of cepahlopod consciousness, based on the presence or uncertainty of these three necessary criteria:

               (1) identification of neural structures that are the functional equivalents
                       of cortex and thalamus;
               (2) neural dynamics analogous to those observed in mammals during
                       conscious states
               (3) rich discriminatory behavior that suggests a recursive linkage
                      between perceptual states and memory

I like their style and their argument. However, I really wanted to write about this paper for a much simpler reason. It has one of the best concluding figures that I have ever seen in a paper:

Not only do they have good ideas, but a great illustrator, too.

The Urbilaterian

2010-06-02T22:13:00.002-04:00

Cephalopods, especially octopuses, have large, complex, functionally differentiated brains. They can learn, perform complex visual and tactile discrimination, play, show complex defensive and aggressive responses, and all sorts of other interesting and highly variable behavior (Jennifer Mather's review of cephalopod behavior is good reading for those who are interested.) Notably, this behavior is unusual among molluscs, who tend to be scavengers or filter-feeders instead of mobile, active predators.

My point is that octopus behavior reminds me a lot of vertebrate behavior and not very much of, let's say, the behavior of clams or sponges, which seems to be mostly limited to sifting for food, moving about to find a better spot to anchor themselves, and mating by ejecting sperm into the water. Their brains are organized in ways that are reminiscent of vertebrate brains, notably in their memory systems and visual processing systems (see my earlier post on the Octopus visual system for a better, though still brief, treatment of this topic.)

These facts about cephalopods are part of what originally piqued my interest in them. The study of the similarities and differences between vertebrate and cephalopod neural systems is intriguing to me because vertebrates and cephalopods are presumably very, very distantly related, evolutionarily speaking. Cephalopod and vertebrate nervous systems have been evolving independently from rather rudimentary beginnings, and have somehow ended up having not only somewhat similar capabilities but also apparently similar organization and mechanisms, even at complex levels of information processing. I have a strong feeling that there is something important to be learned about the evolution and development of nervous systems from the study of cephalopods.

Following this line of reasoning, it's important to understand just how cephalopods (part of the phylum mollusca) and vertebrates (of the phylum chordata) are evolutionarily related.

The last common ancestor between vertebrata and mollusca is though to have existed at least 550 million years ago (most probably more), around a time referred to as the Cambrian explosion. It's called that because drastic evolutionary differentiation occured during a short time, resulting in the evolution of many of the taxons that we know today. This ancestor was the "urbilaterian", or the last common ancestor of all of the bilaterians. Bilaterians are animals who have a bilaterally symmetrical body plan - not that their bodies are always symmetrical (just look at the flounder), but their body plan is.

This organism (or a similar one - it depends on who you ask) is also called the protostome-deuterostome ancestor (PDA), because it is thought to represent the last common species before the divergence of the deuterostomes (whose gut grows from their anus inwards, basically) and the protostomes (whose gut used to be thought to grow from the mouth inwards, but is now know to develop in a few different patterns.)

There is a slight technical difference between these terms, with the "urbilaterian" being the last common ancestor of all of bilateria, and the "PDA" being the last common ancestor of only the deuterostomes and the protostomes, but not of the few other small phyla that are also included within bilateria. Despite this, it is not known how to differentiate the two possibilities, nor how they would affect the probable attributes of such an organism. Although the "missing link" that would characterize the relationship between cephalopods and chordates should be technically referred to as the PDA, the authors of the papers I cite use the term "urbilaterian", and so I will stick with this.

It might seem like a stretch to purport to study something that hasn't existed for hundreds of millions of years and that we can never unambiguously identify. Nevertheless, we can know what features the urbilaterian must have had by looking at those features that are common to all Bilateria. This is apparently done using genetic and genomic techniques (which I am admittedly not very familiar with - here I am trusting the authority of the cited authors and their citations.) Erwin and Davidson, in a review titled The Last Common Bilaterian Ancestor (2002) make the argument that one of the important conserved elements of bilateria are genes that regulate cell differentiation - that is, certain cell types (which presumably will later allow the evolution of certain morphological structures) are already present in the urbilaterian and are conserved throughout bilateria. The examples cited by Erwin and Davidson are (possibly among others): photoreceptors, neurons, intestinal-secretory and neuro-secretory cells, cardiac-type and striated muscle cells. Also conserved across Bilateria are a variety of regulatory genes that determine how the expression of genes the cause cell differention occurs during an organisms development. Most of the variation within bilateria is therefore constructed by these (approximately) common cell types and regulatory mechanisms.

So, based on our current understanding of comparative developmental genetics and morphology, the urbilaterian looks something like this:

(Figure is from Acoel development supports a simple planula-like urbilaterian by Hejnol and Martindale, 2007.) This hypothetical little guy has a central nervous system; although, Hejnol and Martindale argue, it's likely that it is primarily net-like rather than based around a centralized ganglion. Notably, it has photoreceptive cells (essential for the evolution of eyes) and epidermal sensory cells. It also has striated and smooth muscle cells, and the nervous apparatus to use them both. It has a blind gut (meaning that its food intake and waste output use the same cavity) with specialized secretory cells, no appendages, and no body segmentation. In short, although it looks very simple, it contains all of the building blocks to make the huge diversity of lifeforms we have today, as well as all those that have evolved from it and since become extinct. These are listed, in part, in the chart in the bottom half of this figure, showing the genes implicated in the differentiation of conserved body features along with a diagram of where they are expressed in two different hypothetical bilaterial (the right being the one supported by the authors.)

So, this is the point of the story: if we understand humans well, and we understand other species (including cephalopods) well, then we might be able to determine what features of each are likely to be due to inherent constraints in all bilaterian biological systems, and which have evolved more through more open-ended mechanisms. From this, we could learn very general rules about how bodies grow and develop, and of specific interest to neuroscientists, how complex neural circuits are wired up. This would bring us a huge step closer to understanding brains in general, as well as our specific human brains.

Cephalopod eyes

2010-05-31T18:46:00.004-04:00

I just wrote a big post about cephalopod eyes, and then realized that I had neglect to show any real-life pictures of cephalopod eyes. This blog seems to be getting a bit dry, so let's take some time off and just gaze at some of our beautiful, squishy friends. All images are from the wikimedia commons and have been under a creative commons license.

(Photo by Parent Géry) This guy is Octopus vulgaris, also known as the common octopus. It the most-studied octopod. You can see the slit-shaped pupil clearly.

(Photo by Theasereje) Here's a body shot of another O. vulgaris. Notice how they can look at you with both eyes at the same time - they have the capability for binocular vision. Octopuses, however, prefer monocular vision, and will always use just one eye to sight their prey during an attack (for more info, see this "Lateral asymmetry of eye use in Octopus vulgaris" by Byrne et al.)

(Photo by Elapied) Here we have another gorgeous shot of O. Vulgaris peering out of a hideout with one eye.

(Photo from www.opencage.info) This is an ocellated octopus, O. ocellatus. Besides being very cute, as he peeks out from the shell, he is probably using his mostly monocular vision to monitor his whole environment for danger.

(Photo by Jens Petersen) Here is Amphioctopus marginatus, the coconut octopus, showing us how it can focus both eyes on the same area of space, even if it usually doesn't like to.

By now, you're probably tired of octopuses. Let me give you a break then, and venture into the world of cuttlefish and squid!

(Photo by Bernd) This is Sepia prashadi, the hooded cuttlefish. Cuttlefish hunt by visually stalking their prey and then shooting out their tentacles to grab it. Thus, they need to have a binocular field of vision so that they can accurately catch prey. This little guy's eyes are apparent on either side of his head (look for the curved, black pupil slits.) As you can see, cuttlefish can look in front of themselves with both eyes.

(Photo by Nick Hobgood) This is Sepia latimanus, the reef cuttlefish. Here you have a better view of the eye. The eyes are not closed - the pupil of cuttlefish is always a horizontal slit.

(Photo by Nick Hobgood) This is another S. latimanus, showing a different coloration.

(Photo by Nick Hobgood) This is Sepioteuthis lessoniana, the bigfin reef squid. Most squid normally have mostly monocular vision, but can move their eyes towards the front of their head to have temporary binocular vision.

(Photo by Nick Hobgood) This is Euprymna scolopes, the Hawaiin bobtail squid. In this photo, you can see the cuttlefish-like pupil shape and the existence of binocular overlap.

(Photo by Michael Vecchione) I'll leave you with the bizarre-looking eye of Helico pfefferi, the piglet squid. I don't know anything about them, but they sure look cool.

Thanks for reading!

The Octopus Visual System

2010-05-31T17:43:00.003-04:00

Visual neuroscience is one of my favorite sub-fields of neuroscience. As such, I've decided to write this post about the visual system of Octopus (I will leave out squid and cuttlefish for this post, but theirs are, overall, pretty similar.)

First, let's take a look at the anatomy of the octopus eye, in comparison to a more familiar specimen (this figure is from Ogura et al., 2004):

They look pretty similar, don't they? Notably, the both have lenses to refract light, a pupil to restrict incoming light, a retinal surface distributed along the back of the eye, and a well-differentiated optic nerve. There are, however, a few notable differences. Firstly, octopus eyes and human eyes focus light on the retina in different ways. Humans bring their eyes into focus by changing the shape of our lenses using the cilliary muscle. Octopuses, on the other hand, focus by moving the lens closer to or further away form the retina. This is the same way that a camera focuses, and so people often refer to cephalopod eyes as "camera eyes." Secondly, the octopus retina is very different from the mammalian retina in terms of its cellular organization. Let's look at an octopus retina first (From Young, 1962).

Light enters the eye from the top of this image. In terms of cellular organization, the limiting membrane (l.m.) at the top of the figure faces towards the front of the eye, with the basal membrane (bas. m.) towards the back of the retina. The distal segments (dist.) of photoreceptors face the front of the eye, and the proximal segments (pr. s.) sit at the back of the retina, from which they send their projections through the optic nerve to the optic lobes where further processing of visual information takes place.

To compare, let's check out a few diagrams of the mammalian retina (both of these are taken from Wassle and Boycott, 1991 ; the first is their own drawing, and the second is by Ramon y Cajal, one of the early geniuses in neuroscience):

Now, you wouldn't know this from looking at the figures, but the mammalian retina is actually opposite in orientation from the cephalopod retina. That is, light enters from the bottom of these drawings, and passes through several layers of cells before reaching the photoreceptors at the back of the retina (the photoreceptors in these images are rod-like structures at the top of the images, labeled as "OS" and "IS" (for "outer segments" and "inner segments", respectively) and as "e" and "f" in Cajal's drawing.)

You, being a smart and inquisitive reader, might just now be asking, "what is all that other stuff doing in our retinas?" It turns out that it processes the information that photoreceptors gather about patterns of light right there in the retina. By the time retinal ganglion cells (labeled "GLC" and "c" or "d" in the two images) leave the mammalian retina, they are already carrying information about properties of the visual environment, such as where isolated, high contract areas of light are and what the overall level of illumination in different areas of the visual field is. This information can then be used by visual processing centers in the brain to very efficiently form a picture of the visual world, including identifying objects and movements.

At first glance, it looks like the octopus must miss out on some visual processing power because it does not have this visual processing system intrinsic to the retinal. It makes up for this, however, in a very interesting way. Let's look on this drawing of the organization of the octopus optic lobe - the place in the brain where the octopus optic nerve ends up (this image is from Young 1961):

Young makes the argument, in this paper, that the outer layers of the octopus optic lobes (which are nestled right under the eyes and directly innervated by the retina) are likely to have the same function of the complex layers of the mammalian retina, with the deeper layers analagous to mammalian central visual processing areas. As far as I know, there has been no direct test of this hypothesis. However, it is an interesting and (at least circumstantially) sensible idea, and it must be the case that octopus forms perceptions of objects and movements are some central location - after all, it does have rather good vision. The optic lobe, after presumably making sense of what the retina is saying, sends projections all over the superoesophageal mass of the brain.

Why does this matter? Who gives a bibble? Well, the evolution of the eye as long been used as a sort of model evolutionary system, that is, we can probably use it to understand evolution, and to determine what principals of genetic selection drive evolution. It's suitable for this for a few reasons: we have extant animals with a variety of types of eyes, we have extant animals with no eyes, the eye is relatively accessable and easy to study (and so the eyes of mammals and insects has already been extensively studied.) As a discrete organ, it is also a relatively straightforward task to characterize morphological and cytoarchitectural variation between species. In addition, the visual system is interesting to study because it is one of the few systems that we can understand and model on a fine-grained computational level. Thus, the differences between cephalopod and human eyes are important because they can not only tell us things about how our eyes work, but help us figure out the way that evolution works. Evolution, as we know, is important to understand because it is, quite literally, the reason we are here.

It seems that there is probably an optimal organization to any visual processing system that involves progressive layers of increasingly synthetic processing of incoming visual information (for example, the progressive abstraction of visual input in humans from light to features, and then to objects and scenes.) This point is strengthened by the fact that insects appear to share this style of processing visual information, albeit with anatomical differences (for more information on insect visual processing, see this paper).

I had wanted to talk about the vestibular system of cephalopods in this post as well, but it's already lengthy and I need to get going. I'll do a post on it another time.

Thanks for reading!

Octopus Olfaction and Ingestive Behavior

2010-05-30T04:37:00.002-04:00

I was the Pittsburgh Zoo today, and had the opportunity to watch their resident Pacific Giant Octopus (Enteroctopus dofleini) being quite active. After moving about for a while, it balled up and sat on the glass, and I noticed an interesting behavior. The animal would wave the tips of its arms around in the water for a moment, and then drag them along the glass in towards its mouth, until they almost touched its lip (that is, near the confluence of its arms.) My armchair theory about this was that this was some sort of chemical sampling of the environment; however, there doesn’t seem to be any good evidence for this on a cursory search of the literature on octopus olfaction (if you know of some, please point it out to me!) I did, however, find a neat paper that addresses the effect of olfaction on octopus eating behavior.

The paper is Chemical Stimuli and Feeding Behavior in Octopus, Octopus vulgaris by Anraku et al (2005). A free full-text version is available here. I like this paper because it uses a very clear (though limited) behavioral coding scheme to quantify what would otherwise be an impossible-to-quantify set of behavioral sequences. It's a very good example of methodologically solid behavioral research on a non-traditional laboratory animal. Let’s get on to it, shall we?

In this study, the authors (who worked, as is somewhat typical in the field of marine biology, at an institute concerned with commercial fisheries – something I have issues with, but which does not invalidate their research) presented octopus with cellulose bait pellets soaked with different putative olfactory signal chemicals. Then, the amount eaten was measured (as a metric of the attractiveness of the food), and the octopuses’ behavior during the bait presentation was coded. The general design of the study is illustrated in the first figure of the paper:

I love this figure. It does what too few papers bother to do: make their experimental design crystal clear at the outset of the paper.

The behavioral coding scheme the researchers used is as shown in this figure:

Their results are basically as follows: octopuses often (63% of the time) showed “positive” consumptive behavior towards the bait pellets with no added olfactory cue. Among a variety of chemicals tested, fish extract was found to significantly raise the probability of consumptive behavior (to 88.5%) while squid ink (but not octopus ink) was found to significantly decrease the probability of this behavior (to 10%.) Octopus ink did, however, significantly decrease the amount of the pellet eaten relative to controls.

This study shows that feeding behavior in the octopus is at least somewhat mediated by olfactory cues. What I would like to see investigated more is the way that olfactory cues from other octopuses (such as ink) might influence behavior; the authors mention that squid have been shown to increase escape behavior in the presence of other squid’s ink. It may be that octopus use similar social cues, either to signal positive or negative aspects of the environment or to mediate encounters between octopuses. Maybe somebody is already working on this problem, and I simply haven’t found that research yet. In any case, I think it would be interesting.

Thanks for reading! If anybody has any good information of octopus olfaction that they'd like to share, please do!

LTP in the Octopus Memory System

2010-05-28T11:15:00.009-04:00

I’ll get back to octopus behavior in the subsequent posts, but I want to digress into octopus neurobiology for a minute. We know that octopuses can learn, and our buddy J. Z. Young proposed that their memory system is much like ours – as evidence, he showed that the structure of the octopus vertical lobe (a little chunk of brain tissue that sits right at the top of the octopus brain – see P. Z. Myers’ post on the subject for a quick introduction to the brain of octopus) may have a lot in common with the structure of the mammalian hippocampus (which is a place in the human brain that is critical for memory – it’s shown here.)

The specific paper that I’ll review here is “A Learning and Memory Area in the Octopus Brain Manifests a Vertebrate-Like Long-Term Potentiation” by Hochner et al. It was published in 2003 (7 years ago already!) in the Journal of Neurophysiology (available at this link.) Much as the title suggests, this study showed the presence of long-term potentiation (or LTP) in the octopus vertical lobe.
Let me explain what LTP is, and then the previous paragraph may become a lot more meaningful to some readers. LTP is the mechanism by which synapses (the points of communication between nerve cells) become “stronger”; that is, synapses can transmit information with a varying degree of degradation of the signal, and stronger ones will transmit the information better than weaker ones. First, a picture of a synapse:

The neuron sending the information (the presynaptic neuron) is in yellow, while the neuron receiving the signal (the postsynaptic neuron) is in green. Imagine that the system works like this: an electrical pulse comes flying down the presynaptic axon from the top of the page. When it gets to the end of the axon, it causes (through a variety of rather complicated biochemical mediators) all those synaptic vesicles to dump their contents into the space between the neurons (the synaptic cleft). Their contents are neurotransmitters, which then act on receptors on the postsynaptic neuron. This activity causes electrical currents to be generated in the postsynaptic neuron, and so the electrical signal has bridged the gap and is on its way.
When a synapse is persistently active, it will tend to become stronger (this is known as Hebb’s law – it’s actually only sometimes true, but it’s a good heuristic for now.) This is called long-term potentiation, as the synapse can be said to be potentiated, and this effect will last a while. Now, a lot of things happen during LTP – the synapse may become physically larger or more efficient, and the types of receptors on each side may change. In any case, the overall effect is that the synapse will become better at propagating signals – that is, the same signal in the presynaptic neuron will elicit a larger signal in the postsynaptic neuron.

In this study, electrical pulses were sent through the MSF (medial superior frontal) tract – a tract that runs parallel to the brain surface and interacts with vertical lobe neurons. Simultaneously, recordings were made from neurons in the vertical lobe that could receive signals from the MSF tract. What the experimenters were testing was whether they could induce LTP in octopus neurons by stimulating them. This procedure is known to work in vertebrates, and is thought to be responsible for much of vertebrate neural plasticity (that is, the adjustment of the way neurons are “wired” together, which is thought to allow us to do things like learn and remember.) If it’s present in octopus, then it means that there is something about the organization of this type of system that is efficient or effective enough to have evolved largely independently in two very different groups of animals (although we don’t actually know exactly what the last common evolutionary ancestor was between people and octopus, we have a pretty good idea – but that’s for another post. It suffices to say that it mostly likely had a very simple nervous system, meaning that octopus and vertebrate brains evolved mostly independently.)

If you’ve read my previous post or another piece of writing about the squid giant axon, let me use this example to drive home its significance. The techniques of neural stimulation and recording in this paper, as well as the theories that the authors employ about the structure and function of neurons, all descend directly from work done on the squid giant axon. It really is a big deal.

So, with the basic experimental design and that little editorial out of the way, let’s hit the meat of the paper:

All of this groups work was done in vertical lobe slices; that is, they anesthetized the octopus by submerging it in a weak ethanol solution, removed a slice of its brain, and kept the brain slice alive in a solution of artificial seawater and antibiotics for a day before experimenting on it.

This figure shows the anatomy of the vertical lobe/MSF tract system. To make it clear, if you imagine an octopus sitting on the ground, the octopus’s tentacles and mouth would be to the right of this figure, and its mantle would be to the left.

This figure shows the location of recording and stimulation electrodes. The graphs are tracings of the voltage recorded by the recording electrode. The authors identify two signals – the large one (TP) is from neurons in the MSF tract, and the small one after it (shown in this figure by arrow heads) is from the vertical lobe neurons that the MSF tract makes synapses with. They are delayed in time simply because it takes some time for a signal to travel down a neuron. In this case, the authors measured the size of each signal, measured as the maximum height of the tracing.

This is a summary of the results of this experiment. After repeated stimulation, most of their test preparations showed a large significant increase in the strength of the synapse, meaning that the same presynaptic signal generated a larger postsynaptic signal. This is a sort of weird graph, so let me explain it: the horizontal axis shows the significant of the trial - the ones to the left are significant, whereas that group on the right is not significant (meaning they didn't actually show any change.) The vertical axis shows how strong the synapse was after LTP-inducing stimulation, proportional to how strong it was before - that is, "2" means that the synapse is twice as strong after stimulation as it was before, "3" means it is 3 times as strong, etc.

In this figure, the top graph represents the size of the recorded signals in postsynaptic neurons of the vertical lobe (that is, field-type postsynaptic potentials, or fPSP.) The bottom graph represents recordings from the presynaptic MSF neurons. The arrows show the beginning and the end of LTP-inducing stimulation. This figure is very informative, as it shows us that the synapse is indeed selective strengthened. The presynaptic signal (TP – bottom graph) does not increase, but the postsynaptic potential (fPSP – top graph) becomes at least twice as strong as it was prior to stimulation. To sum it up, the presynaptic signal stays the same, but because the synapses have become better at transmitting the signal, the postsynaptic signal is larger.

This is good evidence that LTP takes place in the memory system of the octopus brain, and could account for the memory of octopuses, as we suspect it accounts for much of the memory ability of humans. The rest of the paper is spent elucidating possible mechanisms which could account for the observed LTP, as well as verifying that it is actually LTP and not just an artifact of their procedure – I don’t have the time to go through this at the moment, mostly because it involves a wide array of neurophysiological techniques, which are a workout to explain in and of themselves. (For the curious neurophysiologically-minded readers, I'll summarize: they find that there are both postsynaptic and presynaptic mechanisms that contribute to LTP in octopuses, as in vertebrates. It is also demonstrated that LTP in the octopus involves a large increase in intracellular calcium concentration, as in vertebrates. Unlike in most vertebrate systems, however, LTP in octopuses is not NMDA-type receptor dependent, although the authors don't offer an alternative explanation. This is neat, because it suggests that the same sorts of neural systems are likely to evolve with some wiggle room as to the specific mechanisms of their functioning.)

Why does this study matter? It implies that this specific type of organization and functioning of a memory system is somehow “special” – that is, it works so much better than an alternative arrangement that it was selected for in (at least) two independent cases. In terms of studying octopus biology, it also means that the great wealth of information on vertebrate neural systems is likely to be applicable (at least in a modified form) to the study of cephalopod nervous systems. In terms of studying vertebrate biology, it is possible that studying how this system work in octopus could give us new insights into the function of vertebrate memory systems. Lastly, the methods used in this paper are just incredibly cool. C’mon, people – keeping octopus brains alive in a bath! Imagine how awesome it would be to explain your job to somebody at a dinner party if you were the experimenter.

If you read this and find yourself with any questions, or noticing any errors, please let me know. I know this was a bit technical, but I think it’s misleading to present science as if it were possible to really grasp it without being at least a bit technical. I think to really understand the importance of research like this, you have to understand the procedures used, at least basically. In any case, I hope this post was informative and interesting.

Thanks for reading!

Detour Experiments in Octopus

2010-05-27T12:51:00.002-04:00

Today I’ll review the earliest Octopus behavioral research study I could find (that is, except for a few very old papers in French, that I shamefully do not have the skill to read, although I am working on translating a few of them, bit by bit.) This is a study by Paul Schiller published in the Journal of Comparative Psychology in 1949, titled “Delayed Detour Response in the Octopus”. It’s a very early experiment on the ability of octopus to apply detours to a learned task (that is, you teach the animal to go somewhere for a reward, usually food, and then you put a barrier in its way. Depending on the character of the animal’s “intelligence”, it may or may not be able to successfully pass the barrier to get the reward.) If you have access to scholarly databases, you can probably get ahold of it (I got mine for Scirius, and I think Ovid has it as well) – unfortunately, I can’t link to a free .pdf of the article here.

Interestingly, Schiller begins his description of his methods by describing a procedure that does not work with octopus:

                    The conventional technique of using two inverted cans, one covering a baited, the other
                    an unbaited container, both of them previously exposed to the vision of the octopus, was
                    tried on 4 animals with rather discouraging results. Both cans were attacked and lifted indiscriminately
                    or, if not far enough from each other, simultaneously. This happened often
                    even in the preliminary stage when the covering cups were transparent. The tendency to
                    crawl in or lift up the containers was so powerful that the animal did not regard the bait at
                   all unless specifically trained to do so.

This makes a lot of sense – it turns out, as shown in this and later experiments on octopus, that their top performance in response-selection tasks is somewhere around 70-80% correct responses. They are “curious” enough that they will choose to investigate the “wrong” stimulus regularly. This makes sense for a foraging, active predator, who is more successful if they inspect many new areas of their environment than if they are entirely predictable.

Shown in this figure is the apparatus he settled on. The octopus is confined in the starting compartment and allowed to investigate a crab in a beaker through a screen. Then, the entrance door is opened, and the octopus learned to move through the opaque corridor to receive the crab. It was found that, after learning this, Schiller’s octopuses made 75% correct responses – well above chance (which is 50%, in this set-up.) Furthermore, Schiller found that the longer it takes the octopus to get through the corridor, the worst its chance of being correct. He also finds that, using a female whose reward is returning to her nest instead of a crab, that disorientation of her body posture by making her crawl through a small hole destroyed her ability to make the correct choice in the delayed detour task:

              It seems, with this one animal now under the more powerful motivation of her
              nest instead of food, that a delay of at least one minute does not interfere with
              the correct choice. The same amount of delay, however, if it involves disorganization
              of the bodily posture while in locomotion, prevents a successful delayed
              choice. There is no need to assume central representative factors for the delayed
              detour performance which, in the octopus, may be mediated by locomotional
              cues.

Basically, although we can explain detour performance in (for example) rats by showing that they probably have some flexible internal representation of the test space (see Tolman's discussion of cognitive maps for more information,) it appears that this same ability in octopus can be explained by intervening postural and sensory cues, without recourse to more complicated cognitive processes.

Thanks for reading!

The "Devil-Fish"

2010-05-26T11:58:00.010-04:00

While working on a bigger post about the timeline of Octopus behavioral research, I came upon this book - "The Octopus; the 'Devil-Fish' of Fiction and of Fact". Read it here on the Internet Archive – it’s available in several formats.

This piece is a colorful account by one Henry Lee of his experience with Octopuses (more properly, about some specific octopuses “with whom [he has] been on friendly terms”.) He has great, livid descriptions of octopus behavior in here, such as his account of feeding an octopus a crab against a pane of glass, so that the process could be observed:

Not a movement, not a struggle was visible or possible : each leg, each
claw, was grasped all over by suckers — enfolded in them — stretched

out to its full extent by them. The back of the carapace was

covered all over with the tenacious vacuum-discs, brought together

by the adaptable contraction of the limb, and ranged in close

order, shoulder to shoulder, touching each other ; whilst, between

those which dragged the abdominal plates towards the mouth, the

black tip of the hard, horny beak was seen for a single instant

protruding from the circular orifice in the centre of the radiation

of the arms, and, the next, had crunched through the shell, and

was buried deep in the flesh of the victim.
All in all, it’s an entertaining and informative (although scientifically questionable) read, and is one of the earliest description of octopus behavior that I have yet found free full text for - Aristotle’s descriptions in “The History of Animals” notwithstanding, a translation of which is available at the link, if you’re interested.

The Squid Giant Axon

2010-05-26T01:50:00.005-04:00

This post is dedicated to the squid giant axon (not the giant squid axon, although there is presumably a giant squid giant axon – and it’s really big!) These axons carry information to the muscles of a squid’s mantle when it is startled, causing them to contract and jet to safety. These axons are notable because they are so large – up to 1mm in diameter. If this doesn’t seem large to you, consider that typical axons in humans are only a few micrometers in diameter. The squid giant axon is several hundred times larger than the typical human axon. You can see the axon in question in this diagram, labeled “III” (It turns out that the axons commonly studied are the third step in the chain of large axons that carry this specific information; hence they are often referred to as “tertiary giant axons.”)

If you haven’t heard of the squid giant fiber system before, you are probably thinking “So what?” Well, I’ll tell you what. Nowadays, we have technologies that let us interact with various neurons in various ways. For example, we can use tiny glass pipettes to inject current or voltage into a neuron or record its activity. We can use arrays of electrodes to do the same thing with a large population of neurons. These procedures are rather routine in neuroscience, and are done with many different types of neurons in a great variety of animals and specific preparations.

When J. Z. Young was dissecting squid in the 1930’s, however, the techniques available to him were not so refined. He devised a way to isolate a single neuro-muscular unit from the rest of the squids anatomy and manipulate it (see The Function of the Giant Nerve Fibres of the Squid for his description of the procedure – I highly recommend this article, as he’s a great writer and it really is a classic in the history of neuroscience.) Although there were already theories of action potential conduction (notably, Bernstein’s theory that action potentials propagated due to changes in ions flowing across the cell membrane, which turned out to be correct,) Young’s preparation allowed him to directly demonstrate basic properties of single nerve cells. This allowed theories about neuronal function to be empirically tested at a whole new resolution. For example, in the paper cited above, he clearly demonstrates the all-or-none nature of action potentials (that is, when neurons are stimulated, they have a binary response: they either send an action potential down their or they don’t. There are no graded, partial responses.)

Young’s technique opened up the squid giant axon as a model system for many investigators who were trying to understand the behavior of neurons. Notably, Hodkin and Huxley developed a quantitative model of the propagation of action potentials using this preparation, in a famous series of papers that are summarized in A Quantitative Description of the Membrane Curent and its Application to Conduction and Excitation in Nerve. Essentially, the squid giant axon preparation gave researchers an incredible tool, with which they developed the basic models and techniques (for example, the development of voltage clamp by Kenneth Cole in the 1940’s, which allowed the ionic basis of action potentials to be investigated.)

In short, the basic electrophysiological techniques that are in use today almost all stem from Young’s work with the squid giant axon.

On a tangentially related note, Young spent much of the rest of his career trying to convince the scientific community that invertebrates, especially cephalopods, were good model animals with which to study neuroscience. At length, he’s convinced me, as well as (at least some) contemporary scientists, as evidenced by this recent review of the octopus as a model organism for studying memory systems (The Octopus: A Model for a Comparative Analysis of the Evolution of Learning and Memory Mechanisms ).

I have my own ideas about why it’s particularly good to study octopus; but alas, that’s for another post.

Cephalopod Systematics

2010-05-25T18:03:00.013-04:00

Before studying an organism, you have to know a bit about where it sits in the phylogenetic tree (that is, how it relates to other animals in the grand scheme of evolution.) Phylogeny is determined by studying morphology, physiology, and (more recently) genetics of organisms. As new organisms are discovered and known ones are studied, biologists fit the into phylogenetic categories that show approximately how they are related to each other. The Tree of Life website (http://tolweb.org/) attempts to construct a complete, interactive phylogenetic tree – it’s pretty fun, and I’ll be using their diagrams throughout this post.

Let’s get started, shall we?

I’ll start by saying that cephalopods are molluscs. They have, like all molluscs, a bilaterian body plan (that is, their bodies are basically laterally symmetrical,) a chitinous shell (although this has been internalized in most cephalopods,) a mantle cavity, and two pairs of main nerve cords.

Cephalopods are differentiated from other molluscs in that they all have a funnel derived from the molluscan neck region, a ring of arms derived from the molluscan foot, chitinous beaks, a shell, and image-forming eyes (although I seem to remember reading about an octopod that only has cup eyes – that is, eyes with no lens, which cannot form an image.) As a heuristic, you can think about cephalopods as including squids, octopuses, or nautiluses.

Within Cephalopoda, there are 5 subdivisions; of those, Nautiloidea and Coleodia still have living representatives, while endoceratoidea, ammonoidea and actinoceratoidea are all extinct nautilus-like groups.

Nautiloidea contains the extant and extinct nautiluses, animals with a chambered spiral shell and a funnel that is not fused but made of two flaps (you’ll see what I mean later – squids and octopods have funnels that are smooth tubes.) The nautilus is often spoken of as the most primitive or most ancient of the cephalopods, due to its resemblance to extinct cephalopods that appeared early in the fossil record.

Notice the funnel, the many arms, and the eye – importantly, it has no lens. It forms images the way a pinhole camera does; thus it is called a pinhole eye.

Now we get into the good stuff. The living Coleoidea are divided into decapodiformes (or decapods) and octopodiformes (or octopods). Decapods have 8 arms and 2 tentacles (for a total of 10 appendages) while octopods have 8 arms and no tentacles (with the exception of the vampire squid, which has 2 modified tentacles). Decapods include squids and cuttlefishes, while octopods include all octopuses.

Let’s start with the decapod family tree.

Decapods are divided up into 6 groups:

Bathyteuthoidea are a group of small squids that live mostly in the open ocean.

Idiosepiidae are a small group of cuttlefish (only 8 species) that live on west pacific coastlines. Their distinguishing feature is an organ on their dorsal side that they use to anchor themselves to seaweed.

Myopsida contains two subgroups – Australiteuthidae and Loliginidae. Australiteuthidae are a type of miniature squid found off of the coast of Australia (if you couldn’t tell from the name.) Loliginidae contains a variety of genera, and these are generally what you think of when you think of squid. Of particular note, Loligo vulgaris is in this group. This species is widely exploited for food (historically, for its ink,) and has been widely studied by marine biologists and neuroscientists. It was this guy that the squid giant axon was isolated from (I’ll write a separate post about that.)

Oegopsida contains a large variety of open-ocean squids – notably, a lot of really cool deep-ocean squids like the Glass Squid and the Giant Squid. I won’t get further into Oegopsid systematics now, as this is already a long post.

Sepioidea contains the cuttlefishes, most of which have internalized shells called “cuttlebones.” These guys hold the title of the cutest cephalopods, at least in my book. If you don’t believe me, check out the Striped Pyjama Squid. Even the name is cute!

Lastly, spirula contains a single species of squid that has a unique internal coiled shell.

Now, moving onto the octopods. These are my personal favorite. I think they are the smartest (or at least the most behaviorally adaptable) cephalopods.

The living octopods are all divided into two groups: octopoda and vampyroteuthidae. Vampyroteuthidae contains a single species, the Vampire Squid. Although this guy is undoubtedly cool (as seen in this clip from Planet Earth), I find octopoda to be more interesting, if only because they have been studied much, much more.

Octopoda is further subdivided into cirrata (which are a small, poorly studied group of deep-water octopods) and incirrata (which are “conventional” octopuses.) There are a great variety of species in the group incirrata, but the most important one to note (in terms of neurobehavioral research) is Octopus, particularly Octopus vulgaris. A great deal of research has been done on this guy, including a comprehensive anatomical study of the central nervous system by J. Z. Young (one of the greats of neuroscience – I’ll have to write a separate post about him, too.)

There you have it. This was a great review for me, and it should set the stage for any other discussion of cephalopod behavior or physiology. It’s immensely important in biology and neuroscience to think about the organisms you study in terms of their evolutionary history, and phylogeny guides us through that history. Hopefully this was informative for you!

Also, let me know if I've made any glaring mistakes, please!

First Post

2010-05-25T16:14:00.002-04:00

I like cephalopods, especially octoposes, for a lot of reasons; so much so that I've decided to author a blog about them.

First, though, a bit of background about myself: I'm a student at the University at Buffalo in the Psychology and Pharmacology departments. I came to my interest in cephalopods through a passing interest in comparative behavioral neuroscience (that is, the study of how the nervous system control behavior across a variety of species.) That passing interest turned into a burning interest, and now I'm hooked on cephalopods (I'll post more about why I love them so much). That brings us pretty much up to speed.

This blog is my attempt to systematize and clarify my own learning about cephalopods. I hope I can entertain and inform other people at the same time, and share all the wonderful knowledge that has been gathered about these creatures. That said, my interest in cephalopods is primarily scientific – I'll try to stay close to the primary literature wherever I can, and I might get jargon-ey at some points, although I'll try to explain myself as much as possible.

Thanks for reading, and I look forward to learning more and more and more with you! I'm working on two posts right now, one about cephalopod systematics (that is, their classification as organisms) and the other about the importance of the cephalopods, especially octopods (that is, cephalopods with eight appendages,) in comparative neuroscience and comparative psychology.