Short and long-term memory in cephalopods

          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

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

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

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

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

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

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

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

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

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