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

          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

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

Cephalopod Consciousness

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

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.

The Octopus Visual System

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!