Cephalove

Here it is, finally: the post you’ve been waiting for. Having already convinced you that you should care about the possibility of consciousness in cephalopods in Part 1 and having briefly outlined the state of research on consciousness in non-human animals in Part 2, I’ll get right down to it and discuss the possibility of consciousness in cephalopods in this post. If you’re unfamiliar with the topic, I suggest reading Parts 1 and 2 of the series – in this article, I’ll be very brief with explaining some concepts that are explained in more detail there.

In this post, I’ll reference Jennifer Mather’s 2008 article (which I can’t recommend highly enough) “Cephalopod consciousness: behavioural evidence” and Edelman and Seth’s article (which is also an excellent read) “Animal consciousness: A synthetic approach”. These are both review articles, so I’ll be citing their descriptions of other people’s experiments a lot – I know this is bad practice, but hey, this is a blog – I can get away with it. I’ll cite a research study itself if I discuss it detail, but I’ll mostly be sticking to the arguments outlined in these two papers.

If you’ll remember from the last post in the series (and I’m sure you do, but I’ll summarize here anyways,) there are several methods that researchers use to get at the question of consciousness. Most directly, there is accurate self-report, whose use is limited to animals with whom we can communicate through language. This is not a useful approach with cephalopods, who (thus far) are not known to use language.

In the absence of language, animals can be trained to report on their experience (such as by performing a task for a reward when they detect a certain stimulus.) This approach is not well developed in cephalopods. Octopuses have been trained through reward and punishment to attack certain stimuli and not others in many studies; despite this, there is no protocol (that I know of) that to train octopuses with a task that would allow hypotheses about the animal’s awareness of its own experience to be tested directly in the ways that has been done for primates (for example.) Nevertheless, there is some evidence suggesting that cephalopods may be consciously aware from studies that use specific trained tasks.

Mather makes the point that the ability of cephalopods to learn a variety of tasks reliably and quickly, and then to forget them afterwards, makes them good candidates for at least primary consciousness because it implies the sort of behavioral and cognitive complexity that appears to be associated with consicousness in vertebrates. As an example of this, when experiments on visual discrimination in the octopus were done (mostly by M. J. Wells in the 1970′s and earlier,) experimenters attempted to discover the basis by which octopuses discriminated between two visual stimuli. In a sense, they were looking at how the octopus categorized stimuli. A number of hypotheses were generated to explain this within a simple, computational framework, but it was eventually concluded that octopuses (that is, individuals of the species O. vulgaris, the common octopus) don’t use a set of simple rules to categorize objects. Rather, Mather argues, they “[evaluate] a figure on several dimensions and [generate] a simple concept, where [a] concept is an abstract or general idea inferred or derived from specific instances.” Other evidence for the ability of cephalopods to exhibit learning like that taken to indicate cognitive ability (and thus the potential for consciousness) in vertebrate species comes from more complex learning tasks. The spatial learning abilities of cephalopods have been studied and it has been found, in general, that they might be capable of spatial learning to rival that of commonly used vertebrate laboratory species (such as rodents,) as long as the apparatus used is adapted to their capabilities (obviously, we cannot expect a rat and a cuttlefish to learn the same things in the same circumstance, but both can show impressive spatial learning given the right circumstances.)

Consciousness can also be suggested by non-trained behavior of an animal. As I’ll address at more length in a little bit, such evidence in cephalopods is found in accounts of their foraging behavior, their responses to novel objects in their environment, and the presence of sleep-like (and possibly REM-like) states. Most convincingly, in my mind, is the evidence suggesting the superior behavioral flexibility of cephalopods.

One of the more straight-forward tasks that is used to suggest conscious awareness in human and non-human alike is the mirror self-recognition task (MSR). What happens when you show a cephalopod a mirror – does it recognize itself, or does it treat its reflection as if it were another animal? Mather cites a personal communication suggesting that cuttlefish fail the MSR. You can see for yourself, in this great video of a cuttlefish at Epcot being shown its own image on an electronic screen. It turns very dark and pursues its image as if it were confronting another cuttlefish. The mechanics are a bit different, but it’s essentially similar to the MSR:

Mather makes a case for the cognitive abilities of cephalopods using the results of a study that looked at the strategies that octopuses use to open bivalves (which she discusses in this interview on Scientific American.) Not only do octopuses use different techniques for opening clams of different species (that is, they pry open the shells of the weaker ones, and drilling holes through the shells of the stronger ones, but they could switch strategies if one wasn’t working properly. When the experimenters took the clams that the octopus normally ate by prying open and wired them together so that they couldn’t be opened, the octopus figured this out and started drilling. This sort of behavioral flexibility, particularly the selection of one possible behavior among many on the basis of its effectiveness in a specific situation, could be attributed to some sort of centralized “executive processor” that might associated with consciousness.

Although definitions of “play” are often disagreed-upon, Mather argues that some octopuses have been observed playing with objects. While the existence of play behavior in a species is not indicative of consciousness, it suggests the possibility of consciousness; object play is, as Mather says, “something that intelligent animals do” to allow them to learn about things in their environment. (You can read my discussion of one study of octopus play at this link.)

It has also been (rather famously) argued that some octopuses have evolved the ability to use tools – specifically, one species of octopus (Amphioctopus marginatus) has been seen carrying empty coconut shells across the sea floor, which they use as mobile shelters. It can be argued that tool use is only possible when the animal using the tool has developed some rather sophisticated cognitive awareness of their surroundings that allows them to appreciate how an object can be used for a certain function. Here’s a video of this behavior, taken by one of the authors of the 2009 paper on the subject:

The comparative neuroanatomical argument for consciousness (epitomized by Panksepp’s “triangulation” approach to the problem, which recommends using affective, behavioral, and neural approaches together to infer consciousness in non-humans) is much more difficult to make for cephalopods than it is for vertebrates. The reason for this is simple: humans are vertebrates, and share many features of the anatomical and functional organization of our brains with other vertebrates. If you dissect a rat brain and a human brain side-by-side, most of the parts in one of them will show up in the other one in some form. Thus, it is rather easy to make an argument from analogy claiming that, because the brain activity and behavior of the two species in some situation are similar, it is likely that their experiences are likely to also be similar. It is harder to make this argument between people and cephalopods, because there is no direct equivalence between any of the parts of a cephalopod brain and the parts of a human brain, with the possible exceptions of the retina and primary visual processing areas of the two species and some parts of memory systems (eg. the vertical lobe system in cephalopods and the hippocampus in humans.) Even these are examples of convergent evolution (meaning they started from different places and got the same functional result,) and so the equivalences between these two brain areas in cephalopods and humans are only approximate, and based on a very limited knowledge of the functions of the cephalopod brain. Despite this difficulty, there are some overall features of the cephalopod brain that suggest consciousness, including its apparent organization as a complex integrator for sensory information, its lateralization, and its patterns of activity during sleep and wakefulness.

Edelman and Seth argue that we have a good reason to suspect that birds have some sort of consciousness, based on apparent anatomical and functional correspondence between the brains of mammals (including humans) and birds. They show this figure, which illustrates this correspondence – it shows diagrams of a human brain and a finch brain, with homologous structures colored similarly in each diagram:

As you can see, human and zebra finch brains (and indeed, mammalian and avian brains in general) have somewhat similar layouts, which allows one to make an argument for the inference of similar subjective states that correspond to certain types of neural activity in multiple vertebrate species. The basic logic is simple: if the brains are similar, and most of the output of the brain (that is, behavior) is similar in a certain situation, the rest of the output of the brain (that is, affective and/or conceptual awareness, eg. consciousness) is reasonably likely to be similar.

At the bottom of the figure, though, they show the octopus brain. Notice that it’s done in a completely different color scheme. This is because the functional or anatomical subunits of the octopus brain are not clearly equivalent to those found in vertebrate brains. A few localized functions of the octopus brain can be compared to those of vertebrate brains – for one, the vertebrate retina and the octopus optic lobe have apparently analogous structures and functions (that being the initial processing of visual information,) and the vertical lobe/medial superior frontal lobe system of the octopus is known to be involved in memory consolidation, and may have a microscopic structure that resembles that found in the mammalian hippocampus (for more info on this, check out Young, 1991, who makes the argument that the cellular structure and computational properties of the mammalian hippocampus might resemble those of the octopus memory system.)

Functionally, however, it is possible to find similarities between cephalopod brains and vertebrate brains, even if it is difficult to do so anatomically. Mather discusses the evidence for lateralized specialization of function in the cephalopod brain at length (that is, the general feature of the brain that two mirror-image halves can work somewhat independently, and may have different functions.) Lateralization is seen in humans and other primates, and seems to be one evolutionary result of the need for cortical tissue to be both locally differentiated and highly interconnected; it allows for more specialized cortical areas, because the right and left sides of the brain need not be functionally equivalent. Thus, the apparent laterality of the octopus brain (as this is already getting on in length, I’ll let you check out Mather’s article for a more complete discussion) might suggest that it has also evolved the sort of complex cognitive capacities that lateralization is associated with in mammals.

Finally, EEG-like recordings have been done in both octopus and cuttlefish, leading to the general (but very preliminary) finding that cephalopods have complex, low-frequency “background” electrical activity in some parts of their brains that seems to vary with their states of consciousness. In addition, they show sensory-evoked changes in this activity, in the same way that human EEGs do. This suggests that some of the gross functional properties of the cephalopod brain might resemble those of mammals on a system-wide level.

All of the arguments by analogy should be taken with a grain of salt, because while it is interesting to consider the possible theoretical importance of the apparent similarities between octopus and vertebrate brains, it seems premature at this point, given how little we know about them. While laterality, distributed low-amplitude electrical activity, and a certain kind of memory system architecture are found in the brains of animals who are almost definitely conscious (eg. mammals and birds,) it’s hard to say that their presence in such highly divergent nervous systems (eg. those of vertebrates and cephalopods) has the same set of functional consequences in all cases.

So there it is – these are the arguments for consciousness in cephalopods. It’s an astoundingly complicated and difficult question, and one that I’m sure I haven’t done justice to. Look for the last planned article of the series later this week, where I’ll reflect upon these arguments and figure out where I stand (and also hopefully invite discussion) on the science of cephalopod consciousness.

Thanks for reading!

P.S. Today is my first day of classes for the Fall semester. Wish me luck!

MATHER, J. (2008). Cephalopod consciousness: Behavioural evidence Consciousness and Cognition, 17 (1), 37-48 DOI: 10.1016/j.concog.2006.11.006

Edelman, D., & Seth, A. (2009). Animal consciousness: a synthetic approach Trends in Neurosciences, 32 (9), 476-484 DOI: 10.1016/j.tins.2009.05.008

Young, J. (1991). Computation in the Learning System of Cephalopods Biological Bulletin, 180 (2) DOI: 10.2307/1542389

Finn, J., Tregenza, T., & Norman, M. (2009). Defensive tool use in a coconut-carrying octopus Current Biology, 19 (23) DOI: 10.1016/j.cub.2009.10.052

This is part on of my series looking to answer the question: “Are cephalopods conscious?” In this post, I’ll try to pin down just why it matters whether or not cephalopods have consciousness.

Consciousness is a difficult term to define, but (working from the Stanford Encyclopedia of Philosophy page on the subject) it seems to be best captured by the criterion of awareness. A conscious creature is one who is aware of the world, who has some subjective state which allows them to experience things. More strictly, we might say that a conscious creature must be aware of itself – it must have some notion that it exists, and that it is separate from the rest of the world. Obviously, the ability to have complex internal representations of things is generally considered a prerequisite to this sort of consciousness. This is sometimes called “cognitive ability” (perhaps more properly, the abilities to perform various tasks requiring this capacity are called “cognitive abilities”.) It does not necessarily imply consciousness, but consciousness as defined here requires that an animal to be able to form such representations of the world “before” it can be considered conscious.

Some authors use the term “primary consciousness” and “secondary consciousness” to refer to different aspects of what others call “cognition” – that is, an animal with “primary consciousness” has awareness of sensory impressions and emotions, and an animal with “secondary consciousness” can think about its experiences.  Either of these abilities might be spoken of as being part of the workings of cognitive abilities, with or without any implication in consciousness.  The primary/secondary terminology emphasizes that consciousness probably comes in many varieties that cannot always be easily described using the binary concepts of “conscious” and “non-conscious”.  This is especially important to keep in mind when talking about animal consciousness, as it is likely than other species have consciousness that is qualitatively very different from ours, but can still be identified as the same type of phenomenon.

It’s relatively easy to determine if a human is conscious; you just ask them. The fact that we can use language makes it very easy to determine if a human is currently conscious (that is, not in a deep sleep, dead, or in a coma.) In general, though, we’re comfortable making the assertion that humans are conscious. It is much harder to make this case with non-human animals (hereafter just called “animals”.) Because animals generally cannot directly report their experience to us – or because we cannot understand their reports well enough – we have difficulty knowing from an animal’s behavior whether or not it is conscious, or how to characterize its possible consciousness. We can determine the extent of an animal’s cognitive abilities relatively routinely using a variety of tests. This approaches the problem of consciousness tangentially, and from these tests we derive most of our information about the possibility of consciousness in animals. I’ll get more into this in Part 2 of this series of posts. For now, another question is at hand:

Who cares? Why in the world should we be concerned with the mental states of animals? In particular, why do we want to know if cephalopods are conscious?

I’ll answer this question two ways: first, as a scientist, and second, as an ethicist.  There are probably other reasons to care, and I cannot cover either of the ones I have chosen exhaustively.  In any case, let’s press forward:

Scientifically, the question of animal consciousness (mostly studied these days in terms of animal cognition) is exceedingly important to neuroscience, zoology, psychology, and biology-in-general. If we accept the dogma of neuroscience, specifically that the nervous system is responsible for all of the behavioral and mental processes of an animal, then it must be that the brain of an animal is responsible for that animal’s consciousness (humans included.) If neuroscience is supposed to learn how the brain works, then it within the goals of neuroscience to understand how the functioning of the brain gives rise to consciousness. As neuroscience is not just about human nervous systems, but nervous systems in general, it is important that we know whether animals are conscious, and if so how this consciousness might differ from or be similar to our own consciousness.

Besides being a good subject for science fiction movies, “solving” consciousness in terms of neural function would also be a huge theoretical milestone for neuroscience and computer science. It might allow us to construct computers that were conscious, and could perform tasks with human-like (or even animal-like) intelligence. Because consciousness is widely thought of as one of the most complex and integrative brain functions (that is, it involves the action of a very large and very variable group of brain areas and functions,) it is likely that, by the time we reach this goal, we will have solved most of the rest of the functions of the brain as well. Thus, understanding consciousness is an important goal in neuroscience.

In zoology, ethology, and psychology, all of which attempt (at least in part) to understand behavior, the question of animal consciousness is central. If animals use conscious processes to make decisions, then it is appropriate (and indeed, necessary) that we identify these and study the animal’s behaviors on these terms. As it stands, cognitive processes are recognized throughout a wide swath of the animal kingdom, but we have yet to reliably extend our inquiry to consciousness. Thus, understanding if and how animals are conscious is important to understanding animals and their behavior in general, which is the goal of these disciplines.

Why cephalopods, though? As I’ve harped on before (for example, here, here, here, and here,) cephalopods are a unique group of model animals in the comparative study of the brain and behavior. Most of the anatomy (and presumably the function) of their nervous systems evolved independently from the other animals we usually grant “cognitive” or “conscious” status to (eg. birds, mammals, and possibly reptiles.) When we theorize about the relationship between neural function and cognition, we can use cephalopods as a way to test our theories about what sorts of neural circuits and/or patterns of activity correspond with different cognitive faculties and conscious states. This is only true if, in fact, cephalopods can be conscious. As far as cephalopods are generally useful in developing theories of behavior and brain function in general, they are useful in the scientific study of consciousness – that is, if they are conscious. Thus, determining whether cephalopods are or are not conscious is important to the future of the comparative study of behavior and cognition.

Finally, the question of cephalopod consciousness has implications for how humans should use animals – that is, in terms of the ethics regarding the way that humans interact with other animals. Panksepp (2005) lists 5 reasons for studying affective consciousness (while he’s interested in emotions, many of the same arguments apply to consciousness in general,) including the following: “an understanding of affect in the lives of other animals may be critical for making informed choices on how we ethically treat other creatures… By failing to study such issues, we may continue to deny animals the respect they deserve.”

If we are going to have a rational ethics that can instruct us as to what is permissible and what is not permissible to do with animals (a goal that all of us should have,) we need to know if animals experience the world, and if they do, how they experience it. The ethical stance most commonly taken when looking at the use of animals by humans, welfarism, has at its center the idea that the suffering and discomfort of animals should be considered when using animals; specifically, the suffering of any animals that people use should be minimized. The focus is on the “welfare” of the animal, which means its general well-being, comfort, and quality of life. This is different from the case for “animal rights”, which ascribes to animals rights not to be treated as a means-to-an-end that, like the rights we ascribe to people, would prevent them from being ethically used by humans at all. As (for example) researchers, farmers, and the pet industry are still using animals, and they (and by proxy, all of us who make use of their discoveries and products) depend on the continued use of animals, we mostly reject the latter argument, focusing on the welfare of animals instead of the rights of animals. It’s a somewhat subtle distinction, but it’s important. From a welfare-based perspective, which is based on preventing suffering, it is important to know how animals can suffer. It seems likely that having self-awareness can allow an animal to suffer in more and possibly deeper ways – for example, from loneliness, self-pity, shame, boredom, unfulfillment, anger, and so forth. Thus, the question of animal consciousness is important to animal welfare-based ethics. From a rights-based perspective, the consciousness of animals is not as important. The supposed right of animals not to be used by humans is intrinsic to sentient animals (that is, animals who can sense and react to their environment.) From this viewpoint, regardless of their specific capacity for cognition or conscious awareness, these animals should be protected from human use. I’ll just (for convenience, because it’s what I believe, and because it’s the dominant view, socially speaking) adopt a welfarist perspective on the ethics of the use of animals.

How does this apply to cephalopods? Well, humans use a lot of cephalopods. More than 4 million tonnes of cephalopods were harvested from the oceans in 2007, according to the FAO yearbook of Fishery and Aquaculture Statistics for that year. Perhaps particularly troubling, depending on the capacity of cephalopods to suffer, is the practice of eating extremely fresh cephalopods – that is, those who are still alive (or killed/incapacitated just prior to eating,) which, as a quick YouTube search will attest, is not unheard of in southern Asia and maybe elsewhere. In addition to their use as food, smaller numbers of cephalopods are kept as pets, as research animals, and in aquaria. If the study of the possibility of consciousness in cephalopods is necessary to inform our ethics regarding how we treat cephalopods (and it seems like it is, given how important consciousness appears to be to our common-sense notions of “suffering”, and even some philosophical formulations thereof) then we should get on the ball and pursue this research.  That is, if we accept the welfarist position, and we want to have a scientifically reasonable ethical viewpoint, both of which I think are relatively conservative assumptions.

I should note, before I finish this up, that the science of animal consciousness and the ethical question of animal consciousness relate to each other, but make different assumptions. Scientists are necessarily conservative about making positive assertions, and for good reason – it’s bad science to speak as if a thing (like consciousness in non-human animals) exists if there’s not some positive evidence for it. Put another way, scientific theorizing is set up to rigorously avoid false positives. On the other hand, in a system of ethics that is based on preventing suffering, it’s more important to avoid false negatives than to avoid false positives. In making an ethical decision about a certain animal (or person,) one would rather accidentally treat an agent that doesn’t need ethical considerations as if it does than to unwittingly subject that agent to undue suffering by assuming that it doesn’t have the capacity to suffer in a certain way. Thus, welfare ethics demands that we fastidiously avoid false negatives in the case of consciousness and other psychological phenomena that might determine an animal’s capacity to suffer, even at the expense of occasional false positives.  Essentially, given no other information than our impression that animals might have consciousness, a scientist should assume that they don’t, and an ethicist should assume that they do.  The best solution to me seems to be to entertain both ideas, and apply them to different problems as the specific problems demand it.

I suspect that this mention of the ethics of using cephalopods will garner more attention than the discussion of the scientific value of the study of consciousness in cephalopods, if only because animal ethics is more politicized than the comparative psychology, and is perceived as somewhat easier to talk and theorize about without much technical background.  I don’t want it to seem as if I’m making an argument for or against any use of cephalopods at this point – although I think this is an important issue, I’m not trying to deal with it here.  I’ve tried to keep this post free of any ulterior agenda, and I think I’ve largely succeeded.  The next few posts will be more science-y and less philosophy-y, I promise – although it’s sort of hard when talking about consciousness, which is written about by philosophers far more often than by scientists.

Thanks for reading!

PANKSEPP, J. (2005). Affective consciousness: Core emotional feelings in animals and humans Consciousness and Cognition, 14 (1), 30-80 DOI: 10.1016/j.concog.2004.10.004

FAO Fisheries and Aquaculture Department, . (2009). Fao yearbook: fishery and aquaculture statistics 2007 (Online Version)

Let’s take a minute to talk about connectomics.  No, not genomics.  No, not metabolomics.  Not any of the other -omics, but connectomics.  It’s a new-ish field that the computational neuroscience geek in all of us can love.

By way of introduction, the “connectome” is the “network of elements and connections forming the human brain” (according to Sporns et al, 2005).  Let’s forget the part about human brain, and (for the purposes of this post) say that a connectome is the set of all the neural connections in a nervous system.  Connectomics is the subfield of neuroscience that attempts to understand the structure and function of nervous systems by studying these connections as a whole.  The goal of this discipline is to determine the anatomy of the nervous system to a very fine scale (on the order of individual cells), and then relate this structural information to the functioning of the nervous system.  “Solving” a connectome is achieved when the connections between all the neurons in a nervous system are mapped.  This has been done for C. Elegans, a nematode who has only 302 neurons, by the use of electron microscopy – this work is summarized in White et al., 1986.  Since then, we’ve expanded our goals, with the Human Connectome Project aiming to solve the connectome of the human brain.   Let’s step back for a second, though, and ask: why do we want to know all of this?

Since the elucidation of the electrical properties of neurons (which, by the way, started with the squid giant axon – you can read one of my older posts about that topic here ), neuroscientists have been interested in the information that neurons carry.  A nervous system can be thought of as an organ that processes information to tell the rest of the body what to do.  Some stimulus might impinge upon a sensory organ (let’s say, for example, that one sees a car speeding towards one’s self,) which causes a cascade of electrical activity through the nervous system, eventually leading to such diverse effects as the movement of one’s muscles to carry one’s self out of the path of the car, the emotional distress that occurs when one is almost killed by some jerk who isn’t paying attention to the road, and the realization that one has just gotten very lucky.  Later on, one might tell the story of this near miss to her friends over dinner, exhibiting the ability of the nervous system not only to process, but to store information for later use.  Further demonstrating this ability, one might learn not to walk in the middle of the road in the future.  The ability of animals to exhibit behavior, to move, feel, and learn, is all due (according to the dogma of neuroscience) to the processing of information by cells in the nervous system.

Now, it’s relatively routine to study how a single neuron processes information.  To sum it up very briefly, information enters a “typical” neuron in the form of electrical impulses on that neuron’s dendrites.  The information flows through the neuron (as an easy-to-get analogy, imagine electronic information flowing through the wire) and then a decision is made: at any given time, if a neuron is electrically excited enough, it can discharge an action potential.  An action potential is a burst of electrical activity that will travel through the neuron’s axon to affect the activity of other neurons that the axon makes synapses with.  Thus, one can imagine a general flow of information through a neuron from the dendrites, through the cell body, and out the axon.  A nerve cell is diagrammed below, with the dendrites and axon clearly labeled, showing the flow of electrical impulses through the neuron.  Such neurons are linked together to form functional circuits that accomplish complex tasks such as recognizing objects, coordinating movement, and recognizing when food tastes good or bad (to name but a few.)

Think of it this way: each neuron works like a tiny computer processor.  At any given time, it’s integrating all of the electrical signals coming to it, and deciding whether or not to fire an action potential.  Nervous systems can process information because they have many such relatively simple processors connected together to process that information.  (Keep in mind that this is a very simplified, and thus necessarily inaccurate description of the nervous system.  It will have to do for now, however, and gets across those aspects of the function of neurons that are most relevant to the problem of the connectome well enough.)  Thus, to understand the function of a nervous system, one only has to understand the functioning of each of its neurons.  This turns out to be incredibly difficult, and at best we only achieve approximations of this goal.  I’ll come back to this later on.

To study how a single neuron processes information is relatively easy, if we’re selective about which neurons we study.  For example, we could record electrical activity from the optic nerve while we expose the eyes of the animal we’re studying to light.  In this way, we would see the way that different visual signals are encoded by neurons in the optic nerve.  In fact, this has been done countless times in studies on the visual system in cats, frogs, ferrets, and many other species.  Using this method of electrical recording, we can determine how neurons are functionally connected to each other, and how they respond to various inputs.  However, to record electrical information from a neuron requires that one physically place an electrode into the brain, and also requires that one focus on a single neuron or a small subset of neurons at a time.  To figure out how an entire brain functions in terms of the interaction of millions of individual neurons would be all but impossible using these electrophysiological methods.  In addition, this method can never be employed on humans, as it is considered unethical to put electrodes into peoples brains without an urgent medical need (of course!)

Another now-classical way of learning about the connections between neurons in a nervous system is through tracer studies.  In these studies, neurons in one part of the brain are dyed in some way.  Then, other parts of the brain (or the whole brain) can be examined to see if they have dye in them.  If they do, it’s concluded that the neurons make some sort of connection between the part of the brain where the dye was injected and the part of the brain where the dye was later seen.  This has many of the same downfalls as electrophysiological methods of figuring out neural circuits.  For one, it can only be done in a small group of neurons in any preparation, and so the connections in the nervous system must be mapped out piecemeal, a few at a time.  In addition, it is often difficult to tell what route an axon might take from the cell body to its destination, even if it is clear where each of these points are.

The difficulty that these methods have in resolving the microscopic structure of the nervous system beg for a faster, more flexible technique.  Even the reconstruction of the relatively simple nervous system of C. elegans, done using images from an electron microscope, had to be done largely by hand.  These processes are labor- and time-intensive, and do not lend themselves well to the reconstruction of nervous systems that may have millions or billions of neurons.

Enter the field of computational neuroscience.  Computational neuroscientists study nervous systems in terms of their information processing capabilities.  Standing at the junction of computer science and neuroscience, they have both the tools and the impetus to understand the details of the connectomes of whichever organisms they study.

An approach that has been taken in humans involves using the technique of diffusion tensor imaging, and MRI technique that can determine the direction that axons run in in an intact brain.  For example, the following image (by Thomas Schultz) shows a DTI-derived image of the connections that run through the midline of a living human brain:

Such images are of great potential use in studying brain lesions, doing studies on brain function, clinical diagnosis, and whole-brain level analysis of neural circuits.  However, they lack the resolution needed to map individual synapses, thus falling short (for the time being) of being able to comprehensively map the connections between neurons in a brain.  For this, we have to go to microscopy techniques that involve looking directly at neural tissue.  These can only been done in animals, because it is presently illegal to harvest brain tissue from humans for experimentals purposes (again, a no-brainer.)

By now, you’re wondering when I’ll mention a cephalopod.  After all, this is a blog about cephalopods.  You have every right to expect that I’ll mention squids, octopodes, or nautiloids at least once in each post.  Never fear!

Last week I came across a poster presentation write-up on Biomed Central called “Charting out the octopus connectome at submicron resolution using the knife-edge scanning microscope.”  As you might imagine, I was tickled.  A research team with members from Texas, Naple, Michigan, Illinois, California, and Seoul (including Graziano Fiorito, notable for his research on observational learning in the octopus) is working on reconstructing the octopus connectome using a mostly-automated 3D microscope called the knife-edge scanning microscope (KESM).  This microscope takes a block of tissue and slices it, taking a picture of each slice of the tissue as it is cut.  Then, a computer program can create a high-resolution 3D image of the tissue.  From this, the computer can (and this is the tricky part) automatically trace the paths that nerve cells take through the tissue, and – this being the goal of this research – reconstruct a detailed network showing the morphology of each neuron in the tissue.  For examples of the resulting images, you can see this gallery from the brain networks laboratory at Texas A&M.

Why the octopus?  Well, in an introduction that makes the comparative neuroanatomist in me jump for joy, the authors suggest that because “the neural architecture of this cephalopod mollusk differs markedly from that of any vertebrate… [investigating] the difference and simlarities between the neural architecture – or connectome – of the octopus and mammals, such as the mouse, may lead to deep insights into the computational principles underlying animal cognition.”  In their concluding remarks, the authors note that they “expect that this pilot study and the more detailed investigations to follow will allow fruitful comparisons of the neural circuitries of individual octopuses with different ecological life histories, as well as of animals that have been exposed to a variety of neurodegenerative insults… In sum, this approach should contribute greatly to our understanding of the computational architecture of invertebrates and ultimately provide insights into the differences between invertebrate and vertebrate cognitive capabilities.”

I’m intriguied by this article, but also a little dissappointed.  Mostly, I’m dissappointed that a more complete study isn’t out yet!  I’ll be watching these guys from now on, and I’ll cover any other publications they put out on the topic.  Hurrah for octopus connectomics!

In closing, I want to mention that a complete neuroanatomical picture of a nervous system does not actually explain its computational properties.  To understand how nervous systems process information, we need to know the physiology of each cell and the biochemistry of the interactions, a topic that is probably more complex than even the very fine-grained study of neuroanatomy represented by the studies I’ve mentioned here.  In terms of our understanding of nervous systems, however, connectomics offers and opportunity to study the relationship between the cellular structure of the nervous system and its overall capabilities – a relationship whose description has been one of the goals of neuroscience practically since its inception.

Thanks for reading!

Sporns, O., Tononi, G., & Kötter, R. (2005). The Human Connectome: A Structural Description of the Human Brain PLoS Computational Biology, 1 (4) DOI: 10.1371/journal.pcbi.0010042

Yoonsuck Choe, Louise C Abbott, Giovanna Ponte, John Keyser, Jaerock Kwon, David Mayerich, Daniel Miller, Donghyeop Han, Anna Maria Grimaldi, Graziano Fiorito, David B Edelman, & Jeffrey L McKinstry (2010). Charting out the octopus connectome at submicron resolution using the knife-edge scanning microscope BMC Neuroscience, 11 (Supplement 1), 136-137 : 10.1186/1471-2202-11-S1-P136

MAYERICH, D., ABBOTT, L., & McCORMICK, B. (2008). Knife-edge scanning microscopy for imaging and reconstruction of three-dimensional anatomical structures of the mouse brain Journal of Microscopy, 231 (1), 134-143 DOI: 10.1111/j.1365-2818.2008.02024.x

White, J., Southgate, E., Thomson, J., & Brenner, S. (1986). The Structure of the Nervous System of the Nematode Caenorhabditis elegans Philosophical Transactions of the Royal Society B: Biological Sciences, 314 (1165), 1-340 DOI: 10.1098/rstb.1986.0056

MORI, S., & ZHANG, J. (2006). Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research Neuron, 51 (5), 527-539 DOI: 10.1016/j.neuron.2006.08.012

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 themselve
s 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

          (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 f
ield 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

          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

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!