Most species of shallow water octopuses appear to be pretty solitary animals. They live in dens and venture out from them to hunt or find mates; defending these dens and getting busy are the only social interaction that many species of octopuses are observed to have in the wild. I like to think of them as the curmudgeons of the reef environment, keeping to themselves because that’s just the way they like it.
Keep movin', buddy; there's nothing to see here. (Photo by algaedoc)
It might surprise us, then, to learn that Elena Tricarico and her coworkers, working out of the Stazione Zoologica in Naples, just published a paper arguing the octopuses (of the species Octopus vulgaris), can recognize other individual octopuses. While it’s clear that this ability might be important to more social cephalopods (like squids, which form schools), what good could it do for a species with such a hermit-like existence?
It turns out that keeping to one’s self in an area where there are lots of other organisms around requires some social skills – you have to know a little about the folks around you and what behavior to expect from them. For example, if you see the same animal patrolling an adjacent territory each day, it doesn’t do much good to make a huge fuss over it all the time. If you have your territory, and she has hers, it behooves you both to be able to recognize each other so that you don’t waste time and energy chasing off somebody who isn’t actually going to cause you any problems (this is called the “dear enemy” effect.) On the other hand, if a wandering octopus comes through looking for a good nesting site, it would be useful to be able to tell that he’s a stranger so that you could drive him away and keep him from taking over your territory. Thinking about it in these terms, it makes sense that the ability to recognize other octopuses could be a useful ability to have.
To test whether octopuses could do this, Tricarico and coworkers divided up their experimental octopuses into two groups; in one group, pairs of octopuses were housed with a clear divider between them, so that they could see their partner, while in the other group the octopuses had an opaque divider. After letting the octopuses either see or not see each other for 3 days, they watched how these pairs interacted with each other when they were put into the same test tank for 15 minutes. It turns out that pairs that had seen each other before avoided each other more, touched each other less, and spent a longer time ignoring each other when they were placed in the same tank than pairs that had been separated by the opaque divider.
This alone isn’t enough evidence to conclude that octopuses can recognize other individual octopuses – after all, the pairs that could see each other might just be getting used to being around any octopus. To test whether the octopuses had learned to recognize their specific partner or just gotten used to the presence of other octopuses, the researchers did one more test – they put the octopuses back in the test tank, but this time, they put some of them in with the familiar octopus they had been seeing throughout the experiment, and some of them in with an octopus they had never seen before. What they saw was this: when octopuses were placed with another octopus that they were familiar with, they touched each other less, avoided each other more, and their interactions were shorter than when they were placed with unfamiliar octopuses. It looked as if the octopuses had learned to recognize their partner, and responded differently to them than to a strange octopus.
Like all good experiments, this one begs plenty of questions: can octopuses tell who individuals are, or do they just categorize other octopuses as familiar or unfamiliar? Does their ability to discriminate other individuals imply some sort of social cognition, and of what sort (I’d argue that it suggests only very basic social cognitive skills, but opens the door for more investigation,) and, finally, do I need to worry that someday, the octopuses will learn to recognize ME?
That's right, buddy, I'm looking at YOU. (photo by Rowland Cain)
Thanks for reading! I’d like to point out that I took the title of this post directly from the paper it discusses; it was such a good title that I couldn’t think of anything more fitting.
Elena Tricarico, Luciana Borrelli, Francesca Gherardi, Graziano Fiorito (2011). I Know My Neighbour: Individual Recognition in Octopus vulgaris PLOS One : 10.1371/journal.pone.0018710
Shallow-water octopuses are generalist predators – this means that they can eat a variety of other animals – and good ones too. They have a few different hunting strategies, with the commonest ones involving the octopus groping along the reef, feeling for food with its arms (although octopuses have been reported to hunt by ambushing (pdf link) as well, striking their prey after spotting it.) You can see the groping strategy at work in this video:
It is clear from previous research that octopus arms are capable of movement, even relatively complex movements, on their own. Thus, when an octopus gropes its way around a reef, it might be that it’s central nervous system is doing very little to control its arms; rather, it seems likely that they move mostly “on their own”. Tamar Gutnick and her colleagues at the Hebrew University of Jerusalem recently published a study that investigated if and how octopuses (of the species Octopus vulgaris) can use information from their central nervous systems to control the movement of a single arm. I’ll let them tell you about it:
(By the way, I love video abstracts/experiments. Thanks, guys!)
The researchers took 7 octopuses and trained them to reach into a clear plastic “maze” where they could choose to put their arm into one of three areas. One of the arms of the maze had a piece of food in it. Since they were only given one chance in each session – if they chose the wrong arm in a session, they weren’t allowed to try again – the octopuses learned to find the food by looking at it through the clear walls of the maze and then make the appropriate arm movements to get it. After the researchers covered the clear maze with masking tape, the octopuses, who could no longer see the food, weren’t able to do the task any more – they got about 1 in 3 trials right, exactly what you’d expect if they were choosing randomly.
The results of this study tell us that octopuses can use visual information to direct the movements of their arms, and that they seem to get more accurate with practice. What we don’t know, however, is how an octopus’s brain could pull this off. It’s clear that simple movements are controlled within the arms themselves, as a disembodied octopus arm can make some movements by itself, but it’s unclear how the “higher-up” parts of the brain that receive visual information from the eyes could mix it with tactile information from the arm to direct these sorts of movements.
The skeptic in me says that there might not be much to be excited about. After all, we’ve known that that octopuses use their vision to do things like find their way around, and size up potential food/predators for a long time. The procedure used, even if it’s new, is sort of limited; it’s essentially a simple detour task, where the animal can see its reward but has to take a complicated route to get to it. As Zen Faulkes pointed out in his post on this study, (which is so cleverly titled as to put me to shame), the octopuses weren’t even very good at learning such an apparently simple task. Compare this to the scores of learning tasks that other laboratory animals like rats (and people, for that matter) whiz through, and it seems like a small step. Some experiments using tasks like this fail while others succeed, and there’s no clear consensus as to how and why octopuses learn (or fail to learn) in certain situations, making it even harder to say anything about how octopuses learn.
Nevertheless, there’s some room to be excited; it’s a small step into an mostly unexplored field. Think about just how foreign an experience this was for the octopuses in the experiment – not over the time scale of the experiment, but over evolutionary time. For millions of years, the ancestors of this species have been hunting on the seafloor in shallow waters, where it’s very unlikely that they’d ever encounter a hard, transparent surface that they might have to move around to get food. Even still, when they’re presented with such a situation, they can navigate it, even if they do it with some difficulty. The behavior of these octopuses, then, seems to me to have evolved not only to work well in a specific situation, but to work (at least minimally) in a wide range of situations – their behavior has evolved to be somewhat flexible. In fact, this is a strategy that is used by all animals that can learn (which seems to be most of them) that helps them deal with the fact that there is no such thing as a perfectly stable and predictable environment, and that behavior needs to adapt to deal with this. For example, your ancestors (if you were an octopus) might have fed on a few specific species of crab for the past few hundred years – if something about the environment changes, you need to be able to learn to hunt something else, or you (and your species) are doomed. Looking at it in this light, it’s not very surprising that a laboratory filled with mazes and puzzles built by scientists would push the limits of a cephalopod’s behavioral flexibility – this is a huge change from the environment the animal evolved in. To quote Zen Faulkes, “the point is not that the animals are slow to learn; the point is that they can learn to do this at all.”
This research is also exciting because it begs questions about how the nervous system of the octopus can do this task. In more familiar research animals (that is, mammals), we know that specific parts of the brain (areas of the motor cortex) control the contraction of specific muscles. Besides this, we’ve identified a whole host of brain structures that play various roles in putting together these movements and in using information from the muscles, skin, and eyes to control and refine them. In mammals, both motor and sensory systems are put together in a such a way that their arrangement in the brain corresponds to their arrangement in the body – this is called somatotopy. (Check out this neat little demonstration of the concept by Jaakko Hakulinen.)
According to another study published in 2009 by researchers from the same university, this doesn’t appear to be the case with the octopus. The investigators in that study couldn’t find any clear relationship between activity in different parts of the octopuses’ brain and different movements. While we know where the information from the eyes goes in the octopus brain (to the sensibly named “visual lobes”,) it’s unclear where it goes from there or how it might interact with the neurons that control the arms, or how this information might be put together with sensory information from the arms. How exactly an octopus’s brain uses vision to control ongoing movements, then, is the most exciting kind of scientific problem: an unsolved one.
Thanks for reading!
Zullo, L., Sumbre, G., Agnisola, C., Flash, T., & Hochner, B. (2009). Nonsomatotopic Organization of the Higher Motor Centers in Octopus Current Biology, 19 (19), 1632-1636 DOI: 10.1016/j.cub.2009.07.067
Gutnick T, Byrne RA, Hochner B, & Kuba M (2011). Octopus vulgaris Uses Visual Information to Determine the Location of Its Arm. Current biology : CB, 21 (6), 460-2 PMID: 21396818
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
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
(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
This will be a quick one – I’ll get back to the meat of my series on octopus sensory systems soon, but I wanted to write a post on this article because it struck me as cool (although it has a sort of sensational title.)
The authors used an apparently elegant experimental design to test whether octopuses can tell people from one another across a long period of time – specifically, this is operationally defined as meaning that they could learn an association between a person’s features and a good or bad stimulus. The experiment was conducted thus: eight octopuses were captured and habituated to their aquaria. Then, for 2 weeks, the octopuses had daily interaction with two people, one of whom fed them and one of whom (I’m not joking) poked them with a “bristly stick” (more specifically, “a length of PVC pipe with one end wrapped in Astroturf.”) Then, the octopuses were tested to see if they reacted differently to the two individuals – presumably, if they remember who is who, they should show anticipatory behaviors related to eating or defensive behaviors in response to the appropriate person.
To get a better feel for the task, here are the experimenters, shown in an image taken from the octopus’s point of view:
My problem with this experiment is that the term “individual” is usually used in cognitive research to mean some entity who is known to persist despite changes in their appearence in one specific sensory modality. When we get a haircut, our friends (and, usually, our pet dogs and cats) still recognize us – thus, we are individuals to them. However, if the visual stimulus of the two keepers didn’t change from day to day (and they took pains to make sure that it didn’t,) then this seems like little more than a complex visual discrimination task. It seems, judging from this image, that it would be pretty easy for an octopus to learn an association between, say, a shiny bald head and being jabbed with a stick, regardless of any ability she might have to recognize “individuals” in the cognitive sense. In any case, we are still a ways away from knowing whether octopuses can recognize individuals, and not just their constant visual features. With this in mind, let’s consider their results.
It turns out that the octopuses learned to move away from the irritator and towards the feeder within two weeks. In addition, the octopuses showed fewer defensive coloration responses to the feeders than to the irritators, as well as changes in their respiration rate and the orientation of their bodies relative to the people. In sum, it looks like (in this test, at least) the octopuses succeeded in learning basic traits about the people interacting with them. I don’t think that the title of the paper is fully supported, however – it’s hard to make the case that this single study proves that octopuses can identify individuals in any sort of robust way.
This paper is pretty solid (besides its unfounded title,) although it begs a few questions:
1. How fine of a discrimination can octopuses make? Would they treat two bald men of similar stature the same? What if the subjects wear different clothes? How is this piece of research fundamentally different from Wells’ experiments using simple visual cues? These are all important questions if we’re actually going to claim that octopuses can identify “individuals” as opposed to simple visual stimuli.
2. What does this mean functionally to the octopus in the wild? Is this sort of ability actually used to identify predators and prey items? Do octopuses remember individuals of any species in the wild? Unfortunately, there is not much literature on the development of behavior in the octopus, so we can’t know how much of octopus behavior is “instinct” and how much of it is based on learning (like that shown in this study.)
3. How does this generalize to other species of octopus? This study used Enteroctopus dofleini, the giant pacific octopus, because it is often kept in public aquaria. However, practically the whole body of research on octopus learning and vision has been done using O. vulgaris and, to a lesser extent, O. cyanea. We know that cephalopods have a pretty wide diversity of life-styles, so it seems important to me to know how these behaviors occur in different species if findings like this are going to be relevent to the rest of cephalopod research.
If nothing else, this study keeps alive my childish hope that Twister, the resident E. dofleini at the Niagara Falls Aquarium (which I visit almost weekly these days) will someday get to know me, if only in the most basic way.
Anyways, I hope this has been as fun for you as it was for me. Thanks for reading!
Anderson, R., Mather, J., Monette, M., & Zimsen, S. (2010). Octopuses (Enteroctopus dofleini) Recognize Individual Humans Journal of Applied Animal Welfare Science, 13 (3), 261-272 DOI: 10.1080/10888705.2010.483892
For several years, a group of researchers in France have been studying the neural correlates of learning in cuttlefish (recently focusing on, among other things, oxytocin-like neuropeptides in the cuttlefish CNS – I’ll review this in a later post.) I reviewed some of their work in an earlier post. Although this is a fascinating concept, their method has been criticized because they use a single learning task to elicit what they claim are learning-induced neural changes, generally. Importantly, it is questionable whether their method causes associative learning or habituation. Associative learning involves the formation of a mental or neural (depending on your conceptual preference) association between some behavior and a consequence of that behavior, such as finding food or feeling pain. This form of learning has long been thought of as one of the hallmarks of adaptive behavior, and it is certainly central to any claims about cephalopod intelligence – if we could not demonstrate associative learning in cuttlefish, we would have very little ground on which to call them intelligent. Habituation occurs when we are exposed to some stimulus for long enough that we just stop responding to it. In the case of habituation, we haven’t learned much about the stimulus – simply that it is generally unrelated to any reward or punishment we might get.
So what is this controversial procedure? The group has given it the obscure name of the prawn-in-the-tube procedure. It is essentially what is sounds like. A cuttlefish is presented with a prawn enclosed in a clear plastic tube. Cuttlefish, being visual predators, will attack the prawn, but their tentacles will hit the tube, and their attack will fail. Over subsequent presentations, they learn not to attack the tube. The difficulty is that it is hard to tell whether the cuttlefish are simply habituating to the prawn-in-the-tube stimulus, or whether some sort of sensory feedback from failed attacks is causing them to suppress their attacks – a type of associative learning known as passive avoidance learning.
In this group’s research on cuttlefish learning (as well as in an older line of research by J. B. Messenger that used the same procedure) it is vital to know what sort of learning they are inducing in order to interpret their results. Specifically, they work under the assumption that their procedure induces passive avoidance learning. This is a pretty big assumption. As such, they decided to settle this problem with a series of experiments, which they published as The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning? (2006) by Agin, Chichery, Dickel, and Chichery.
This study uses two techniques. The first is called dishabituation. In these experiments, a strong competing stimulus is presented alternatively with the “habituated” stimulus. If this elicits a greater response, the it is likely to be the case that the animal has habituated rather than learned by association. If the response is still suppressed after the novel stimulus is presented, it must be that the familiar stimulus is repressing behavior, and that passive avoidance learning has taken place. The logic is that the effects of habituation will decrease if the animal becomes generally aroused by some other stimulus. Their results show, however, that this is not the case. Novel stimuli did not dishabituate the cuttlefish to the prawn-in-the-tube assembly. Strike on against the habituation theory.
The second test that they used involved showing the cuttlefish a piece of bait (a live prawn,) and then removing it from the tank as the cuttlefish attacked, preventing them from ever catching it. In this test, the cuttlefish never received any sort of tactile feedback when they attacked. If the prawn-in-the-tube procedure causes habituation, we would expect attacks to decrease in this condition, as there is no reward or punishment to shape the behavior. If the prawn-in-the-tube procedure works mainly by passive avoidance learning, we would expect that, as there is no negative sensory feedback following unsuccessful strikes, the cuttlefish would not change their response at all during this version of the procedure. As it turns out, the procedure was almost completely ineffective in inducing any sort of learning in this condition. The cuttlefish continued to strike regularly at the prawn, and their latency to strike actually decreased. This experiment clearly does not support the habituation hypothesis. Strike two!
Actually, these results could presumably be overturned by some more sensitive or definitive test in the future. For the moment, however, these studies allow the cuttlefish memory research community to investigate the neural bases of memory in the cuttlefish with a reasonable amount of certainty that they are studying associative learning. They also make a nice general point about the sort of fine-grained analysis that’s needed in order to study complex psychological processes like learning and memory, as well as emphasizing the importance of being critical of the assays that one uses to study these things.
Thanks for reading!
(Sepia apama. Photo by Nick Hobgood, used under a Creative Commons license.)
I’ll get back to octopus behavior in the subsequent posts, but I want to digress into octopus neurobiology for a minute. We know that octopuses can learn, and our buddy J. Z. Young proposed that their memory system is much like ours – as evidence, he showed that the structure of the octopus vertical lobe (a little chunk of brain tissue that sits right at the top of the octopus brain – see P. Z. Myers’ post on the subject for a quick introduction to the brain of octopus) may have a lot in common with the structure of the mammalian hippocampus (which is a place in the human brain that is critical for memory – it’s shown here.) The specific paper that I’ll review here is “A Learning and Memory Area in the Octopus Brain Manifests a Vertebrate-Like Long-Term Potentiation” by Hochner et al. It was published in 2003 (7 years ago already!) in the Journal of Neurophysiology (available at this link.) Much as the title suggests, this study showed the presence of long-term potentiation (or LTP) in the octopus vertical lobe. Let me explain what LTP is, and then the previous paragraph may become a lot more meaningful to some readers. LTP is the mechanism by which synapses (the points of communication between nerve cells) become “stronger”; that is, synapses can transmit information with a varying degree of degradation of the signal, and stronger ones will transmit the information better than weaker ones. First, a picture of a synapse:
The neuron sending the information (the presynaptic neuron) is in yellow, while the neuron receiving the signal (the postsynaptic neuron) is in green. Imagine that the system works like this: an electrical pulse comes flying down the presynaptic axon from the top of the page. When it gets to the end of the axon, it causes (through a variety of rather complicated biochemical mediators) all those synaptic vesicles to dump their contents into the space between the neurons (the synaptic cleft). Their contents are neurotransmitters, which then act on receptors on the postsynaptic neuron. This activity causes electrical currents to be generated in the postsynaptic neuron, and so the electrical signal has bridged the gap and is on its way. When a synapse is persistently active, it will tend to become stronger (this is known as Hebb’s law – it’s actually only sometimes true, but it’s a good heuristic for now.) This is called long-term potentiation, as the synapse can be said to be potentiated, and this effect will last a while. Now, a lot of things happen during LTP – the synapse may become physically larger or more efficient, and the types of receptors on each side may change. In any case, the overall effect is that the synapse will become better at propagating signals – that is, the same signal in the presynaptic neuron will elicit a larger signal in the postsynaptic neuron.
In this study, electrical pulses were sent through the MSF (medial superior frontal) tract – a tract that runs parallel to the brain surface and interacts with vertical lobe neurons. Simultaneously, recordings were made from neurons in the vertical lobe that could receive signals from the MSF tract. What the experimenters were testing was whether they could induce LTP in octopus neurons by stimulating them. This procedure is known to work in vertebrates, and is thought to be responsible for much of vertebrate neural plasticity (that is
, the adjustment of the way neurons are “wired” together, which is thought to allow us to do things like learn and remember.) If it’s present in octopus, then it means that there is something about the organization of this type of system that is efficient or effective enough to have evolved largely independently in two very different groups of animals (although we don’t actually know exactly what the last common evolutionary ancestor was between people and octopus, we have a pretty good idea – but that’s for another post. It suffices to say that it mostly likely had a very simple nervous system, meaning that octopus and vertebrate brains evolved mostly independently.)
If you’ve read my previous post or another piece of writing about the squid giant axon, let me use this example to drive home its significance. The techniques of neural stimulation and recording in this paper, as well as the theories that the authors employ about the structure and function of neurons, all descend directly from work done on the squid giant axon. It really is a big deal.
So, with the basic experimental design and that little editorial out of the way, let’s hit the meat of the paper:
All of this groups work was done in vertical lobe slices; that is, they anesthetized the octopus by submerging it in a weak ethanol solution, removed a slice of its brain, and kept the brain slice alive in a solution of artificial seawater and antibiotics for a day before experimenting on it.
This figure shows the anatomy of the vertical lobe/MSF tract system. To make it clear, if you imagine an octopus sitting on the ground, the octopus’s tentacles and mouth would be to the right of this figure, and its mantle would be to the left.
This figure shows the location of recording and stimulation electrodes. The graphs are tracings of the voltage recorded by the recording electrode. The authors identify two signals – the large one (TP) is from neurons in the MSF tract, and the small one after it (shown in this figure by arrow heads) is from the vertical lobe neurons that the MSF tract makes synapses with. They are delayed in time simply because it takes some time for a signal to travel down a neuron. In this case, the authors measured the size of each signal, measured as the maximum height of the tracing.
This is a summary of the results of this experiment. After repeated stimulation, most of their test preparations showed a large significant increase in the strength of the synapse, meaning that the same presynaptic signal generated a larger postsynaptic signal. This is a sort of weird graph, so let me explain it: the horizontal axis shows the significant of the trial – the ones to the left are significant, whereas that group on the right is not significant (meaning they didn’t actually show any change.) The vertical axis shows how strong the synapse was after LTP-inducing stimulation, proportional to how strong it was before – that is, “2″ means that the synapse is twice as strong after stimulation as it was before, “3″ means it is 3 times as strong, etc.
In this figure, the top graph represents the size of the recorded signals in postsynaptic neurons of the vertical lobe (that is, field-type postsynaptic potentials, or fPSP.) The bottom graph represents recordings from the presynaptic MSF neurons. The arrows show the beginning and the end of LTP-inducing stimulation. This figure is very informative, as it shows us that the synapse is indeed selective strengthened. The presynaptic signal (TP – bottom graph) does not increase, but the postsynaptic potential (fPSP – top graph) becomes at least twice as strong as it was prior to stimulation. To sum it up, the presynaptic signal stays the same, but because the synapses have become better at transmitting the signal, the postsynaptic signal is larger.
This is good evidence that LTP takes place in the memory system of the octopus brai
n, and could account for the memory of octopuses, as we suspect it accounts for much of the memory ability of humans. The rest of the paper is spent elucidating possible mechanisms which could account for the observed LTP, as well as verifying that it is actually LTP and not just an artifact of their procedure – I don’t have the time to go through this at the moment, mostly because it involves a wide array of neurophysiological techniques, which are a workout to explain in and of themselves. (For the curious neurophysiologically-minded readers, I’ll summarize: they find that there are both postsynaptic and presynaptic mechanisms that contribute to LTP in octopuses, as in vertebrates. It is also demonstrated that LTP in the octopus involves a large increase in intracellular calcium concentration, as in vertebrates. Unlike in most vertebrate systems, however, LTP in octopuses is not NMDA-type receptor dependent, although the authors don’t offer an alternative explanation. This is neat, because it suggests that the same sorts of neural systems are likely to evolve with some wiggle room as to the specific mechanisms of their functioning.)
Why does this study matter? It implies that this specific type of organization and functioning of a memory system is somehow “special” – that is, it works so much better than an alternative arrangement that it was selected for in (at least) two independent cases. In terms of studying octopus biology, it also means that the great wealth of information on vertebrate neural systems is likely to be applicable (at least in a modified form) to the study of cephalopod nervous systems. In terms of studying vertebrate biology, it is possible that studying how this system work in octopus could give us new insights into the function of vertebrate memory systems. Lastly, the methods used in this paper are just incredibly cool. C’mon, people – keeping octopus brains alive in a bath! Imagine how awesome it would be to explain your job to somebody at a dinner party if you were the experimenter.
If you read this and find yourself with any questions, or noticing any errors, please let me know. I know this was a bit technical, but I think it’s misleading to present science as if it were possible to really grasp it without being at least a bit technical. I think to really understand the importance of research like this, you have to understand the procedures used, at least basically. In any case, I hope this post was informative and interesting.
Today I’ll review the earliest Octopus behavioral research study I could find (that is, except for a few very old papers in French, that I shamefully do not have the skill to read, although I am working on translating a few of them, bit by bit.) This is a study by Paul Schiller published in the Journal of Comparative Psychology in 1949, titled “Delayed Detour Response in the Octopus”. It’s a very early experiment on the ability of octopus to apply detours to a learned task (that is, you teach the animal to go somewhere for a reward, usually food, and then you put a barrier in its way. Depending on the character of the animal’s “intelligence”, it may or may not be able to successfully pass the barrier to get the reward.) If you have access to scholarly databases, you can probably get ahold of it (I got mine for Scirius, and I think Ovid has it as well) – unfortunately, I can’t link to a free .pdf of the article here.
Interestingly, Schiller begins his description of his methods by describing a procedure that does not work with octopus:
The conventional technique of using two inverted cans, one covering a baited, the other an unbaited container, both of them previously exposed to the vision of the octopus, was tried on 4 animals with rather discouraging results. Both cans were attacked and lifted indiscriminately or, if not far enough from each other, simultaneously. This happened often even in the preliminary stage when the covering cups were transparent. The tendency to crawl in or lift up the containers was so powerful that the animal did not regard the bait at all unless specifically trained to do so.
This makes a lot of sense – it turns out, as shown in this and later experiments on octopus, that their top performance in response-selection tasks is somewhere around 70-80% correct responses. They are “curious” enough that they will choose to investigate the “wrong” stimulus regularly. This makes sense for a foraging, active predator, who is more successful if they inspect many new areas of their environment than if they are entirely predictable.
Shown in this figure is the apparatus he settled on. The octopus is confined in the starting compartment and allowed to investigate a crab in a beaker through a screen. Then, the entrance door is opened, and the octopus learned to move through the opaque corridor to receive the crab. It was found that, after learning this, Schiller’s octopuses made 75% correct responses – well above chance (which is 50%, in this set-up.) Furthermore, Schiller found that the longer it takes the octopus to get through the corridor, the worst its chance of being correct. He also finds that, using a female whose reward is returning to her nest instead of a crab, that disorientation of her body posture by making her crawl through a small hole destroyed her ability to make the correct choice in the delayed detour task:
It seems, with this one animal now under the more powerful motivation of her nest instead of food, that a delay of at least one minute does not interfere with the correct choice. The same amount of delay, however, if it involves disorganization of the bodily posture while in locomotion, prevents a successful delayed choice. There is no need to assume central representative factors for the delayed detour performance which, in the octopus, may be mediated by locomotional cues.
Basically, although we can explain detour performance in (for example) rats by showing that they probably have some flexible internal representation of the test space (see Tolman’s discussion of cognitive maps for more information,) it appears that this same ability in octopus can be explained by intervening postural and sensory cues, without recourse to more complicated cognitive processes.