Cephalove

To get things started, here’s a video of an octopus with a Mr. Potato Head Toy (and other things):

You’ll see why this is relevant in a minute. Now on to the post!

“Enrichment” is a psychological term that’s been thrown around a lot. It’s become a buzzword in publications about education, perhaps rightly so given its huge impact on the field of developmental psychology. It has been the subject of intense study in psychology, and continues to be the subject of study. But what exactly is it that we are referring to when we use the term “enrichment”?

Before I get to that, let’s take a step back and consider how brains work. Brains, in the sense that I am talking about, are simply big networks of neurons (there are other types of cells, but we can ignore them for now.) These neurons get sensory input from the body, talk amongst themselves, and send out signals that cause the organism to behave in a certain way. This is, in a nutshell, what brains do – they generate behavior. Importantly, though, they don’t just generate any behavior at a given time; they generate the appropriate behavioral response to the immediate situation. Even more impressively, in some animals, they generate the response that will lead to a positive outcome in some hypothetical future situation (for example, when birds hide food to recover later.) Thus, brains work because they can process incoming sensory information into relevant and adaptive behaviors. Neurons can do this because they are connected to each other in complex but well-controlled and highly-specific ways. Much in the way that an electrical device will only operate if all of its components are connected correctly, brains will only work if all of their neurons (or at least most of them) are “wired” together into functional circuits.

It may come as no surprise, then, that brains only wired the way they are because of the sensory input they receive. During brain development (and, to a lesser extent, throughout life,) neurons require sensory input and behavioral output to form proper connections as well as get rid of improper connections. At the cellular level, this phenomenon is called activity-dependent or experience-dependent plasticity. One can think of it this way: connections between neurons (called synapses) that are used a lot and produce functional behaviors get stronger; that is, they become more efficient and transmit larger signals from neuron to neuron. Synapses that are not used, or that don’t contribute or contribute negatively to the function of a certain circuit become weaker; that is, they become smaller and less efficient, and may even disappear altogether.

This can be demonstrated directly by looking at neurons that process incoming visual information from the eyes. Suppose we were to raise one group of animals (lets say, ferrets) completely in the dark, and another, otherwise identical group of animals normally. Then, we kill both groups of animals and look at the neurons in their visual system (for example, in visual cortex.) The group that was raised under normal light will have, by definition, normal connections between the neurons in the visual system – specifically, these neurons will form functional circuits that allow animals to sense and respond to their environment. In the animals that were reared in the dark (called, sensibly, “dark-reared” animals,) we’ll see a host of abnormalities – cells will have the wrong shapes, end up in the wrong places, and have the wrong connections. Besides this, we could demonstrate some deficiencies in visual perception in the dark-reared animals. Taken together, these results, which have been replicated in a variety of vertebrates, strongly support the idea that sensory systems need input during development in order to develop properly.

It’s a small logical step to tentatively extend the principal of experience-dependent plasticity to brain functions that are more complex than immediate sensory analysis. In the mammalian cortex (which is involved in such complex behaviors as navigation, auditory and visual perception, social behavior, speech, thought, and so forth,) normal development is dependent on the experience of the animal in question during development. The input that these brain areas deal with is almost unthinkably complex. Their function often involves the monitoring the interaction of large parts of the organism with the environment over an extended period of time. For example, cortical areas involved in directing complex hand movements (say, playing a musical instrument) receive their input in the context of a feedback loop that involves planning a movement, executing it, and then determining whether the movement was successful and, if it was not, how it needs to be changed in order to be successful the next time. More abstract cognitive processes become even more complicated, as the brain areas responsible for these have to take into account such complex “stimuli” as the animals current and previous emotional states, inferred emotional states in other animals, the value of various hypothetical outcomes to the organism, prior cognitive states the animal has had, and so forth.

Here’s where the idea of environmental enrichment comes into the picture. The logic goes like this: because neural development is facilitated by the nervous system’s interaction with the environment, and because the more integrative areas of the brain (like the cortex) interact with the environment in very complex ways, normal brain development requires interaction with a very complex environment. If this theory is true, animals raised in very restricted environments (we might call them “environmentally impoverished”) should show maladaptive or sub-normal behavior as adults. In fact, this prediction has been borne out in many studies, which find that (among other things) environmentally impoverished animals (and, although it has been less directly demonstrated, people) have altered learning abilities, exploratory behavior, cognition, stress reactivity, and social behavior.

A corollary of this theory is the idea that nervous systems which have evolved to deal with the environment in very complex ways function abnormally when they do not have complex environments to deal with, much like the way that muscles atrophy if they are not used. Part of successfully engaging a complex environment is continually interacting with and exploring it – indeed, many animals have evolved a propensity to explore and manipulate their environment. Thus, animals with complex behavioral repertoires require complex environments to interact with in order to maintain normal brain function. This theory predicts that a lack of complexity in some animals’ (or people’s) environments should lead to aberrant behavior, and that such behavior can be corrected by providing an appropriately complex environment to those animals (or people.) This prediction is borne out in a variety of studies that show that, in captive adult animals, providing more complex environments leads to lower stress levels, less aggression, and fewer pathological and stereotyped behaviors.

Dr. James Wood’s article, “Environmental Enrichment in the Giant Pacific Octopus; Happy as a clam?” makes the case that aquariums should provide environmental enrichment for captive octopuses. I won’t follow his arguments exactly, but I will examine some of the same questions that he covers, and make reference to and critiques of his work as I find it relevant.

The big question is this: Should we provide environmental enrichment to captive cephalopods? Let me rephrase this: do the benefits of providing environmental enrichment to cephalopods justify the costs incurred by doing so?

First, let’s consider the possible benefits. Anderson and Wood point out several:

1. Captive animals should be kept healthy and allowed to behave normally. Behavioral health is as important to the longevity and quality of animal’s lives as is physiologic health. The real question here is whether cephalopods have complex enough behavior that they might show pathological behavior in response to captive conditions. Put in a more cognitive frame: are cephalopods smart enough to be hurt by captivity and, consequently, to benefit from enrichment?

Indeed, it is hard to tell whether cephalopods could benefit from enrichment. To the question of how we can tell if giant pacific octopuses could benefit from enrichment, Anderson and Wood succinctly conclude: “Simply put, we cannot.” Because cephalopods have evolved under predation from fishes, they reason, they spend most of the time during which they are not hunting hiding in their dens. It’s hard to tell if this is “good” for the octopus (after all, it seems like it would be nice not to have the daily stress of fleeing from predators and risking death during hunting) or bad (because, if cephalopods can become bored, this behavior certainly seems like it would be really boring.) In addition, little is know about how behavioral pathology might look in cephalopods, because we know so little about their behavior in general.

In sum, cephalopods may or may not benefit from enrichment. Given how complex their behavior appears to be, and the likelihood that at least some cephalopods possess cognitive capacities to rival at least some vertebrates, it seems like there’s a reasonably good chance that they could. This isn’t a convincing case in itself – it really depends on the costs of providing enrichment to cephalopods. If the costs are low, this might be enough of a reason to do it; with increasing costs, it becomes an increasingly bad bet.

2. Animal enclosures should meet the expectations of the public. Showing the public what they want to see – which is, it seems, natural-looking enclosures that animals can interact with) will lead to financial success and public support for zoos and aquariums. Researchers, institutions, and the enterprise of biological science in general stand to benefit from the increased public support that comes with presenting a public-pleasing image of animal husbandry in research. Also, if the public sees naturally-behaving animals instead of pathologically-behaving animals, they learn more about the animal’s behavior. A primary function of zoos and aquariums is to educate the public about animals, and so the potential to improve on this education is an important possible result of providing enrichment to cephalopods.

This is an interesting idea to me. Octopuses are popular aquarium animals, but not very popular research animals. The public face of animal research is usually mammalian, including rats, mice, rabbits, and primates. It’s doubtful to me that researchers would benefit from an improved public image if all octopuses used in research were given lots of enrichment. In zoos and aquariums, though, this seems like a valid concern. Indeed, it could offset the monetary costs of providing enrichment for these institutions, which allows less tangible benefits (like the possibility of relieving the suffering of bored octopodes) to be given more weight in deciding whether or not to provide enrichment for captive cephalopods.

3. Finally, zoos and aquariums often care for animals with the goal of eventually releasing them into the wild. Animals whose behavior is dependent on learning need to practice skills that will allow them to succeed, such as hunting, defending from predators and rivals, and maintaining good relationships with other individuals of their species. The Seattle aquarium, for example, does this with their giant pacific octopuses. They catch individuals, hold and display them for a few years, and then release them into the wild so that they have a chance to breed.

It’s doubtful to me that enrichment benefits cephalopods in this way. I can’t say that it’s impossible, but it seems unlikely. While cephalopods are able learners, the basics of cephalopod behavior – feeding, escape, and mating – appear to be largely innate. For example, octopuses learn things in order to adapt to the specific micro-environments they end up in. The characteristics of these environments are impossible for aquariums to predict, and so they cannot be simulated. Feeding a cephalopod common local prey species so that it learns how to eat those species efficiently might help it succeed if it is released, but besides this one example there seems to be relatively little to do in the way of “preparing” a cephalopod for release.

Before I hash out some of the costs of providing enrichment to captive cephalopods, let’s consider what providing such enrichment entail. Anderson and Wood suggest several ideas for giant pacific octopuses, most of which could work with other species of cephalopods. The one that sticks out to me is feeding the animals a variety of live prey. This would provide them with a good deal of activity, a variety of problems to solve (how to catch and eat different species of prey,) and is very entertaining for the public to watch. Some cephalopods (cuttlefish come to mind – I’ve read cuttlefish keepers complaints about this) will only reliably eat live food, anyways.

The authors also suggest that the octopuses be given objects to explore, which can be smeared with fish drippings or have food hidden in them to attract the octopus and encourage exploration. In my favorite quote of the paper, they recount a particular use of this technique:

Wood and Wood… hid food in a play ship – the octopus had to “sink” the ship to get the proffered food. Such a demonstration with a large octopus… would interest the paying customers of a public aquarium by invoking a “sea monster” image.”

The future of cephalopod husbandry.

They also suggest the use of “training” to provide enrichment to octopuses (I put “training” in scare quotes, because some of their specific suggestions, such as smearing fish-smelling fluid on parts of the tank, don’t necessarily involve learning.) This seems like a moot point to me. There are two ways in which you can train a cephalopod – by rewarding it with food, or by punishing it with electric shocks (or some other unpleasant stimulus.) In the first case, you might as well simply give the animal the food, the capture of which seems like it would provide most of the activity inherent in training. In the latter case, well, who’s going to argue that training an animal by electric shock improves its quality of life or reduces its suffering (assuming that the training isn’t absolutely necessary, such as teaching it not to attack people or run into traffic, etc.)?

What would be the costs of providing this sort of enrichment to cephalopods? In my estimation, they would be small. Here’s my reasoning:

It should be relatively easy for aquariums, especially those near coasts, to obtain live prey to feed to cephalopods. By advertising the feeding times (as is done with the animals like sharks, dolphins, and sea lions) aquariums could turn this into a way to entertain visitors and draw more business. The increased popularity of octopus exhibits would likely make up for the extra cost of providing more live food. One of the complaints I hear about the giant pacific octopus exhibit at the Niagara Falls Aquarium is that it just sits there all the time. In the interest of furthering public interest in cephalopods, I make sure to write “Please publicize octopus feeding times!” in their guestbook each time I visit. I’m sure that if they did this, their visitors would be more interested in the octopus and happier with the aquarium overall.

Similar reasoning applies to constructing interesting enclosures that encourage cephalopods to explore. The public likes to see animals doing things, and the increased public interest will more than make up for the expenses of outfitting an octopus tank (which can be as cheap as a few plastic toys) These forms of enrichment are probably very cost effective, at least for public aquariums, even if they have only a small chance of benefit the captive animals.

When we consider animals used for research, the costs become larger. Giving animals a less monotonous environment may exaggerate inter-individual variation. It is usually argued that enrichment produces consistently healthy experimental animals, and so reduces variation in experimental results. The research that is used to make this argument in the case of mammals, however, has not been replicated in cephalopods. Without such evidence, it’s hard to say what effect different kinds of enrichment would have on behavioral experiments with octopuses. Such evidence would be rather expensive and time-consuming to obtain, and providing enriched environments to experimental cephalopods on the assumption that it would improve results could be, if that assumption were wrong, very costly as well. If behavioral research on cephalopods becomes more popular, this will become a more urgent question, and somebody will have to take on the task and expense of answering it.

Generally, providing enrichment for captive cephalopods seems worth it. Given the (even relatively slight) chance that they could benefit from basic environmental enrichment and the small cost of such enrichment, there’s no reason not to do it. The deal only becomes sweeter when you take into account the benefits to aquarium popularity and public education. Even if the cephalopods don’t benefit from it, it can hardly hurt.

Thanks for reading!

Anderson, R., & Wood, J. (2001). Enrichment for Giant Pacific Octopuses: Happy as a Clam? Journal of Applied Animal Welfare Science, 4 (2), 157-168 DOI: 10.1207/S15327604JAWS0402_10

van Praag H, Kempermann G, & Gage FH (2000). Neural consequences of environmental enrichment. Nature reviews. Neuroscience, 1 (3), 191-8 PMID: 11257907

          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