Cephalove

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

Cephalopods have a lot to offer – tentacles, beaks, and big scary (and perhaps cute) eyeballs. Today, though, let’s look at a part of the cephalopod body that doesn’t get paid so much attention to, especially by us neurobiologist types: the ink.

Fossil squid with preserved ink sac. Ink sacs are often easily visable in coleoid cephalopod fossils. (via Maitri on Flickr - click through for original.)

Most coleoid cephalopods (that is, all the living cephalopods excluding nautiluses and a few deep-water octopuses) produce ink. This ink is composed chiefly of melanin, which is a dark brown pigment that is found throughout the animal kingdom. Humans have used cephalopod ink for a variety of purposes, including writing, drawing, dying, and cooking (the fact that both a dark brown color of ink and a genus of cuttlefish are both named Sepia is not coincidence.) In fact, you can buy tubs of cephalopod ink online.

Cephalopods use their ink for a different purpose, though; it helps them get away from sticky situations. When severely startled, cephalopods will release ink from their ink sac, which is pushed out of their funnel with a jet of water (which usually also jets the cephalopod in the opposite direction away from the perceved danger.) The resulting cloud of ink could serve many functions; it could conceal the escaping cephalopod’s location from the predator, serve as a false target for the predator (who would attack the dark ink instead of pursuing its prey,) frighten the predator, or even trick the predator’s sensory systems into thinking it had already caught something (I’ll explain this last one at the end of the post.)

One neat property of cephalopod ink, though, has nothing to do with how predators perceive it, but rather how cephalopods perceive it.

When one squid in a shoal inks (“inking” being the action of expelling ink into the water) the rest of the shoal can certainly see what has happened and be alerted to the immanent danger that way. In addition to this, though, it has been hypothesized that squid can chemically sense the ink in the water, which would give them another way to keep abreast of squid-predator interactions going on around them.

One study that found evidence for this hypothesis (which is actually a part of a series of studies in this line of research) was done by Gilly and Lucero (1991) at Hopkins Marine Station in California. These investigators restrained squid (loligo opalescens) by attaching their dorsal mantle to a platform with cyanoacrylate glue (the same stuff that Super Glue is made of,) and then used a pipette to place small amounts of various substances onto a chemoreceptive organ located behind the squid’s eye.

Photograph and photomicrograph of squid olfactory organ - from Gilly and Lucero (1992)

They recorded the activity of the squid with a video camera, and everything was done remotely, so that the movement of the experimenter’s would not upset the squid and cause extra escape-like behavior. Escape-like behavior was measured in terms of the pressure inside the squid’s mantle, which was recorded via a tiny pressure transducer inserted inside the squid’s mantle. One of their records is shown here – the spikes in pressure reflect jets of water being expelled from the squid’s mantle, as it presumably attempts to escape from the chemical stimuli that signal some sort of danger in the environment.

They found that pipetting ink from an animal of the same species of the test animal onto the olfactory organ caused jetting. Furthermore, they found that a specific component of squid ink, L-DOPA (which is a precursor of melanin, the main pigment in squid ink) caused jetting just as much as did whole ink. On this basis, the authors concluded that L-DOPA is used as a sort of chemical alarm signal between L. opalescens individuals. (I should note that some of the authors cited in this post write that squid ink is actually a cue, not a signal, as a signal results in an action on the part of the receiver that benefits both the receiver and the sender of the signal. Escape responses by squid in response to the ink of conspecifics do not fit this definition.)

A more recent study by Wood, Pennoyer, and Derby (2008) looked at the responses of Caribbean reef squid (Sepioteuthis sepioidea) to squid ink preparations. This species of squid has ink that hangs together in a mucous-ey glob in the water, forming what the authors call a “psuedomorph”, or false animal shape that confuses predators.

Each squid was tested by placing a small amount of an ink preparation into its aquarium and videotaping its behavior during and after this event. The authors used a scoring system to determine how defensively each squid behaved during each test, with points on a scale of defensiveness being awarded for behaviors like jetting, specific postures that are used to hide from predators, and certain color changes that are known to signal alarm. A higher score on this measure of defensiveness indicated that the squid was “alarmed” (or something like that) during the test. Below is a video showing on of their tests, produced by New Scientist:

The authors found that S. sepioidea responsed with alarm to fresh squid ink placed in their aquarium. The ink worked to cause alarm responses even after it had been frozen, albeit not as well – the authors noted that it changed in consistency, and dispersed much more quickly. Ink that was placed into an adjacent aquarium (meaning the squid could see it, but could definitely not chemically sense it) worked very well to stimulate escape behavior. This argues that one of the stimuli that this species of squid uses to respond to ink is its appearance. What about chemoreception, though?

The authors produced “melanin-free ink” by centrifuging fresh ink to remove all of the melanin-containing granules in it. They reasoned that this ink was just link the whole ink chemically, except that it did not contain the specific chemical that made it opaque (melanin). They found that the squids did not respond to this ink that they could not see. These results point to the use of vision exclusively in S. sepioidea in responding to other squid’s ink, apparently conclusively.

Frustratingly, they don’t, really. It would be easy enough to chalk this result up to species differences – one species can chemically sense ink, and the other species cannot. These results, however, don’t say enough to make this claim (although there may exist other research that answers this question.)

In a paper by Lucero, Farrington, and Gilly (1994), squid (L. opalescens) ink was analyzed for the presence of L-DOPA and dopamine (they found it, but that’s not the reason I mention it.) They found that, in seawater, L-DOPA and dopamine are rapidly degraded via oxidation reactions, which would certainly dampen any effects they would have on the behavior of squid swimming in that water. They also found that the L-DOPA and dopamine in squid ink did not degrade this rapidly – these preparations behaved as if they were being protected by some sort of antioxidant contained within squid ink. While the authors used ascorbic acid (a small, soluble molecule) to replicate this effect, it’s possible that any anti-oxidant activity in the squid ink is provided by a protein (or another large, centrifuge-seperable molecule.) When Wood et al. prepared their “melanin-free ink”, they may also have removed some component of the ink that is essential for its activity as a chemical signal (for a hypothetical example, a protein that prevents that oxidation of L-DOPA and dopamine in the vicinity of the ink blob.) They may even have done something that eliminated the L-DOPA and dopamine altogether – they provide not chemical analysis of their ink preparations, and so it’s hard to know. The authors acknowledge that this is a shortcoming of their work in their paper, so there’s been no oversight on their part – it just would have been nice if they’d done a bit more in the way of quantifying the chemistry of the preparations they were using. Oh well – it’s something for the next round of studies, I guess.

I mentioned that squid ink might trick predators into “thinking” they had already caught the squid and were eating it, a trick called phagomimicry. This is because squid ink (and the exudates that other molluscs exude under stress) contains, among other things, a full complement of free amino acids – these are chemicals that predators taste when they eat flesh. If a predator gets a mouthful of ink, if they can sense the amino acids that normally tell them that they’re eating flesh, they may behave as if they have already caught and/or eaten their prey, and give up pursuit.

Thanks for reading!

W. F. Gilly and Mary T. Lucero (1992). Behavioral Responses to Chemical Stimulation of the Olfactory Organ of the Squid, Loligo opalescens Journal of Experimental Biology

WOOD, J., PENNOYER, K., & DERBY, C. (2008). Ink is a conspecific alarm cue in the Caribbean reef squid, Sepioteuthis sepioidea Journal of Experimental Marine Biology and Ecology, 367 (1), 11-16 DOI: 10.1016/j.jembe.2008.08.004

Lucero, M., Farrington, H., & Gilly, W. (1994). Quantification of l-Dopa and Dopamine in Squid Ink: Implications for Chemoreception Biological Bulletin, 187 (1) DOI: 10.2307/1542165

Cephalopods are great subjects for studies on vision, because they are so dependent on their vision that you can get robust behavioral effects by manipulating the visual environment of a test animal. In some new research in the October edition of the Journal of Experimental Biology, CM Talbot and J Marshall (from Queensland) investigate the visual system of the pyjama squid (S. lineolata) and two species of cuttlefish (S. plangon and S. mestrus) – specifically, to find out whether they can respond to polarized light, and in the case of S. lineolata, how photoreceptors are distributed on its retina. I’ve blogged about a study on visual perception in Nautilus before, as well as a study on the retinal topography of squid, so if you would like to see more of the same sort of research, check out those posts.

In these two papers, the authors assessed the ability of their experimental specimens to respond to polarized light by monitoring their optokinetic and optomotor responses to a rotating drum. The optokinetic response is the movement of an animals eyeballs to follow a moving object in the visual environment, while the optomotor response is the movement of the animal’s body to follow movement in the visual environment. The experimenters monitored the optokinetic response in S. lineolata, because it tends to stay motionless on the substrate, partially buried – as such, it will not exhibit an optomotor response under most circumstances. On the other hand, S. plangon and S. mestus both tend to hover in the water, and so show optomotor responses more readily.

A basic scheme of the apparatus used is shown in this figure from the S. lineolata paper:

The animal is in the tank (in this case, prevented from burying itself by being enclosing in a transparent cylinder,) while a drum is rotated around the tank. By varying the pattern on the drum, it is possible to determine the sensory abilities of the animal – assuming that animals generally don’t inhibit optokinetic or optomotor responses, the animal will respond to any pattern it can perceive. If the animal can’t perceive the pattern on the drum (for example, if the drum is visually continuous, as is the case with an all white drum,) it will not perceive any motion and the response will be absent.

The authors used a drum that consisted of alternating stripes of orthogonally oriented polarization filters – that is, the drums were striped, but the difference between adjacent stripes was only in the direction of polarized light that they transmitted. All the stripes transmitted the same total amount of light, and had the same appearance. Thus, the animals would only show an optomotor or optokinetic response to these drums if they could perceive the direction of polarization of the light.

In fact, this is what happened, in all three species. Two control drums were used, one of alternating black and white stripes (to make sure the animals had otherwise normal optokinetic and optomotor responses) and one of a uniform-direction polarization filter (to make sure that the animals weren’t responding to some other part of the drum – the tape used to hold it together, seams resulting from the drum’s construction, etc.,) making it pretty clear that the animals were responding to the alternating directions of polarization and not anything else.

This result is pretty unambiguous, but I’d like to point out a problem that this type of experiment presents in its interpretation: specifically, it’s very difficult to interpret negative results. In this case, it’s very easy to know what it means in terms of the animal’s sensory ability when it responds to a stimulus: it means the animal can detect that stimulus. But what if the cuttlefish didn’t respond (for example, as was found in a very similar study by Darmaillacq and Shashar (2008) in a different species of cuttlefish, Sepia elongata)? It’s hard to know what that means – did the animal fail to perceive the stimulus, or did the stimulus just not mean enough to generate a behavioral response? This is a general problem that crops up in studies on sensation and perception in animals, or any study that relies on an animal perceiving something and emitting a behavioral response. Many things need to happen to get any behavioral response to a stimulus, even one as apparently simple as eye movements. The animal must have a functional sensory apparatus appropriate to perceive the stimulus, it must have the energy and intact musculature to perform whatever behavior it is you’re looking for, it must be expressing no other behaviors that might mask or supress the behavior of interest, it must be motivated to perform the behavior of interest, etc. A negative result in such an experiment means that one of these many things is not the case, but because it’s so difficult to tell the difference between all of these steps between “stimulus” and “behavior”, it’s hard to say what exactly it is that the animal isn’t doing. Is it failing to sense the stimulus, is it failing to respond because the stimulus isn’t relevant, or is it failing to behave because it’s afraid, or stressed, or tired? Darmaillacq and Shashar note that S. elongata has retinal anatomy that looks like it would allow the animal to sense polarized light, and so they are (wisely) wary of claiming that their subjects could not perceive polarized light – but there’s no way to make any claim about S. elongata‘s vision at all from these results (except, of course, the most conservative assertion that S. elongata failed to show an optomotor response to a certain type of polarized-light stimulus under the experimental conditions used in that specific study.)

Fortunately, though, Talbot and Marshall found positive results, and so avoided that quagmire all together. It turns out that all three species they studied can respond to polarized-light stimuli with optokinetic or optomotor responses. They went on to examine the distribution of photoreceptor cells (also called “retinal topography”) in the S. lineolata retina. If you’ll remember from my post on squid visual ecology, it turns out that you can relate the retinal topography of cephalopods to their lifestyle – squids that live near coasts have retinas that are specialized to allow the animal to see below it clearly, whereas oceanic squids have retinas that are specialized for monitoring the water column above them. What might we expect from S. lineolata, an animal who spends much of its time buried in sand? The sensible answer is that is eyes would be specified to look up, since that’s where its predators and prey would be in most cases. Let’s take a look at what Talbot and Marshall found:

The darker the blue is, the higher photoreceptor density is in that area. It turns out that the striped pyjama squid does indeed have a high photoreceptor density in the ventral part of its retina, which probably gives it good visual acuity in the upper part of its visual field (if you don’t know why this is, check out this explanation of image formation in the eye for a primer.) This fits in neatly with what we know about the lifestyle of this squid.

I hope these studies represent the start of a trend towards the study of less “classical” cephalopod species (the “classical” ones being Loligo pealai, Octopus vulgaris, Sepia officinalis.) There’s a lot to learn from the less common species of cephalopods, due in part to the fact they we know very little about most of them.

Thanks for reading!

Talbot CM, & Marshall J (2010). Polarization sensitivity and retinal topography of the striped pyjama squid (Sepioloidea lineolata – Quoy/Gaimard 1832). The Journal of experimental biology, 213 (Pt 19), 3371-7 PMID: 20833931

Talbot CM, & Marshall J (2010). Polarization sensitivity in two species of cuttlefish – Sepia plangon (Gray 1849) and Sepia mestus (Gray 1849) – demonstrated with polarized optomotor stimuli. The Journal of experimental biology, 213 (Pt 19), 3364-70 PMID: 20833930

Here at Cephalove, I tend to focus on octopuses.  The reason for this is pretty simple – out of all of the cephalopods, the most behavioral research has been done on octopuses, so they are the easiest cephalopod to write about.  To keep things lively, though, and to do something special to commemorate my first new post as part of the SFS Network, I want to dedicate this post to the oft-forgotten member of the cephalopod family: the nautilus.  Specifically, I want to talk about the eye of the nautilus. First, to cover the basics: nautiluses are the only extant cephalopods who still have an external shell.  There are only six species of nautilus still around, 4 in the genus Nautilus and 2 in the genus Allonautilus, with the most well-know being N. pompilus, the chambered nautilus (although this name accurately describes the shell of this species, all species of nautilus have chambered shells that help them achieve neutral bouyancy.)  A nautilus has about 80-100 small tentacles protruding from its shell, with which it catches food – mostly small crustaceans and fish.  They are found in the Pacific ocean, where they live in the deeper parts of coral reefs.  Here’s a picture (in the public domain – thanks, J. Baecker!) showing a chambered nautilus: You can’t see it too well here, but the eye protrudes on a stalk (the optic stalk, to be precise) from the head.  If you are used to looking at octopuses, cuttlefish, and squid (and aren’t we all, by now?) you’ll notice that the nautilus eye looks very different from theirs.  In fact, it is lensless, with the pupil being open to the water (sort of – there may actually be a sort of covering over it, but I’ll get to that later.)  This sort of eye is called a pinhole eye, and is also seen on giant clams.  It works very much like a pinhole camera, where an image is formed (albeit a relatively crude one) by restricted the angles at which light can enter the eye.  As those familiar with photography know, smaller pinholes create a sharper image; however, they are less sensitive, and require a much greater intensity of light to form a good image.  The nautilus’s eye works similarly, and so its pupil size is ultimately the result by a compromise between resolution and sensitivity.  A cross-sectional diagram of the eye (from Muntz and Raj, 1984) is shown below.  The dashed line shows the area where the eye connects to the rest of the body, and the thick line shows the location of the retina.  The gap at the right of the image is the pupil.

How good is the nautilus’s eyesight?  To find out, we’ll take a look at Muntz and Raj (1984), a paper that examines the spatial resolution of the nautilus eye through two different methods.  First, the authors used the nautilus’s natural tendency to maintain its orientation and direction in the water to determine its approximate visual acuity.  Then, they constructed model nautilus eyes and took pictures through them.  These are both elegant (although incomplete) ways to get an idea of what the nautilus sees, which is a very basic question in the problem of understanding the behavior of a particular organism.  I’ll skip over any more discussion of the anatomy of nautilus in this post – that’s another story for another day.  Muntz and Raj succinctly address the anatomy of the eye in the paper, so look there if you’d like more information on the subject.

To test the functional acuity of the nautilus’s vision, the authors exploited the animals optomoter response.  This is a reflexive motor behavior that keeps the animal in a stable orientation relative to landmarks in its environment.  This is very useful for a neutrally buoyant creature living in the water, who might otherwise easily be flipped over or turned around by water movement.  The authors did this by putting a nautilus into a tank in the middle of a drum.  The inside of the drum was striped, and the drum was slowly rotated around the tank.  If the nautilus could perceive the stripes, it would presumably rotate with the drum, trying to maintain its orientation to its surroundings.  If it could not perceive the stripes, it would let the drum rotate around it without attempting to correct for this movement.  A diagram of the apparatus, taken from the paper, is shown below.

By varying the width of the stripes, the authors were able to determine just how well resolved nautilus vision is.  After some calculation, the authors concluded that the nautilus has a minimum visual resolution between (roughly) 5 and 11 degrees of the visual field.  In comparison, a human has a minimum visual resolution resolution of about 1 minute of arc (1/60 of a degree.)  This means that as long as two objects are more than 1/60 of a degree apart in the image formed on a human’s retina, she will be able to tell that there are two objects there.  The nautilus, on the other hand, requires that the objects be at the very least 5 degrees apart in order to resolve them separately.  Thus, if stripes smaller than the equivalent of 5 degrees of visual field were used, the nautilus could not perceive them, and so showed no orienting response to this stimulus.

There’s a problem with this interpretation, though.  It might be that the 5-11 degree limit is not a limit of the eye, but rather just a differential behavioral response to different types of stimuli.  What if nautiluses tend to orient themselves to large objects (like the seafloor, or the light of the surface) but not to smaller objects (like animals swimming around them, or floating debris?)  This certainly seems adaptive. To help make the argument that the 5-11 degree limit was a limit of the eye itself, the authors constructed a model eye and took pictures through it.  In this way, they got a sense of the resolution of the image formed on the retina, which sets (albeit not directly) a lower limit on the resolution of the image that the brain can form.  Seen below is a set of such images.  The top left image shows the chart that they used.  The remaining three were taken through model eyes with increasing pupil diameters, corresponding to the range of pupil diameters found in wild nautiluses.  Under the experimental conditions, the top line is distinguishable at a minimum resolution of 4 degrees, and the bottom is distinguishable at a resolution of 2 degrees.  As you can see, some of the model nautilus eyes could not resolve either line, suggesting that the minimum resolution found in the behavioral test (5-11 degrees) agrees with the optics of the eye. Now that we know a bit about the optics of the Nautilus eye, what about that open pupil?  (I told you I’d get back to this.)  Having a gaping hole in one’s eye seems like it presents a problem to the animal, as it leaves the delicate interior of the eye open to the water – and any tiny particle or organism that might be floating around.  A simple experiment by W. R. A. Muntz (1987) discovered for one mechanism that protects the interior of the nautilus’s eye.  First of all, notice the groove that runs from the pupil to the bottom of the eyeball:

Photo by Hans Hillewaert

That groove is lined with cilia that sweep mucous downwards across the surface of the eye.  Muntz place drops of india ink on the surface of detached nautilus eyes, and found that the the india ink traveled downwards across the eye and into the groove.  Drops of ink were even seen moving over the opening of the pupil, indicating that this sheet of mucus is viscous enough to form a semi-solid covering over the pupil.  Without a lens to cover this opening, the nautilus seems to have evolved another way to keep particles out. Well, I hope you enjoyed this as much as I did.  Thanks for reading! W. R. A. Muntz (1987). A Possible Function of the Iris Groove of Nautilus Nautilus: the Biology and Paleobiology of a Living Fossil, 245-247 DOI: 10.1007/978-90-481-3299-7_16

W.R.A. Muntz, & U. Raj (1984). On the visual system of Nautilus Pompilus Journal of Experimental Biology, 109, 253-263

Keeping with the theme of sensory systems, I thought I’d review some newer research on squids.

While searching for recent cephalopod neurobehavioral research (which is pretty scant) to blog about, I came upon Makino and Miyazaki’s study on the distribution of retinal cells in the retina of squids.  I have a soft spot for visual neuroscience that I picked up from working with my first research advisor, who works on the visual system of frogs.  In any case, this is a good paper (although it was a bit hard to get my hand on,) and I’ll review it here.

The study aims to look at the distribution of retinal cells in the retinas of a variety of squid species.  This has been done in several vertebrates, with the general finding that animals have retinas that perform well for their lifestyle.  Seems pretty simple, right?  For example, fish who live in “closed” environments have dense retinal ganglion cells (RGCs) in the area of the retina that sees light from directly ahead, while oceanic fish have a strip of high-density RGCs that stretch laterally across the whole visual field.  Thus (to make a horribly crude generalization,) cave and reef dwelling fish have focused binocular vision, while oceanic fish largely lack this but have a greater ability to monitor their whole visual field, ie. for predators or food items.

In vertebrates, retinal ganglion cells are often mapped in this sort of study.  By the time RGCs exit the retina, they are carrying visual information that is already processed into the very basic components of visual perception (namely, hue and tone contrast.)  As vertebrates have complex retinas, it is also possible to map photoreceptors in vertebrate retina, or a variety of other types of cells (which might be more or less informative.)  Cephalopods, however, only have one type of visual cell in their retina – the retinal cell (or rhabdomere.)  So, the authors chose to map this.  It is useful to keep in mind that this is not directly comparable to the mapping of retinal ganglion cells in vertebrates – it could be the case that the density of visual cells in an animal’s retina is not always correlated with the importance of that piece of the visual field in further levels of visual processing.  This problem is partially solved in studies on vertebrates by the use of RGCs, in which the processing of information from photoreceptors is already underway.  With cephalopods, however, there is currently no way to probe this any deeper, and so for now it remains an assumption – albeit a pretty noncontroversial one – that rhabdomere density is correlated well with the relative importance (behaviorally and neurophysiologically) of portions of the visual field.  (For more on cephalopod visual anatomy, check out my earlier post on cephalopod eyes.)

The image to the left shows cell counts (in retinal cells per mm) across the retinas of the 5 species of squid.  I added color to this image to make it easier to see the distribution of cells.  It’s important to not that the colors are relative within each figure, and do not represent absolute cell density, which is shown as (difficult to read) numbers on the boundaries of regions.  Also note the scale bars, which are 10mm in every image. 

In terms of orientation, keeping things straight gets a little tricky (as it does with all cephalopods.)  Dorsal-ventral orientation is pretty easy – remember that the lens of the eye inverts the light coming through it, so that the ventral part of the retina forms the top part of the visual field and the dorsal part of the retina forms the bottom part of the visual field.  Anterior is the direction the squids’ arms point in, so the anterior retina forms the posterior part of the visual field.  The posterior retina is the part that forms the anterior part of the visual field.  This is the part that is used when squids look forward to form a binocular image.

Using this data, the authors estimated the visual axes of the squids, based on the location of the highest density of photoreceptors.  The visual axis is the general point of focus, which is known to be of utmost behavioral importance in vertebrates.  When you follow a moving object with your eyes, you are keeping it in your visual axis.  The location of an animal’s visual axis is key to its visual ecology – many predators have forward facing visual axes so that they can see their prey accurately, while prey species often have very laterally oriented visual axes (think of rabbits and deer) so that they can monitor more of their environment at any given time.  Thus, we’d expect that squids with different lifestyles have different visual axes, because they will be looking for food and predators in different places.

In coastal squid (E. morsei and S. lessoniana), the visual axis is directed downwards, presumably reflecting the importance of monitoring activity on the substrate that these species live on.  In oceanic squid (T. pacificus, E. luminosa, and T. rhombus,) the visual axis is directed upwards, and the eyes have a much greater density of photoreceptors overall.  I think the retinal cell density map of E. luminosa is especially interesting, because the concentration of cells on the extreme posterior edge of the retina suggests that binocular vision is disproportionately important to this species.  The authors conjecture that this eye may be specialized to detect and track bioluminescence in the open ocean, but this is purely speculation.

These findings are important because they expand our knowledge of cephalopod eyes, which are a model evolutionary system.  If we can begin understand the impact of ecology on the organization of visual systems (which is part of the emerging field of visual ecology,) we can generate a wealth of testable hypotheses about the ecological conditions that occurred during the evolution of differnt species eyes, as well as the other sorts of adaptations we might see in sensory systems as they diverge (or converge) during evolution.  It’s also a nice piece of evidence that our rather basic theories about visual ecology and the structure-function relationship of the visual system are largely correct.  This is good to know, as we base an incredible amount of more complicated neuroscience research on these theories.

Thanks for reading!

Akihiko Makino, & Taeko Miyazaki (2010). Topographical distribution of visual cell nuclei in the retina in relation to the habitat of five species of dec
apodiformes (Cephalopoda) Journal of Mulluscan Studies, 76, 180-185 : 10.1093/mollus/eyp055

It has been known that cephalopods can respond to polarized light for some time – Wells did the work showing that octopuses can detect polarized light in the 1960′s, and it’s been studied in fits and spurts since then.  In the late 1990′s and early 2000′s (from what I can tell,) it became a relatively hot topic among researchers who study animal communication, because it appeared as if cuttlefish might be able to use polarized light for some sort of intraspecific communication.  A good though somewhat dated review of the topic is Shashar et al’s Polarization Vision in Cuttlefish – a Concealed Communication Channel? (1996).

How can cephalopods see polarized light?  It turns out that their photoreceptors are orientated at a variety of angles, so that incoming light will cause the most stimulation in photoreceptors that are oriented the “right” way.  In unpolarized light, all of the cells would be pretty much equally stimulated – nothing unusual happens here.  Upon being hit by polarized light, though, a specific population of retinal cells (those that are oriented in the proper direction) will be activated, and the animal will be able to see the polarization of light.

The top image is a cuttlefish as seen by the human eye. The bottom image has been given false color, so that areas which reflect polarized light show up as green.  On an unrelated note, cuttlefish sure are cute.

In addition to discovering the patterns of reflection of polarized light by cuttlefish skin, the authors found that cuttlefish respond differently to their own reflections when they view them through a filter that screens out polarized light.  Specifically, they found that cuttlefish responded less noticibly to the disrupted image.  While the authors declare that these findings are “fully consistent with the hypothesis that cuttlefish use controllable polarization patterns for intraspecific communication,” they are also consistent with the more parsimonious explanation that cuttlefish don’t respond to any stimulus made of non-polarized light as strongly as they do when it is at least partially polarized.  While the theoretical argument presented in this paper is interesting, I think it’s a bit too eager for what the data show.

Fast-forward to 2004: Boal et al. published a study called Behavioral evidence for intraspecific signalling with achromatic and polarized light by cuttlefish. In this study, they exposed cuttlefish (S. officinalis) to conspecifics (that is, other cuttlefish) through either a clear or a polarized light-blocking barrier.  They found that only females responded differentially to conspecifics behind the polarization-distorting barrier, not responding to them at all (cuttlefish confronting each other unexpectedly often show some sort of postural and color change.)  This was the only significant result that they found, and it is ambiguous in its interpretation.  Again, it might simply be that a non-polarized stimulus is not very interesting to an animal who is used to seeing a world of polarized light.

So, do cuttlefish use polarized light to communicate?  I’m not convinced.  It seems as if everybody’s hoping that it’s true, but th
ere’s not any good data showing it to be so.  I can’t sum it up any better than Mathger et al. did in their 2009 review:

The fact that cephalopods can detect polarized light
and can also produce changeable polarized light
patterns in their skin begs the question whether
cephalopods communicate using polarized light signals.
The likely answer is that they do. Unfortunately, we
have little evidence to support this statement.

Thanks for reading!

Shashar N, Rutledge P, & Cronin T (1996). Polarization vision in cuttlefish in a concealed communication channel? The Journal of experimental biology, 199 (Pt 9), 2077-84 PMID: 9319987

Mathger, L., Shashar, N., & Hanlon, R. (2009). Do cephalopods communicate using polarized light reflections from their skin? Journal of Experimental Biology, 212 (14), 2133-2140 DOI: 10.1242/jeb.020800

Boal, J., Shashar, N., Grable, M., Vaughan, K., Loew, E., & Hanlon, R. (2004). Behavioral evidence for intraspecific signaling with achromatic and polarized light by cuttlefish (Mollusca: Cephalopoda) Behaviour, 141 (7), 837-861 DOI: 10.1163/1568539042265662

Shashar N, Hagan R, Boal JG, & Hanlon RT (2000). Cuttlefish use polarization sensitivity in predation on silvery fish. Vision research, 40 (1), 71-5 PMID: 10768043

This will be a quick one – I’ll get back to the meat of my series on octopus sensory systems soon, but I wanted to write a post on this article because it struck me as cool (although it has a sort of sensational title.)

The article I’m talking about is Octopuses (Enteroctopus dofleini) Recognize Individual Humans (2010) by Anderson et al. in the Journal of Applied Animal Welfare Science.

The authors used an apparently elegant experimental design to test whether octopuses can tell people from one another across a long period of time  – specifically, this is operationally defined as meaning that they could learn an association between a person’s features and a good or bad stimulus.  The experiment was conducted thus:  eight octopuses were captured and habituated to their aquaria.  Then, for 2 weeks, the octopuses had daily interaction with two people, one of whom fed them and one of whom (I’m not joking) poked them with a “bristly stick” (more specifically, “a length of PVC pipe with one end wrapped in Astroturf.”)  Then, the octopuses were tested to see if they reacted differently to the two individuals – presumably, if they remember who is who, they should show anticipatory behaviors related to eating or defensive behaviors in response to the appropriate person.

To get a better feel for the task, here are the experimenters, shown in an image taken from the octopus’s point of view:

My problem with this experiment is that the term “individual” is usually used in cognitive research to mean some entity who is known to persist despite changes in their appearence in one specific sensory modality.  When we get a haircut, our friends (and, usually, our pet dogs and cats) still recognize us – thus, we are individuals to them.  However, if the visual stimulus of the two keepers didn’t change from day to day (and they took pains to make sure that it didn’t,) then this seems like little more than a complex visual discrimination task.  It seems, judging from this image, that it would be pretty easy for an octopus to learn an association between, say, a shiny bald head and being jabbed with a stick, regardless of any ability she might have to recognize “individuals” in the cognitive sense.  In any case, we are still a ways away from knowing whether octopuses can recognize individuals, and not just their constant visual features.  With this in mind, let’s consider their results.

It turns out that the octopuses learned to move away from the irritator and towards the feeder within two weeks.  In addition, the octopuses showed fewer defensive coloration responses to the feeders than to the irritators, as well as changes in their respiration rate and the orientation of their bodies relative to the people.  In sum, it looks like (in this test, at least) the octopuses succeeded in learning basic traits about the people interacting with them.  I don’t think that the title of the paper is fully supported, however – it’s hard to make the case that this single study proves that octopuses can identify individuals in any sort of robust way.

This paper is pretty solid (besides its unfounded title,) although it begs a few questions:

1.  How fine of a discrimination can octopuses make?  Would they treat two bald men of similar stature the same?  What if the subjects wear different clothes?  How is this piece of research fundamentally different from Wells’ experiments using simple visual cues? These are all important questions if we’re actually going to claim that octopuses can identify “individuals” as opposed to simple visual stimuli.

2.  What does this mean functionally to the octopus in the wild?  Is this sort of ability actually used to identify predators and prey items?  Do octopuses remember individuals of any species in the wild?  Unfortunately, there is not much literature on the development of behavior in the octopus, so we can’t know how much of octopus behavior is “instinct” and how much of it is based on learning (like that shown in this study.)

3.  How does this generalize to other species of octopus?  This study used Enteroctopus dofleini, the giant pacific octopus, because it is often kept in public aquaria.  However, practically the whole body of research on octopus learning and vision has been done using O. vulgaris and, to a lesser extent, O. cyanea.  We know that cephalopods have a pretty wide diversity of life-styles, so it seems important to me to know how these behaviors occur in different species if findings like this are going to be relevent to the rest of cephalopod research.

If nothing else, this study keeps alive my childish hope that Twister, the resident E. dofleini at the Niagara Falls Aquarium (which I visit almost weekly these days) will someday get to know me, if only in the most basic way.

Anyways, I hope this has been as fun for you as it was for me.  Thanks for reading!

Anderson, R., Mather, J., Monette, M., & Zimsen, S. (2010). Octopuses (Enteroctopus dofleini) Recognize Individual Humans Journal of Applied Animal Welfare Science, 13 (3), 261-272 DOI: 10.1080/10888705.2010.483892