Squid Visual Ecology

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 decapodiformes (Cephalopoda) Journal of Mulluscan Studies, 76, 180-185 : 10.1093/mollus/eyp055

What the cuttlefish sees that you don't

I thought I'd mix things up a little bit and take a look at some research on the sensory abilities of cuttlefish.  Specifically, I'd like to take a look at an aspect of cuttlefish vision that has shown up in the literature recently (it's actually one of the few threads of cuttlefish research that seems to be active at the moment - the other ones I've noticed are memory and fishery ecology and management): the ability of cuttlefish to perceive polarized light.  Polarized light is composed of photons that are all oscillating in the same plane - we cannot sense the polarization of light, but it seems to play some role in the lives of cephalopods and some other animals.  For more info on polarized light, check out this explanation of polarization.

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.

This is an image of cuttlefish (S. officinalis) photoreceptors (From Shashar et al 1996.)  The lines are folds in the photoreceptor cells called microvilli.  Notice how the two adjacent cells have microvilli at a right angle to each other - this is what allows cephalopods to see the difference between polarized and non-polarized light.

Detecting polarization can help a creature in a lot of ways.  In a basic sense, it almost always helps an animal (especially one who, like the cuttlefish, is both a predator and a prey item) to have as much information about the environment.  If sensing polarization allows the cuttlefish to know more about its environment at any given time, it's already a huge advantage.  In fact, it has been shown that the perception of polarized light probably helps cuttlefish to catch certain prey that is difficult to see otherwise (see Shashar et al 2000.)  But I mentioned the possibility of communication through polarized light - how does that work?

It turns out that iridophores, organs in the skin of cephalopods that reflect light, polarize that light to some extent.  The anatomy of iridophores is such that they preferentially reflect light polarized in a certain plane.  It is known that cephalopods, especially cuttlefish, have wonderful neural control over the pigment organs in their skin, which allows them to display such a dazzling array of colors and patterns.  Cuttlefish might be able to manipulate the polarizing properties of their iridophores, adding another layer of complexity to their body patterns.  Importantly, however, this would be a type of display that not everybody in the sea could perceive.  Shashar's theory is that cuttlefish might use polarized light as a type of social signal, while still being able to maintain the camoflauge which is key to avoiding being eaten.

Shashar and friends did a few experiments to test this hypothesis: first, they observed cuttlefish during a variety of behaviors, and found that the polarization of light being reflected from the cuttlefish's arms varied with different behaviors in much the same way as their patterns of coloration.  Polarized light is reflected from stripes on the arms and the area around the eye, as seen in this image from a review on the use of polarized light by cuttlefish by Mathger et al (2009):

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 there'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

Octopus Sensory Systems: Part 2.5

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