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

Octopus Sensory Systems: Part 2

In this post, I'll be talking about octopus tactile sensation.  M. J. Wells and J. Z. Young did the classic experimental work on touch discrimination and learning in the octopus, although a bit of recent work has been done on the neurochemical basis of touch learning in the octopus (which I won't get into here.)

We'll focus on Tactile Discrimination of Surface Curvature and Shape by the Octopus (1964) by Wells.  This was one of his later papers in a series on tactile learning in the octopus.  Prior to this paper, Wells had already determined that octopus do not use proprioception to discriminate between objects (as a blindfolded person might do when trying to feel what an object is with his hand,) but rather use (almost exclusively) tactile cues about the object's shape.  Let me explain.

It had been found that a blinded octopus could discriminate, on the basis of touch, between a sphere and a cube.  This could be explained by the presence of some sort of proprioception that monitors the relative position of the octopus's arms in space - a system like this is known to exist in most vertebrates.  However, Wells carried out a series of experiments that show that this is, if anything, a very subtle factor contributing to the octopus's ability to perform tactile discriminations.  He found that octopuses learn to recognize the corners of a cube as variations in texture, which are encoded in reference to the extent that the suckers contacting the object are deformed.  For example, a sucker that is on the corner of a cube will wrap around the corner, bending itself along a sharp angle.  This information is encoded as some sort of distinct textural component, and sent along to the brain where it can interact with learning centers (which I'll discuss in a later post, hopefully) that will allow the octopus to remember what a particular texture means.  Thus, if you teach an octopus to respond to a cube (meaning that you reward it with food when it grabs the cube, and punish it with electric shock when it grabs another object, say, a sphere,) this theory would predict that it would also respond to any object which induces a similar deformation of the suckers that contact it, such as a rectangular prism, or a thin rod.  This is called a transfer experiment, because it tests the extent to which a learned task transfers to situations other than the one it was learned in.  Indeed, Wells found that he could substitute a thin rod for the cube, and the octopus will respond to it as if it is a cube, presumably because the suckers contacting the rod are bent into a relatively sharp angle, as are those contacting the edges of the cube.

This evidence alone didn't quite clear up the question of how octopus performed touch discriminations, though - specifically, Wells' experiment with the cube, sphere, and rod did not use enough variations of form and dimension to really probe the mechanism of touch discrimination.  Thus, Wells decided to conduct a number of transfer experiments between differently sized and textured cylinders in order to figure out the characteristics that octopuses use to identify objects by touch.  The stimuli he used are shown here:

The numbers under the cylinder cross-sections indicate their diameter in millimeters.  Wells notes that the octopus he is working with have suckers that are 10mm or less in diameter.  Knowing this, one can gauge the approximate deformation of a sucker that the different cylinders would produce.  For example, a 6mm wide cylider would induce a significant curvature in the sucker, whereas the 38mm cylinder would produce a very slight curvature, and thus would appear essentially "flat" to the octopus, if Wells' theory is correct.

Wells quantified this difference, and generally found that the greater the difference in curvature between two cylinders, the easier the discriminate was.  This is great, but it doesn't rule out the proprioception theory.  What if the octopus was actually "feeling" the position of the arm as it bent around the cylinder? 

To solve this problem, Wells used the two cylinders shown at the bottom of Figure 1, those labeled 8* and 6*.  These are "composite cylinders" were made of 7 small cylinders attached together, parallel to each other.  If the sucker-distortion hypothesis is correct, then these objects should be treated as equivalent to small cylinders, because they create equivalent deformation of the suckers contacting them.  If there is some mechanism that determines the shape or position of the grasping arm as a whole, then they should be treated as equivalent to the large cylinders, as they would require the same arm position and curvature to grasp as the 24mm and 18mm "simple" cylinders, respectively.  In fact, this is what Wells found, although the experiments with compound cylinders did not adhere quite as closely to his proposed model regarding differences in curvature as did those with the simple cylinders.  This might be expected, as the actual curvature experienced by the suckers is more variable with a more complex object.

Wells tested his idea further, by offering already trained octopuses P1 (which was grooved) and P4 (which was smooth.)  Other than their texture, these objects did not differ at all.  If sucker deformation is the basis of discrimination, we would predict that P1 feels most like a small-diameter rod to an octopus, as it would deform the suckers touching it greatly.  P4, on the other hand, would feel like a large-diameter cylinder, because, well, it is.  In fact, this is what Wells found - octopuses who were trained to take the larger diameter cylinder transfered this learning to the P1/P4 discrimination, and tended to take the smooth one.  Animals who were trained to take the smaller diameter cylinder tended to take the grooved one.

Wells goes on to consider discrimination using a cube with rounded corners (which proves difficult for an octopus) and a cube/rectangular prism discrimination (which is also difficult,) but I'll let him tell you about those, as the point is amply made already.

What about the neuroanatomy of this system?  Wells provides us with a figure showing the cross-sectional structure of a single sucker, including the receptors that putatively monitor mechanical distortion of the sucker (in the area labeled "2" at the rim of the sucker, towards the bottom of the diagram.

 

These receptors detect the mechanical forces from the object deforming the rim of the sucker, and then send this information to the ganglia of the arm.  It seems likely (although I don't know that it has been tested) that these mechanoreceptors don't send their information the whole way to the central nervous system, but rather input into some processing system in the nervous system of the arms first.  It would be interesting to know the minimum number of steps that information from the suckers might go through before it gets to the brain, because this would give a rough idea of how "processed" the sensation is before it gets to brain areas involved in learning.  J. Z. Young's "Anatomy of the nervous system of Octopus vulgaris" didn't seem to have a clear answer for this question, so for the time being, I'll assume that it's unanswered (though, if I'm wrong, please point me to the literature.)

All in all, this might seem like a poor way to distinguish two things from each other.  When you keep in mind the fact that octopus can't discriminate objects based on weight, either, even though it can adjust its posture and muscle tone to hold a heavy object, it would seem that the octopus has a sort of crappy tactile sensory system.  We should ask, then: what does the octopus use this for?

When octopuses hunt, they often use a "blind" foraging strategy.  They will pounce on an area where prey is likely to be with their arms and web spread open and then feel for prey.  Alternatively, in rocky areas, an octopus might feel around in cracks for prey items.  If the octopus feels a prey item, she grabs it, moves it towards her mouth, and eats it.  It seems likely to me that the sort of touch discrimination that Wells trained octopuses with is not anything like what is demanded of them under ecological conditions.  For one, it is likely that octopuses are sensitive to movement as well, as they must be able to discriminate between rocks and prey, both of which might be similarly textured.  While hunting, an octopus also has other sensory systems to rely on.  They're not primarily visual predators, but they can be, spotting prey and then attacking it (as they do when shown a live crab in an aquarium.)  They also probably have chemoreceptors on their arms which could help them identify objects under their web.  It doesn't seem to me as if lacking proprioceptive input to the central nervous system is at all a deficit to the octopus in its natural habitat.

Thanks for reading!


M. J. Wells (1964). Tactile Discrimination of Surface Curvature and Shape by the Octopus Journal of Experimental Biology, 41, 433-445

Octopus Sensory Systems: Part 1

I've been reading M. J. Wells' book "Octopus", one of the "classic" works on the octopus.  It was published in 1978, and is an essentially complete review of research on octopuses (primarily O. vulgaris, the common octopus) up until that time.  It must have been fun to write the book, because he had done much of the research he cites (he cites at least 45 of his own papers in the book.)

Wells has published a large number of experimental studies on octopuses, and I've become very interested in his series of experiments dealing with the sensory capabilities of the octopus.  In this series of posts (there will be 3 or 4, I anticipate, over the next week or two) I'll relate his findings, as well as others, about the sensory systems of the octopus.  Forgive me if I write brief posts, as I'm rather busy writing other things at the moment.

I'll jump right into the octopus visual system.  It's a good place to start, I think, because it's relatively easy for us to imagine what it's like to see, and so to think about octopus visual perception by analogy.  It's relatively harder to imagine what it's like to control eight boneless arms (just like it's hard to think about what lateral line perception is like in fish - we simply do not have the anatomy to do it.)  We'll move on to other senses in the next few posts.  For now, though: vision!  (For a brief look at the anatomy of the octopus visual system, check out my earlier post on that topic.)

Vision in octopus has been studies mostly through the technique of visual discrimination tasks.  Simply put, an octopus is taught (via food rewards for correct answers and/or electric shocks for incorrect answers) to attack one visual stimulus and not another.  The visual stimuli are then varied, and it can be discovered what stimuli the octopus can discriminate between.  If two shapes are not discriminated between, they can be said to be perceptually identical (or at least perceptually similar) to the octopus.  These experiments were widely done (well, as widely done as anything in octopus neurobehavioral research) throughout the 1950's, 60's and 70's, with some research still going (albeit at a slower pace and with shifting foci) today. 

Octopuses, it turns out, can see pretty well.  They can reliable learn to discriminate a variety of shapes, and can even tell the difference between rectangles that are identical except that one is rotated through a small angle relative to the other.  An interesting deficit showed up after a variety of experiments were carried out, however - Octopuses are unable to recognize the difference between certain mirror images!  For example, an octopus does very poorly when discriminating between two diagonally oriented rectangles, even though they are perpendicular to each other.  This result is not too surprising, as this is the case to a greater or lesser extent with many vertebrates (to whom the octopus is often compared in its sensory abilities.)  It is, however, remarkable in its extent - it seems like a big deal not to be able to make such a discrimination at all.

In any case, these experiments gave theorists of visual perception a lot of things to think about (I'll write about their theories later in the series.)  What I find interesting about the whole series of experiments, however, is that they laid the groundwork for the investigation of the role of statocysts in octopus visual perception.  Statocysts in cephalopods are like the vestibular systems in our ears: they are tiny, fluid filled chambers that contain hair cells which detect the movement of this fluid (see The Fine Structure of the Octopus Statocyst (1965) by V. C. Barber for a more complete description.)  It appears that the main function of the statocysts is to help the octopus maintain its equilibrium by detecting changes in velocity as well as the direction of gravity.  For example, an octopus whose statocysts have been surgically removed will move unsteadily and fail to make normal eye movements in response to the movement of its environment.

Under normal conditions, an octopus will keep its pupil slit horizontal, relative to the pull of gravity.  However, when the statocysts are removed, the octopus will no longer be able to do this; her pupils will be fixed relative to her body position, and will not adjust to remain horizontal.  This is a figure from Proprioception and Visual Discrimination of Orientation in the Octopus (1960) by Wells, showing this effect:

 So what happens when you test these octopuses on orientation discrimination tasks?  It turns out that they can no longer discriminate between differently-oriented bars.  This is a big deal, because it can tell us something about the way that the visual system of the octopus processes shapes.  Specifically, it reveals that there is something important about the orientation of the retina that makes it possible for the octopus to discriminate shapes.  When the octopus cannot keep its retina level, it cannot discriminate between long shapes and tall shapes.  Thus, we know that the circuitry processing visual information in the octopus is relying on the input from the eye always being in the same orientation.

This can be contrasted with the way that people (and probably other vertebrates, although I don't know this for sure) determine orientation in their visual field, which is determined partly by non-visual cues but also largely by the presence of some sort of horizon line in the visual field (see A Horizontal Bias in Human Visual Processing of Orientation and its Correspondence to the Structural Components of Natural Scenes (2004) by Hanson and Essock for a neat demonstration of this.)  If there is no available horizon line, orientation is gathered from other parts of the context, such as common or known objects.  This means that in humans, even when the orientation of retina is perturbed, the visual processing system can use what it knows about the visual environment to adapt to the new orientation.  As long as the input is otherwise normal, it doesn't matter which way the retina is turned - that is, one can still make orientation discriminations when one's eyes aren't on the level.

This might seem puzzling or maladaptive on the part of the octopus, but a little thinking about the visual ecology of humans and octopuses reveals that it's perfectly sensible.  Octopuses, living in the ocean, don't often have very clear horizon lines or reliably-oriented objects around them.  Their strongest clue about orientation is the pull of gravity.  People, living on land, have reliable horizon lines almost all the time, so they can take advantage of this to orient themselves.  In addition, octopus eyes have muscles that can rotate the eyeball around any which way relative to the body - human eyes do not.  Octopuses never needed to evolve the complex orientation-correcting systems that vertebrates did, because they can just hold their eyes level.  They can, in a sense, afford this apparent deficiency in their visual processing system, because they compensate for it easily.  If this was the case with people, every time we laid down, bent over, or leaned to one side, the world would be full of novel objects that we couldn't make sense of!

I hope this was informative.  I can't wait to write the next one, about octopus touch and proprioception.  See you next time!