Having finished the last post with a short discussion of hunting/foraging behavior in the octopus, I figured I should do a lighter post with some fun video examples of cephalopod predatory behavior.
This is a short video of an octopus hunting (I don't know the species) by For the Sea Productions. The octopus catches a fish, apparently by spreading its web and feeling around. There's some great color-changing behavior here, too. It's hard to know how typical this behavior is, though, as it's obviously influenced by the presence of the person filming.
This is a clip from Deep Sea 3D (I think - I haven't seen the IMAX film, but that's what the caption says) showing a visually-provoked attack on a crab. I believe that the octopus here is a Pacific giant octopus.
Let's not leave out the other cephalopods! In contrast to octopuses, cuttlefish are primarily visual predators, who shoot out two long tentacles (these are tentacles proper - they are distinct from arms, which octopuses also have) to grab their prey.
This video was made by the California Academy of Sciences, and shows some adorable cuttlefish attacking crabs. I'm not sure what species they are. Again, you can see dramatic color changes as the animals become aroused.
This one, also by the CAS, shows a great slow-motion shot of the cuttlefish tentacular strike.
I'll end with one of my favorite videos of cephalopod predation:
Notice how the octopus turns mostly white and spreads its arms when the cuttlefish (most likely Sepia apama, although I'm not sure) approaches. This is called the deimatic display, and it's a defensive behavior seen in adult octopuses.
I feel obligated to warn anyone reading this that when you search "octopus eating" or similar strings on youtube, you are much more likely to find videos of people eating octopuses than octopuses eating anything. : (
A blog documenting my intellectual love affair with our many-armed friends.
Wednesday, June 30, 2010
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
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:
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
Thursday, June 24, 2010
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!
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!
Monday, June 21, 2010
Notes on the Argonaut
(Photo by Bernd Hofman.)
One of my favorite parts about reading the research on any topic is reading very old research on that topic. Today, I came across this paper on the argonaut, Notes on the Argonaut (1869), by W. H. Dall, published in The American Naturalist, volume 3. The argonauts are a neat genus of pelagic octopods (Argonauta,) the females of which secrete a thin shell from specialized areas on their arms (pictured above in ecological conditions, inside the shell, and drawn below without the shell.)
(Lithograph by Arthur Bartholomew, ~1870)
Almost 150 years ago, this guy put together a pretty good description of argonaut behavior, although it was brief. Reading his work renews my faith in the power of good old observation, as well as flowery phrasing in otherwise dry writing. For example, Dall comments on the argonaut's sexual dimorphism, with a healthy dose of Victorian sexism:
The Argonant shell is formed, curiously enough, by the females only;
as among more highly organized beings sometimes, the gentler sex
outshine their brothers in the splendor of their apparel, and the
extent it occupies. Unlike many, however, the Argonaut toils not,
neither does she spin.
The last sentence of that quote is genuinely confusing to me. What exactly does he mean? What evidence is there that argonauts do not "toil"? What does it even mean for an octopod to toil? Without being accustomed to the zoological vernacular that Dall is writing in, it's hard to get what he means by this.
Another gem is his description of argonaut mating habits. Unlike today's biological authors (fortunately or unfortunately, it's your call,) Dall doesn't shy away from anthropomorphism:
When the tender passion seizes him, as he rocks on some sunny wavelet,
far from female society, he does not go in search of a wife, but with
Spartan courage, detaches one of his eight hands (or arms) and consigns
it to the deep, in the hope that some tender hearted individual of the other
sex will fall in with it and take it under her protection. Thus for a long time
the male Argonaut was unknown, the arm (which does not die when
detached, but lives an independent worm-like life) was, when found in
the gill-chamber of the female, supposed to be a parasite, and was called
Hecto-cotylus.
Interestingly enough, although this name was given to the organ because it was thought to be a parasite, the modified arm that octopus and squid use to mate is still called a heteroctylus.
In closing, Dall acknowledges the unique contributions of one Madame Jeannette Power (a pioneer of the use of aquaria) to the study of the argonaut with a quaint tone of amazement:
It is pleasant to add that our first detailed account of the Argonaut and its
development, was published by a lady, Madame Power, who made her
observations in the Mediterranean, having a sort of marine enclosure
made, where she kept these animals and observed their habits from life.
I know this was a short one. I couldn't help it - I can't resist dusting off a few of the old chestnuts in the scientific literature and reveling in my own fantasies of some lost scientific world, where it's considered adequately professional to use the term "tender passions" when describing the behavior of a mollusc in a leading biology journal.
Thanks for reading!
Thursday, June 17, 2010
Prawn-in-the-tube (More Cuttlefish Memory)
For several years, a group of researchers in France have been studying the neural correlates of learning in cuttlefish (recently focusing on, among other things, oxytocin-like neuropeptides in the cuttlefish CNS - I'll review this in a later post.) I reviewed some of their work in an earlier post. Although this is a fascinating concept, their method has been criticized because they use a single learning task to elicit what they claim are learning-induced neural changes, generally. Importantly, it is questionable whether their method causes associative learning or habituation. Associative learning involves the formation of a mental or neural (depending on your conceptual preference) association between some behavior and a consequence of that behavior, such as finding food or feeling pain. This form of learning has long been thought of as one of the hallmarks of adaptive behavior, and it is certainly central to any claims about cephalopod intelligence - if we could not demonstrate associative learning in cuttlefish, we would have very little ground on which to call them intelligent. Habituation occurs when we are exposed to some stimulus for long enough that we just stop responding to it. In the case of habituation, we haven't learned much about the stimulus - simply that it is generally unrelated to any reward or punishment we might get.
So what is this controversial procedure? The group has given it the obscure name of the prawn-in-the-tube procedure. It is essentially what is sounds like. A cuttlefish is presented with a prawn enclosed in a clear plastic tube. Cuttlefish, being visual predators, will attack the prawn, but their tentacles will hit the tube, and their attack will fail. Over subsequent presentations, they learn not to attack the tube. The difficulty is that it is hard to tell whether the cuttlefish are simply habituating to the prawn-in-the-tube stimulus, or whether some sort of sensory feedback from failed attacks is causing them to suppress their attacks - a type of associative learning known as passive avoidance learning.
In this group's research on cuttlefish learning (as well as in an older line of research by J. B. Messenger that used the same procedure) it is vital to know what sort of learning they are inducing in order to interpret their results. Specifically, they work under the assumption that their procedure induces passive avoidance learning. This is a pretty big assumption. As such, they decided to settle this problem with a series of experiments, which they published as The “prawn-in-the-tube” procedure in the cuttlefish: Habituation or passive avoidance learning? (2006) by Agin, Chichery, Dickel, and Chichery.
This study uses two techniques. The first is called dishabituation. In these experiments, a strong competing stimulus is presented alternatively with the "habituated" stimulus. If this elicits a greater response, the it is likely to be the case that the animal has habituated rather than learned by association. If the response is still suppressed after the novel stimulus is presented, it must be that the familiar stimulus is repressing behavior, and that passive avoidance learning has taken place. The logic is that the effects of habituation will decrease if the animal becomes generally aroused by some other stimulus. Their results show, however, that this is not the case. Novel stimuli did not dishabituate the cuttlefish to the prawn-in-the-tube assembly. Strike on against the habituation theory.
The second test that they used involved showing the cuttlefish a piece of bait (a live prawn,) and then removing it from the tank as the cuttlefish attacked, preventing them from ever catching it. In this test, the cuttlefish never received any sort of tactile feedback when they attacked. If the prawn-in-the-tube procedure causes habituation, we would expect attacks to decrease in this condition, as there is no reward or punishment to shape the behavior. If the prawn-in-the-tube procedure works mainly by passive avoidance learning, we would expect that, as there is no negative sensory feedback following unsuccessful strikes, the cuttlefish would not change their response at all during this version of the procedure. As it turns out, the procedure was almost completely ineffective in inducing any sort of learning in this condition. The cuttlefish continued to strike regularly at the prawn, and their latency to strike actually decreased. This experiment clearly does not support the habituation hypothesis. Strike two!
Where's the third strike? Oh, yeah, Purdy et al found similar results using a variation of this procedure in their paper Prawn-in-a-Tube Procedure: Habituation or Associative Learning in Cuttlefish? (2006). Strike three, and the habituation hypothesis is out!
Actually, these results could presumably be overturned by some more sensitive or definitive test in the future. For the moment, however, these studies allow the cuttlefish memory research community to investigate the neural bases of memory in the cuttlefish with a reasonable amount of certainty that they are studying associative learning. They also make a nice general point about the sort of fine-grained analysis that's needed in order to study complex psychological processes like learning and memory, as well as emphasizing the importance of being critical of the assays that one uses to study these things.
Thanks for reading!
(Sepia apama. Photo by Nick Hobgood, used under a Creative Commons license.)
Tuesday, June 15, 2010
Octopus ethology: the case of Abdopus aculeatus
Ethology is a discipline that I have been enamored of ever since I first discovered it.
The field started with the studies of animal behavior by Konrad Lorenz, who was interested in "instinctive" behaviors in a variety of species, most of them birds (for a good review of history, see http://apophenia.wdfiles.com/local--files/start/tinbergen.pdf). The goal of ethology is stated in a deceptively simple way: to study the behavior of animals. It seems to me to straddle the junction of zoology and psychology, studying behavior from the perspective of animal biology, much as biological psychology studies human behavior in reference to human biology.
It turns out that ethologists do, in essence, the legwork that allows comparative psychologists to study animal behavior with the hope of generalizing across species. Ethology generates the systematic, cross-taxon descriptions of behavior that comparative psychologists rely on. If you don't know what an animal does, how in the world are you supposed to study it?
The basic structure of an animal's behavior is referred to as an ethogram. Ethograms have been developed for a wide variety of species. These are essentially attempts to create a complete catalogue of a species' behavior. Ethograms can be quantitative (that is, quantify how much an animal does each activity in its repertoire) or merely descriptive. In some commonly used laboratory species (take the rat, for example) ethology has been largely left by the wayside, due in part to a focus on generalizing experiments to human psychology or biology. This appears, to me, to be very unfortunate, as we risk losing our perspective on what the behaviors we study mean to the animal performing them.
The field started with the studies of animal behavior by Konrad Lorenz, who was interested in "instinctive" behaviors in a variety of species, most of them birds (for a good review of history, see http://apophenia.wdfiles.com/local--files/start/tinbergen.pdf). The goal of ethology is stated in a deceptively simple way: to study the behavior of animals. It seems to me to straddle the junction of zoology and psychology, studying behavior from the perspective of animal biology, much as biological psychology studies human behavior in reference to human biology.
It turns out that ethologists do, in essence, the legwork that allows comparative psychologists to study animal behavior with the hope of generalizing across species. Ethology generates the systematic, cross-taxon descriptions of behavior that comparative psychologists rely on. If you don't know what an animal does, how in the world are you supposed to study it?
The basic structure of an animal's behavior is referred to as an ethogram. Ethograms have been developed for a wide variety of species. These are essentially attempts to create a complete catalogue of a species' behavior. Ethograms can be quantitative (that is, quantify how much an animal does each activity in its repertoire) or merely descriptive. In some commonly used laboratory species (take the rat, for example) ethology has been largely left by the wayside, due in part to a focus on generalizing experiments to human psychology or biology. This appears, to me, to be very unfortunate, as we risk losing our perspective on what the behaviors we study mean to the animal performing them.
For example, consider the classical learning experiments in rats that use the lever press as an operant response. Ethologists would never have tried to study learning in the rat using a lever-pressing behavior. Rats, if left to their own devices, simply do not tend to press levers! More recently, nose-poking (a very common and easy thing for a rat to do) has gained some popularity as an operant response, and has made this research much easier to conduct as well as more flexible. Knowing the behavioral repertoire of an animal is a prerequisite to understanding any particular behavior in that animal, let alone using it to draw inferences about behavior across species.
The take home point: I like ethology.
I didn't bring up ethology just to rave about it, though. I've been reading a number of cephalopod ethograms, and wanted to spread them around. Ethograms are interesting to read because they provide a snapshot of a species - they provide some understanding of its biology, its ecology, and its psychology, all in one.
In Ethogram of Abdopus aculeatus (d'Orbigny, 1834) (Cephalopoda: Octopodidae): Can behavioural characters inform octopodid taxomony and systematics?, Christine Huffard lays out an ethogram of Abdopus aculeatus, a species of small octopus that lives in indonesia (for videos and a press release on her findings, see this link) In this press release, she mentions how much of our information about octopus behavior comes from a few, rather old sources, and not a diverse and current range of ethological studies, as one might hope for. I find this to be frustratingly true - when you look at the literature on octopus behavior, it seems like many experimental biologists quickly jumped on the octopus as a system to study something (vision, motor control, learning) largely without taking to trouble to investigate and re-investigate its behavior in ecological conditions. The sources that exist on this topic are mainly books, not journal articles - both less accessible and less stringently peer reviewed. Huffard's articles are like a breath of fresh air in the world of octopod behavior.
Here's a few pictures of the pretty little guy:
(Figure 2 from Locomotion by Abdopus aculeatus (Cephalopoda: Octopodidae): walking the line between primary and secondary defenses (2006), also by Huffard. The supplementary material for this paper also has a few good videos of A. aculeatus moving about.)
Now comes the big question: what did the study find?
Well, the study does a very good job answering the question: what does this animal do? Huffard found that A. aculeatus is diurnal, both mating and foraging primarily during the day. Like other octopuses, they forage using mainly their tactile sense (although sometimes visually,) groping the substrate to locate prey.
A. aculeatus shows a great variety of body patterns, including really impressive papillae (bumps on the skin that can be made larger or smaller as part of a body pattern) and a variety of color patterns, mainly used for camouflage.
Perhaps the most striking findings are about the social and sexual behavior of A. aculeatus. Octopuses are known for being solitary creatures, but Huffard describes the presence of specific male-male aggressive interactions, usually in the presence of a female. Sometimes, it even appeared that one octopus would try to strangle its opponent by "[wrapping] one arm around the mantle opening of another individual, presumably cutting off ventilation." It was also found that males actively guarded their mate females from other males, whom they often mated repeatedly with over a few days. This is in contrast to the relatively simple meet-and-mate behavior that has been described in other octopus species.
Huffard ends the paper with a discussion of the use of skin components and other behaviors to clarify octopus systematics. She makes the argument that O. cyanea shows certain behavioral similarities to A aculeatus, as well as being closely phylogenetically related, demonstrating that behavior can inform phylogeny. While this is suggestive that behavior might be useful in classifying organisms, I think that it remains to be seen whether this is a reliable way to do it (at least, more reliable than molecular phylogenetics, upon which her argument appears to rest.) The case for this seems like it would fall prey to the problem of convergent evolution, as it appears relatively easy to evolve nearly identical behaviors and morphologies independently, but harder to evolve identical nucleotide sequences independently. Frustrating this issue, she mentions, is the fact that there are no published ethograms for cogeners of A. aculeatus.
Thanks for reading!
Saturday, June 12, 2010
Cuttlefish Chromatophores
I'd like to take a minute to talk about chromatophores. These are the pigment organs that allow cephalopods to change their color and body pattern, like this pretty little guy is doing:
(Photo by Nick Hobgood)
Neuroscientists (at least some of them) seem to get pretty excited about cephalopod chromatophores, because they are neurally controlled instead of hormonally controlled - this makes them unique among chromatophores, which are found in a wide variety of animals including fish, reptiles, and some invertebrates. Each of a cephalopod's chromatophores is innervated directly, which allows it to change color quickly to make a huge variety of patterns. Besides allowing cephalopods to exhibit remarkable color-changing behavior, chromatophores give us a chance to study a unique neural system whose operation probably sits somewhere between autonomic or reflexive activity and voluntary control, and which has no clear homolog in vertebrate neurvous systems.
Chromatophores themselves are interesting structures. They consist of a central area of pigment surrounded by radially organized muscles. When these muscles contract, the chromatophore widens from its usual contracted state. By coordinating the movement of the muscles of many chromatophores, cephalopods can create a variety of body patterns. Here is a diagram of the organ:
(Figure from Peptidergic Regulation of Chromatophore Function in the European Cuttlefish Sepia Officinalis by Loi et al. (1996).)
When one considers that even a small cuttlefish has hundreds of these organs, all controlled via neurons emanating from the central nervous system, the chromatophore system and the behaviors it makes possible become very impressive.
To bring this post back towards the topic of brains, let's consider the innervation of chromatophores. I should point out that chromatophores are mostly studied in Sepia (that is, in cuttlefish,) because this species has very densely placed chromatophores and some of the most conspicuous patterns of coloration. Some work has been done in squid and octopus, but the vast majority of the literature on cephalopod chromatophores is restricted to cuttlefish. As such, while I work under the assumption that most cephalopod chromatophore systems are similar to what's been described in the cuttlefish, this is only an assumption on my part, and remains to be seen.
In Peripheral innervation patterns and central distribution of fin chromatophore motoneurons in the cuttlefish Sepia officinalis by Gaston and Tublitz (2004), the authors present data illustrating the pattern of innervation of chromatophores in the fin of cuttlefish. What they find is that the fin nerve is highly branched and innervates the fin muscles and chromatophores in an apparently efficient manner. Here is a photograph of their preparation, showing the branching fin nerve:
While this is cool, I'm more concerned with their findings regarding of the source of the neurons that innervate the chromatophores. The authors used a method called retrograde labeling to investigate this. In this technique, nerves are dyed somewhere in the periphery (in this case, the fins), the dye is given time to fill the whole neuron, and the it can be located in the central nervous system by slicing the brain and looking at it microscopically. Gaston and Tublitz found that most of the neurons innervating chromatophores originated from the posterior suboesophageal mass (in the following image, found towards the bottom right - one of the lobes of the posterior suboesophageal mass, the pallidovisceral (pv.) is labeled.) This is perhaps not surprising, because it has been known since Young's work in Octopus in the 1960's that much of the innervation of the mantle organs and musculature arises from the posterior suboesophageal mass.
The cuttlefish brain is pretty similar to the octopus brain in its organization. The following figure is a sagittal section of a cuttlefish brain and buccal mass from "The Brains and Lives of Cephalopods" by Nixon and Young (which is a wonderful book, by the way.) In terms of orientation, the mouth is to the left of this figure (the beak and lip are labeled,) the supraoesophageal mass is towards the top of the image, and the suboesophageal mass is towards the bottom of the image. I like this image because it situations the brain in the context of the larger structure of the head of the cuttlefish.
Although there is a growing literature on the subject, there are still lots of questions to be asked about chromatophores. I would personally love to see more research on the representation of the skin's surface within the neural system controlling the chromatophores. It would be neat to see if somatotopy was present, and in what forms. Also, the possibility of the systems that control chromatophores working as part of some sort of generalized stress- or motivation-related system is very interesting to me.
For the interested reader, here are some other free, full-text resources on chromatophores:
Neural regulation of a complex behavior: body patterning in cephalopod molluscs by Tublitz, Gaston, and Loi (2006, Integrative and Comparative Biology)
Cephalopod chromatophores: neurobiology and natural history by Messenger (2001, Biological Reviews)
Neural Correlates of Colour Change in Cuttlefish by Messenger and Miyan (1986, Journal of Experimental Biology)
Thanks for reading. See you next time!
Neuroscientists (at least some of them) seem to get pretty excited about cephalopod chromatophores, because they are neurally controlled instead of hormonally controlled - this makes them unique among chromatophores, which are found in a wide variety of animals including fish, reptiles, and some invertebrates. Each of a cephalopod's chromatophores is innervated directly, which allows it to change color quickly to make a huge variety of patterns. Besides allowing cephalopods to exhibit remarkable color-changing behavior, chromatophores give us a chance to study a unique neural system whose operation probably sits somewhere between autonomic or reflexive activity and voluntary control, and which has no clear homolog in vertebrate neurvous systems.
Chromatophores themselves are interesting structures. They consist of a central area of pigment surrounded by radially organized muscles. When these muscles contract, the chromatophore widens from its usual contracted state. By coordinating the movement of the muscles of many chromatophores, cephalopods can create a variety of body patterns. Here is a diagram of the organ:
When one considers that even a small cuttlefish has hundreds of these organs, all controlled via neurons emanating from the central nervous system, the chromatophore system and the behaviors it makes possible become very impressive.
To bring this post back towards the topic of brains, let's consider the innervation of chromatophores. I should point out that chromatophores are mostly studied in Sepia (that is, in cuttlefish,) because this species has very densely placed chromatophores and some of the most conspicuous patterns of coloration. Some work has been done in squid and octopus, but the vast majority of the literature on cephalopod chromatophores is restricted to cuttlefish. As such, while I work under the assumption that most cephalopod chromatophore systems are similar to what's been described in the cuttlefish, this is only an assumption on my part, and remains to be seen.
In Peripheral innervation patterns and central distribution of fin chromatophore motoneurons in the cuttlefish Sepia officinalis by Gaston and Tublitz (2004), the authors present data illustrating the pattern of innervation of chromatophores in the fin of cuttlefish. What they find is that the fin nerve is highly branched and innervates the fin muscles and chromatophores in an apparently efficient manner. Here is a photograph of their preparation, showing the branching fin nerve:
The cuttlefish brain is pretty similar to the octopus brain in its organization. The following figure is a sagittal section of a cuttlefish brain and buccal mass from "The Brains and Lives of Cephalopods" by Nixon and Young (which is a wonderful book, by the way.) In terms of orientation, the mouth is to the left of this figure (the beak and lip are labeled,) the supraoesophageal mass is towards the top of the image, and the suboesophageal mass is towards the bottom of the image. I like this image because it situations the brain in the context of the larger structure of the head of the cuttlefish.
Although there is a growing literature on the subject, there are still lots of questions to be asked about chromatophores. I would personally love to see more research on the representation of the skin's surface within the neural system controlling the chromatophores. It would be neat to see if somatotopy was present, and in what forms. Also, the possibility of the systems that control chromatophores working as part of some sort of generalized stress- or motivation-related system is very interesting to me.
For the interested reader, here are some other free, full-text resources on chromatophores:
Neural regulation of a complex behavior: body patterning in cephalopod molluscs by Tublitz, Gaston, and Loi (2006, Integrative and Comparative Biology)
Cephalopod chromatophores: neurobiology and natural history by Messenger (2001, Biological Reviews)
Neural Correlates of Colour Change in Cuttlefish by Messenger and Miyan (1986, Journal of Experimental Biology)
Thanks for reading. See you next time!
Wednesday, June 9, 2010
A View of the Octopus Brain.
In this post, I am going to outline octopus neuroanatomy, to the best of my ability. It's a complicated subject that I am only beginning to have a grasp on, but I want to post more about specific research papers regarding cephalopod brains, so I figure I should review this first. Let's get right to it.
This figure is from J. Z. Young's "The Anatomy of the Nervous System of Octopus Vulgaris" (1971, which I was fortunate enough to come across recently. If you're familiar with looking at mammalian brains (like me,) you'll be utterly lost. This is a view of the octopus brain from above - imagine that the octopus is lying on a table, it's mantle away from you and its tentacle towards you, it's eyes looking longingly into yours. Its brain would be oriented as shown. The two big swellings on either side are the optic lobes, which sit just underneath the eyes. The rest of the octopus brain is wrapped around the esophagus. The brachial nerve (labeled "n.br." and seen towards the bottom of this figure) travels out to innervate the arms (more precisely, we might say, to connect the nervous system of the head and the nervous system of the arms, which is hugely complex in its own right.) See this diagram of octopus general anatomy to get an idea of the size of the brain relative to the octopus's body, as well as the nervous system of the arms.
This is a figure from the same work showing a section of the octopus brain from the side. In this figure, the mouth and tentacles would be off to the left, with the mantle off to the right. The big white hole in the middle of the brain is at the level of the oesophagus, although I'm not sure if it is actually the oesophagus in this section. The brain is thus divided into supraoesophageal and suboesophageal masses (the former being above and the latter below the oesophagus.) This image does not include the optic lobes.
While the octopus brain is smaller than that of birds or mammals when adjusted for body weight, it is still a highly-developed, centralized brain with specialized substructures within it. Within the next few weeks, I'll try to cover some of the research that has been done to map the functionality of the cephalopod brain, as scant as it is in comparison to the literature on mammalian brains. For now, though, I'll go through it briefly.
It is misleading, actually, to focus only on the brain if we're trying to understand the nervous system of octopus - most of the neurons in an octopus (roughly 2/3 of them, actually) lie in the nervous system of the arms, which is thought to control some aspects of movement with little input from the brain.
Young divides the octopus brain into 5 functional areas: Lower, intermediate, and higher motor centers, receptor analyzers, and memory centers. We'll go through them all briefly.
Lower motor centers are those which contains the neurons controlling muscles directly. These neurons effect muscle contraction, and so make possible the movement of the animal. These are analagous to some neurons in human motor cortex, as well as those in the spinal cord. In the octopus, these are located in the nervous system of the arms.
Intermediate motor centers (located in the anterior suboesophageal mass in the pre- and post-brachial lobes (br.pr. and br.po.), as well as others) coordinate movements between the arms in a way that is beyond that of the lower motor centers. These areas are comparable to some neurons in mammalian motor and premotor cortex that, when stimulate, produce complex patterns of movements, but which generally fall short of that seen when an organism is behaving freely.
Higher motor centers, located (for example) in the basal lobe (b.l.) control complex behaviors that involve the animal's whole body. I am not sure that these have a parallel in the mammalian brain, but my guess is that it would lie somewhere in premotor cortex, coordinating the activities of the motor units further down the chain of command.
Receptor analyzers are those parts of the brain that interpret incoming information from sensory receptors. Notable, in the octopus, they include the optic lobes (opt.) which analyzes incoming visual information, and the buccal system (buc.s.) which analyzes information from touch receptors in the arms and buccal mass (the area at the convergence of the arms, where the beak is located.) The mammalian brain has lots of these as well, for example the inferior and superior colliculi, which analyze incoming auditory and visual information, respectively.
Last, but certainly not least, are the memory centers. The memory system in octopus (and in cuttlefish, as I'll post about later on) is distributed among the superior frontal (f.sup.med.), vertical (v.), and subverticle (subv.) lobes, as well as the buccal system, and the inferior frontal (fr.i.med.) lobes. J. Z. Young has made the argument that the organizations of this system show analogy to circuits in the human hippocampus (see Computation in the Learning System of Cephalopods, 1991). I do not know enough about the two systems to agree or disagree with him at this point, but it is an interesting idea, nonetheless.
I hope this has been as informative for you as it has for me! You can count a few more posts on memory research in cuttlefish soon.
Sunday, June 6, 2010
Cuttlefish Memory
Image by David Sim, used under a Creative Commons License.
Being, up to this point, rather octopus-centric in my posts, I decided to dig into the literature on cuttlefish behavior. Cuttlefish are (relatively) easily kept in aquaria, and have been extensively studied in terms of their complex color-changing behavior (see A review of cuttlefish camouflage and object recognition and evidence for depth perception by Kelman, Osorio, and Baddeley for more information on this area of study) as well as their predatory behavior learning abilities, and possible social behavior.
The first paper I want to talk about in this post is Evidence for a specific short-term memory in the cuttlefish by Agin, Dickel, Chichery, and Chichery (1998).
Agin et al's experiment ran as follows: cuttlefish of various ages were shown a prawn or shrimp sealed inside of a glass tube during a training phase. As one might expect, the cuttlefish attacked the glass tube, but learned to suppress their attacking as they learned that the prey was inaccessable. Then, after a 5 minute break, the cuttlefish were tested to see how well they could remember not to attack the prey in the tube. There were 3 groups - the first got 20 minutes of training, the second got 5 minutes of training, and the last was exposed to the empty glass jar for 20 minutes as a control group.
In a nutshell, here are their results: Juvenile cuttlefish (15-30 days old) learned to suppress attack in the 20-minute condition only, while for older cuttlefish, a 5 minute exposure was enough for them to learn the lesson and almost completely suppress attack.
This is all well and good by itself. We would more or less expect that cuttlefish should be able to retain this simple memory, knowing how good cephalopods are at that sort of thing. What makes this story more interesting is this groups follow-up paper.
In Effects of learning on cytochrome oxidase activity in cuttlefish brain by Agin, Chichery, and Chichery (2001), the group subjected cuttlefish to the same learning task and then measured cytochrome oxidase levels in their brains at different time points after learning. Cytochrome oxidase expression is increased in metabolically active cells, putatively indicating (in neurons, at least) the overall activity level of the cell (with rather poor spatial resolution, of course.) What this experiment revealed was that the pattern of cytochrome oxidase staining changed depending on how long it had been since the cuttlefish did the learning task. In other words, it looks rather like different populations of neurons are involved in the early stages of memory than the late stages of memory. A similar effect was found using a marker of acetylcholine synthesis in this study, Central acetylcholine synthesis and catabolism activities in the cuttlefish during aging by Bellanger et al .
This is notable because it suggests that cephalopods, like birds and mammals, may have dissociable short- and long-term memory systems. According to the generally accepted theory of human memory, the short-term and long-term memory systems are comprised of distinct but overlapping neural circuits. It would be very interesting if the same dissociation had developed in cephalopods (in fact, this same group has gathered more behavioral evidence supporting this hypothesis since these studies were published, ie. their study Developmental study of multiple memory stages in the cuttlefish, Sepia officinalis, 2006 .) While it seems that the study of cephalopod memory processes is still in its infancy (compared, at least, to the study of human memory processes) and no strong assertions about this system can be made yet, it's a tantalizing thought that we might be able to find and understand such a striking example of the convergent evolution of neural systems as this.
The first paper I want to talk about in this post is Evidence for a specific short-term memory in the cuttlefish by Agin, Dickel, Chichery, and Chichery (1998).
Agin et al's experiment ran as follows: cuttlefish of various ages were shown a prawn or shrimp sealed inside of a glass tube during a training phase. As one might expect, the cuttlefish attacked the glass tube, but learned to suppress their attacking as they learned that the prey was inaccessable. Then, after a 5 minute break, the cuttlefish were tested to see how well they could remember not to attack the prey in the tube. There were 3 groups - the first got 20 minutes of training, the second got 5 minutes of training, and the last was exposed to the empty glass jar for 20 minutes as a control group.
In a nutshell, here are their results: Juvenile cuttlefish (15-30 days old) learned to suppress attack in the 20-minute condition only, while for older cuttlefish, a 5 minute exposure was enough for them to learn the lesson and almost completely suppress attack.
This is all well and good by itself. We would more or less expect that cuttlefish should be able to retain this simple memory, knowing how good cephalopods are at that sort of thing. What makes this story more interesting is this groups follow-up paper.
In Effects of learning on cytochrome oxidase activity in cuttlefish brain by Agin, Chichery, and Chichery (2001), the group subjected cuttlefish to the same learning task and then measured cytochrome oxidase levels in their brains at different time points after learning. Cytochrome oxidase expression is increased in metabolically active cells, putatively indicating (in neurons, at least) the overall activity level of the cell (with rather poor spatial resolution, of course.) What this experiment revealed was that the pattern of cytochrome oxidase staining changed depending on how long it had been since the cuttlefish did the learning task. In other words, it looks rather like different populations of neurons are involved in the early stages of memory than the late stages of memory. A similar effect was found using a marker of acetylcholine synthesis in this study, Central acetylcholine synthesis and catabolism activities in the cuttlefish during aging by Bellanger et al .
This is notable because it suggests that cephalopods, like birds and mammals, may have dissociable short- and long-term memory systems. According to the generally accepted theory of human memory, the short-term and long-term memory systems are comprised of distinct but overlapping neural circuits. It would be very interesting if the same dissociation had developed in cephalopods (in fact, this same group has gathered more behavioral evidence supporting this hypothesis since these studies were published, ie. their study Developmental study of multiple memory stages in the cuttlefish, Sepia officinalis, 2006 .) While it seems that the study of cephalopod memory processes is still in its infancy (compared, at least, to the study of human memory processes) and no strong assertions about this system can be made yet, it's a tantalizing thought that we might be able to find and understand such a striking example of the convergent evolution of neural systems as this.
Wednesday, June 2, 2010
Cephalopod Consciousness
In their paper Identifying hallmarks of consciousness in non-mammalian species (2005), Edelman, Baars, and Seth put forth the idea that research on consciousness needs to expand beyond methodologies which rely solely on the ability of organism somehow report their concious awareness of something (that is, behavioral tests) and encompass neuroanatomical and neurophysiological investigation. To my delight, they chose to focus on birds and octopuses as examples of animals whose possible consciousness might be probed via non-traditional methods of inquiry.
Citing evidence related the neuroanatomical and functional bases of consciousness in humans and other mammals, the authors eventually conclude that it there is a good case for avian consciousness, and the possibility of cepahlopod consciousness, based on the presence or uncertainty of these three necessary criteria:
(1) identification of neural structures that are the functional equivalents
of cortex and thalamus;
(2) neural dynamics analogous to those observed in mammals during
conscious states
(3) rich discriminatory behavior that suggests a recursive linkage
between perceptual states and memory
I like their style and their argument. However, I really wanted to write about this paper for a much simpler reason. It has one of the best concluding figures that I have ever seen in a paper:
Not only do they have good ideas, but a great illustrator, too.
Citing evidence related the neuroanatomical and functional bases of consciousness in humans and other mammals, the authors eventually conclude that it there is a good case for avian consciousness, and the possibility of cepahlopod consciousness, based on the presence or uncertainty of these three necessary criteria:
(1) identification of neural structures that are the functional equivalents
of cortex and thalamus;
(2) neural dynamics analogous to those observed in mammals during
conscious states
(3) rich discriminatory behavior that suggests a recursive linkage
between perceptual states and memory
I like their style and their argument. However, I really wanted to write about this paper for a much simpler reason. It has one of the best concluding figures that I have ever seen in a paper:
The Urbilaterian
Cephalopods, especially octopuses, have large, complex, functionally differentiated brains. They can learn, perform complex visual and tactile discrimination, play, show complex defensive and aggressive responses, and all sorts of other interesting and highly variable behavior (Jennifer Mather's review of cephalopod behavior is good reading for those who are interested.) Notably, this behavior is unusual among molluscs, who tend to be scavengers or filter-feeders instead of mobile, active predators.
My point is that octopus behavior reminds me a lot of vertebrate behavior and not very much of, let's say, the behavior of clams or sponges, which seems to be mostly limited to sifting for food, moving about to find a better spot to anchor themselves, and mating by ejecting sperm into the water. Their brains are organized in ways that are reminiscent of vertebrate brains, notably in their memory systems and visual processing systems (see my earlier post on the Octopus visual system for a better, though still brief, treatment of this topic.)
These facts about cephalopods are part of what originally piqued my interest in them. The study of the similarities and differences between vertebrate and cephalopod neural systems is intriguing to me because vertebrates and cephalopods are presumably very, very distantly related, evolutionarily speaking. Cephalopod and vertebrate nervous systems have been evolving independently from rather rudimentary beginnings, and have somehow ended up having not only somewhat similar capabilities but also apparently similar organization and mechanisms, even at complex levels of information processing. I have a strong feeling that there is something important to be learned about the evolution and development of nervous systems from the study of cephalopods.
Following this line of reasoning, it's important to understand just how cephalopods (part of the phylum mollusca) and vertebrates (of the phylum chordata) are evolutionarily related.
The last common ancestor between vertebrata and mollusca is though to have existed at least 550 million years ago (most probably more), around a time referred to as the Cambrian explosion. It's called that because drastic evolutionary differentiation occured during a short time, resulting in the evolution of many of the taxons that we know today. This ancestor was the "urbilaterian", or the last common ancestor of all of the bilaterians. Bilaterians are animals who have a bilaterally symmetrical body plan - not that their bodies are always symmetrical (just look at the flounder), but their body plan is.
This organism (or a similar one - it depends on who you ask) is also called the protostome-deuterostome ancestor (PDA), because it is thought to represent the last common species before the divergence of the deuterostomes (whose gut grows from their anus inwards, basically) and the protostomes (whose gut used to be thought to grow from the mouth inwards, but is now know to develop in a few different patterns.)
There is a slight technical difference between these terms, with the "urbilaterian" being the last common ancestor of all of bilateria, and the "PDA" being the last common ancestor of only the deuterostomes and the protostomes, but not of the few other small phyla that are also included within bilateria. Despite this, it is not known how to differentiate the two possibilities, nor how they would affect the probable attributes of such an organism. Although the "missing link" that would characterize the relationship between cephalopods and chordates should be technically referred to as the PDA, the authors of the papers I cite use the term "urbilaterian", and so I will stick with this.
It might seem like a stretch to purport to study something that hasn't existed for hundreds of millions of years and that we can never unambiguously identify. Nevertheless, we can know what features the urbilaterian must have had by looking at those features that are common to all Bilateria. This is apparently done using genetic and genomic techniques (which I am admittedly not very familiar with - here I am trusting the authority of the cited authors and their citations.) Erwin and Davidson, in a review titled The Last Common Bilaterian Ancestor (2002) make the argument that one of the important conserved elements of bilateria are genes that regulate cell differentiation - that is, certain cell types (which presumably will later allow the evolution of certain morphological structures) are already present in the urbilaterian and are conserved throughout bilateria. The examples cited by Erwin and Davidson are (possibly among others): photoreceptors, neurons, intestinal-secretory and neuro-secretory cells, cardiac-type and striated muscle cells. Also conserved across Bilateria are a variety of regulatory genes that determine how the expression of genes the cause cell differention occurs during an organisms development. Most of the variation within bilateria is therefore constructed by these (approximately) common cell types and regulatory mechanisms.
So, based on our current understanding of comparative developmental genetics and morphology, the urbilaterian looks something like this:
(Figure is from Acoel development supports a simple planula-like urbilaterian by Hejnol and Martindale, 2007.) This hypothetical little guy has a central nervous system; although, Hejnol and Martindale argue, it's likely that it is primarily net-like rather than based around a centralized ganglion. Notably, it has photoreceptive cells (essential for the evolution of eyes) and epidermal sensory cells. It also has striated and smooth muscle cells, and the nervous apparatus to use them both. It has a blind gut (meaning that its food intake and waste output use the same cavity) with specialized secretory cells, no appendages, and no body segmentation. In short, although it looks very simple, it contains all of the building blocks to make the huge diversity of lifeforms we have today, as well as all those that have evolved from it and since become extinct. These are listed, in part, in the chart in the bottom half of this figure, showing the genes implicated in the differentiation of conserved body features along with a diagram of where they are expressed in two different hypothetical bilaterial (the right being the one supported by the authors.)
So, this is the point of the story: if we understand humans well, and we understand other species (including cephalopods) well, then we might be able to determine what features of each are likely to be due to inherent constraints in all bilaterian biological systems, and which have evolved more through more open-ended mechanisms. From this, we could learn very general rules about how bodies grow and develop, and of specific interest to neuroscientists, how complex neural circuits are wired up. This would bring us a huge step closer to understanding brains in general, as well as our specific human brains.
My point is that octopus behavior reminds me a lot of vertebrate behavior and not very much of, let's say, the behavior of clams or sponges, which seems to be mostly limited to sifting for food, moving about to find a better spot to anchor themselves, and mating by ejecting sperm into the water. Their brains are organized in ways that are reminiscent of vertebrate brains, notably in their memory systems and visual processing systems (see my earlier post on the Octopus visual system for a better, though still brief, treatment of this topic.)
These facts about cephalopods are part of what originally piqued my interest in them. The study of the similarities and differences between vertebrate and cephalopod neural systems is intriguing to me because vertebrates and cephalopods are presumably very, very distantly related, evolutionarily speaking. Cephalopod and vertebrate nervous systems have been evolving independently from rather rudimentary beginnings, and have somehow ended up having not only somewhat similar capabilities but also apparently similar organization and mechanisms, even at complex levels of information processing. I have a strong feeling that there is something important to be learned about the evolution and development of nervous systems from the study of cephalopods.
Following this line of reasoning, it's important to understand just how cephalopods (part of the phylum mollusca) and vertebrates (of the phylum chordata) are evolutionarily related.
The last common ancestor between vertebrata and mollusca is though to have existed at least 550 million years ago (most probably more), around a time referred to as the Cambrian explosion. It's called that because drastic evolutionary differentiation occured during a short time, resulting in the evolution of many of the taxons that we know today. This ancestor was the "urbilaterian", or the last common ancestor of all of the bilaterians. Bilaterians are animals who have a bilaterally symmetrical body plan - not that their bodies are always symmetrical (just look at the flounder), but their body plan is.
This organism (or a similar one - it depends on who you ask) is also called the protostome-deuterostome ancestor (PDA), because it is thought to represent the last common species before the divergence of the deuterostomes (whose gut grows from their anus inwards, basically) and the protostomes (whose gut used to be thought to grow from the mouth inwards, but is now know to develop in a few different patterns.)
There is a slight technical difference between these terms, with the "urbilaterian" being the last common ancestor of all of bilateria, and the "PDA" being the last common ancestor of only the deuterostomes and the protostomes, but not of the few other small phyla that are also included within bilateria. Despite this, it is not known how to differentiate the two possibilities, nor how they would affect the probable attributes of such an organism. Although the "missing link" that would characterize the relationship between cephalopods and chordates should be technically referred to as the PDA, the authors of the papers I cite use the term "urbilaterian", and so I will stick with this.
It might seem like a stretch to purport to study something that hasn't existed for hundreds of millions of years and that we can never unambiguously identify. Nevertheless, we can know what features the urbilaterian must have had by looking at those features that are common to all Bilateria. This is apparently done using genetic and genomic techniques (which I am admittedly not very familiar with - here I am trusting the authority of the cited authors and their citations.) Erwin and Davidson, in a review titled The Last Common Bilaterian Ancestor (2002) make the argument that one of the important conserved elements of bilateria are genes that regulate cell differentiation - that is, certain cell types (which presumably will later allow the evolution of certain morphological structures) are already present in the urbilaterian and are conserved throughout bilateria. The examples cited by Erwin and Davidson are (possibly among others): photoreceptors, neurons, intestinal-secretory and neuro-secretory cells, cardiac-type and striated muscle cells. Also conserved across Bilateria are a variety of regulatory genes that determine how the expression of genes the cause cell differention occurs during an organisms development. Most of the variation within bilateria is therefore constructed by these (approximately) common cell types and regulatory mechanisms.
So, based on our current understanding of comparative developmental genetics and morphology, the urbilaterian looks something like this:
(Figure is from Acoel development supports a simple planula-like urbilaterian by Hejnol and Martindale, 2007.) This hypothetical little guy has a central nervous system; although, Hejnol and Martindale argue, it's likely that it is primarily net-like rather than based around a centralized ganglion. Notably, it has photoreceptive cells (essential for the evolution of eyes) and epidermal sensory cells. It also has striated and smooth muscle cells, and the nervous apparatus to use them both. It has a blind gut (meaning that its food intake and waste output use the same cavity) with specialized secretory cells, no appendages, and no body segmentation. In short, although it looks very simple, it contains all of the building blocks to make the huge diversity of lifeforms we have today, as well as all those that have evolved from it and since become extinct. These are listed, in part, in the chart in the bottom half of this figure, showing the genes implicated in the differentiation of conserved body features along with a diagram of where they are expressed in two different hypothetical bilaterial (the right being the one supported by the authors.)
So, this is the point of the story: if we understand humans well, and we understand other species (including cephalopods) well, then we might be able to determine what features of each are likely to be due to inherent constraints in all bilaterian biological systems, and which have evolved more through more open-ended mechanisms. From this, we could learn very general rules about how bodies grow and develop, and of specific interest to neuroscientists, how complex neural circuits are wired up. This would bring us a huge step closer to understanding brains in general, as well as our specific human brains.
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