Cephalopods are great subjects for studies on vision, because they are so dependent on their vision that you can get robust behavioral effects by manipulating the visual environment of a test animal. In some new research in the October edition of the Journal of Experimental Biology, CM Talbot and J Marshall (from Queensland) investigate the visual system of the pyjama squid (S. lineolata) and two species of cuttlefish (S. plangon and S. mestrus) – specifically, to find out whether they can respond to polarized light, and in the case of S. lineolata, how photoreceptors are distributed on its retina. I’ve blogged about a study on visual perception in Nautilus before, as well as a study on the retinal topography of squid, so if you would like to see more of the same sort of research, check out those posts.
In these two papers, the authors assessed the ability of their experimental specimens to respond to polarized light by monitoring their optokinetic and optomotor responses to a rotating drum. The optokinetic response is the movement of an animals eyeballs to follow a moving object in the visual environment, while the optomotor response is the movement of the animal’s body to follow movement in the visual environment. The experimenters monitored the optokinetic response in S. lineolata, because it tends to stay motionless on the substrate, partially buried – as such, it will not exhibit an optomotor response under most circumstances. On the other hand, S. plangon and S. mestus both tend to hover in the water, and so show optomotor responses more readily.
A basic scheme of the apparatus used is shown in this figure from the S. lineolata paper:
The animal is in the tank (in this case, prevented from burying itself by being enclosing in a transparent cylinder,) while a drum is rotated around the tank. By varying the pattern on the drum, it is possible to determine the sensory abilities of the animal – assuming that animals generally don’t inhibit optokinetic or optomotor responses, the animal will respond to any pattern it can perceive. If the animal can’t perceive the pattern on the drum (for example, if the drum is visually continuous, as is the case with an all white drum,) it will not perceive any motion and the response will be absent.
The authors used a drum that consisted of alternating stripes of orthogonally oriented polarization filters – that is, the drums were striped, but the difference between adjacent stripes was only in the direction of polarized light that they transmitted. All the stripes transmitted the same total amount of light, and had the same appearance. Thus, the animals would only show an optomotor or optokinetic response to these drums if they could perceive the direction of polarization of the light.
In fact, this is what happened, in all three species. Two control drums were used, one of alternating black and white stripes (to make sure the animals had otherwise normal optokinetic and optomotor responses) and one of a uniform-direction polarization filter (to make sure that the animals weren’t responding to some other part of the drum – the tape used to hold it together, seams resulting from the drum’s construction, etc.,) making it pretty clear that the animals were responding to the alternating directions of polarization and not anything else.
This result is pretty unambiguous, but I’d like to point out a problem that this type of experiment presents in its interpretation: specifically, it’s very difficult to interpret negative results. In this case, it’s very easy to know what it means in terms of the animal’s sensory ability when it responds to a stimulus: it means the animal can detect that stimulus. But what if the cuttlefish didn’t respond (for example, as was found in a very similar study by Darmaillacq and Shashar (2008) in a different species of cuttlefish, Sepia elongata)? It’s hard to know what that means – did the animal fail to perceive the stimulus, or did the stimulus just not mean enough to generate a behavioral response? This is a general problem that crops up in studies on sensation and perception in animals, or any study that relies on an animal perceiving something and emitting a behavioral response. Many things need to happen to get any behavioral response to a stimulus, even one as apparently simple as eye movements. The animal must have a functional sensory apparatus appropriate to perceive the stimulus, it must have the energy and intact musculature to perform whatever behavior it is you’re looking for, it must be expressing no other behaviors that might mask or supress the behavior of interest, it must be motivated to perform the behavior of interest, etc. A negative result in such an experiment means that one of these many things is not the case, but because it’s so difficult to tell the difference between all of these steps between “stimulus” and “behavior”, it’s hard to say what exactly it is that the animal isn’t doing. Is it failing to sense the stimulus, is it failing to respond because the stimulus isn’t relevant, or is it failing to behave because it’s afraid, or stressed, or tired? Darmaillacq and Shashar note that S. elongata has retinal anatomy that looks like it would allow the animal to sense polarized light, and so they are (wisely) wary of claiming that their subjects could not perceive polarized light – but there’s no way to make any claim about S. elongata‘s vision at all from these results (except, of course, the most conservative assertion that S. elongata failed to show an optomotor response to a certain type of polarized-light stimulus under the experimental conditions used in that specific study.)
Fortunately, though, Talbot and Marshall found positive results, and so avoided that quagmire all together. It turns out that all three species they studied can respond to polarized-light stimuli with optokinetic or optomotor responses. They went on to examine the distribution of photoreceptor cells (also called “retinal topography”) in the S. lineolata retina. If you’ll remember from my post on squid visual ecology, it turns out that you can relate the retinal topography of cephalopods to their lifestyle – squids that live near coasts have retinas that are specialized to allow the animal to see below it clearly, whereas oceanic squids have retinas that are specialized for monitoring the water column above them. What might we expect from S. lineolata, an animal who spends much of its time buried in sand? The sensible answer is that is eyes would be specified to look up, since that’s where its predators and prey would be in most cases. Let’s take a look at what Talbot and Marshall found:
The darker the blue is, the higher photoreceptor density is in that area. It turns out that the striped pyjama squid does indeed have a high photoreceptor density in the ventral part of its retina, which probably gives it good visual acuity in the upper part of its visual field (if you don’t know why this is, check out this explanation of image formation in the eye for a primer.) This fits in neatly with what we know about the lifestyle of this squid.
I hope these studies represent the start of a trend towards the study of less “classical” cephalopod species (the “classical” ones being Loligo pealai, Octopus vulgaris, Sepia officinalis.) There’s a lot to learn from the less common species of cephalopods, due in part to the fact they we know very little about most of them.
Thanks for reading!
Talbot CM, & Marshall J (2010). Polarization sensitivity and retinal topography of the striped pyjama squid (Sepioloidea lineolata – Quoy/Gaimard 1832). The Journal of experimental biology, 213 (Pt 19), 3371-7 PMID: 20833931
Talbot CM, & Marshall J (2010). Polarization sensitivity in two species of cuttlefish – Sepia plangon (Gray 1849) and Sepia mestus (Gray 1849) – demonstrated with polarized optomotor stimuli. The Journal of experimental biology, 213 (Pt 19), 3364-70 PMID: 20833930