This is possibly the best opening line to a peer-reviewed research paper that I have ever read:
When I tell people I've been working on headless fruit flies' responses to light, they often look puzzled or laugh nervously. Allow me briefly to explain why I started cutting off flies' heads.
In this highly readable paper by Marc Egeth, we learn that flies continue to respond to light under conditions where they shouldn't be able to—namely, when their phyiscal movement is dulled by high doses of anesthesia, and (more astoundingly) when their heads have been severed from their bodies. This has some implications for the anesthesia—obviously, it doesn't completely restrict movement, so it would be interesting to know whether it's dulling pain as much as we think it is.
But it also raises some questions about what the heck is going on with the flies' sensory perception. Egeth has two theories. Prepare to get your mind blown a bit, on several subjects:
By what mechanism might headless flies detect light? Two possibilities are photodetection or thermodetection.
The light source itself was not hot because the light was channeled away from the halogen bulb by fiber optics (the instrument was a Schott ACE microscope light). In addition, I also found that headless anesthetized flies would move in response to a light from a 100-lumen LED flashlight, which does not get hot.
But, the flies might be responding to being heated by the infrared components of these lights. Or, the flies' extracephalic photoreceptors, which have previously been implicated in circadian entrainment, might also directly drive behavior. For readers of Perception, photoreception might be a more interesting alternative than movement in response to warmth, but either mechanism would be a novel phenomenon for the body of fly literature (Xu et al, 2006).
Headless flies are known to maintain posture, walk around, entrain to new circadian rhythms, engage in defensive behavior against conspecifics, and even learn to avoid a shock - and this even faster than flies with heads [emphasis mine](Booker & Quinn, 1981).
Butterflies have photoreceptors in their penises that guide mating behavior (leading to the phenomenon termed "hindsight"), and crayfish have "caudal photoreceptors" and thermoreceptors that can drive walking behavior without the involvement of the brain (Arikawa, Suyama & Fujii, 1997; Wilkens, 1988). After I submitted this paper, Xiang et. al. (2010) reported that light-responsive cells "enable [Drosophila] larvae to sense light exposure over their entire bodies and move out of danger." It seems plausible that similar cells are present in adult Drosophila bodies. These phenomena remind us that central human processes may be found distributed throughout the invertebrate body.
Naturally, the first thing this makes me think about is cephalopods. Like the flies, cephalopods are invertebrates. They also have a brain that distributes processing around the body. And, the like animals mentioned by Egeth, researchers have found evidence that cephalopods sense light in places other than their eyes. In fact, Roger Hanlon, a researcher at the Woods Hole Marine Biological Laboratory, thinks that octopuses might be color-blind in their eyes, but perceive color through light-sensitive parts of their skin. (You can find out more about this by fast forwarding to the 20-minute mark in the video I made for BoingBoing about cephalopod neurobiology.)
There's clearly some really interesting stuff going on in the world of the invertebrate senses. I, for one, cannot wait to see what we find out next.
Read Marc Egeth's paper on light-responsive headless flies
Watch a video Egeth made where you can see the flies respond as he turns a microscope light on and off.
Big thanks to Daniel Graham!