Do leeches have free will?

If a leech (limatek, aka Hirudo medicinalis) is poked on its side, sometimes it swims, sometimes it crawls, sometimes it does nothing at all. For a supposedly simple animal, that is quite a remarkable repertoire of responses to the same stimulus. How does it decide what to do? Does it actually decide? Indeed, is "decision" an appropriate term to use in connection with a leech?

When this behavior is shown by a leech in the wild, we may wonder if the poke is the only stimulus provoking its reaction. Does its response depend also on the temperature of the water in which it finds itself? Does it depend on the motion, or lack of motion of the water? Maybe it depends on the way in which the poke was delivered? After all, just "poking" is hardly a controlled experimental procedure.

Mindful of the need to study the leech’s behavior under controlled circumstances, biologists have devised a way of studying the animal’s nervous system in isolation. By performing a delicate surgery, they detach the leech’s nervous system from the rest of its body, they throw away the latter, and study the isolated network of nerve cells, giving it an "out of body experience," as it were.

The state of the isolated nervous system is indicated by the electrical signals that the various nerve cells generate and transmit to each other. Although muscles are no longer there to perform swimming or crawling motions, motor neurons still generate signals that biologists can identify uniquely as commands for the no longer existent muscles to swim, or to crawl. "Fictive swimming," and "fictive crawling," they call these signals.

One reason for the interest in the leech is that its nervous system is relatively simple. Almost every nerve cell and its interconnections have been identified. On the other hand, it is complicated enough that it can display the variety of behaviors that made us wonder earlier if it is, in fact, capable of making decisions.

Once the leech’s nervous system has been isolated and mounted on a dish, instead of poking it on its side, an experimenter can now deliver a precisely controlled amount of electrical charge to a neuron in one of the leech’s brains (it has two brains, by the way, one at its front end, another at the rear). When stimulated in this manner, under tightly controlled conditions, it is still so that sometimes it displays fictive swimming, sometimes fictive crawling, sometimes nothing at all…

I first heard of this phenomenon from a colleague, Peter Brodfuehrer, who teaches biology at Bryn Mawr College. My immediate reaction was only half in jest – "surely, this shows that the leech has free will!"

"Shut up," Peter said. "You’re a physicist. Go calculate something."

Thus began a collaboration between Peter and his students and me and my students. The biologists do the electrophysiological experiments, the physicists do the numerical analysis. It has worked quite well. The biologists enjoy manipulating the leech’s nervous system, and the physicists, some of whom do not wish to get any closer to leeches than the CDs on which leech data have been recorded, happily deal with the numbers.

Bryn Mawr College biologist Peter Brodfuehrer and his students and my students and I have been engaged for some time in a collaboration to study some aspects of the behavior of the leech (limatek). When an interneuron in one of the leech’s two brains is electrically stimulated, sometimes its nervous system generates signals associated with swimming, sometimes it generates signals associated with crawling, sometimes, it does not generate any signals associated with any obvert behavior. In this interdisciplinary study, the biologists perform the electrophysiological experiments while the physicists do the numerical analysis of the biologists’ results.

So, what has this motley crew found? So far, maybe just the beginnings of what could well be a very long and complex story. Before the stimulus is delivered, the level of electrical activity in the ventral cord of those that will eventually swim (let’s call them the "swimmers") significantly exceeds the activity in those that will eventually crawl (the "crawlers") which, in turn, is slightly greater than in those who will do nothing (the "do-nothings"). It is as if there is a threshold level of activity for swimming or crawling to occur and if, before stimulation, the activity is already high enough, it would become easier for the stimulus to bring it up to the threshold. But it gets more complicated than that.

Once the stimulus is delivered, the nervous system activity in all cases suddenly jumps. The swimmer and crawler signals rise to the same maximum level, then they both decline following pretty much indistinguishable trajectories. After about a second, however, the swimmer signal rises again, diverging from the crawler signal, which now has leveled off. Some three seconds on average after the divergence of the signals, with the swimmer signal still rising, swimming begins. Crawling also occurs at about this time.

The signal from the "do-nothings," on the other hand, does not rise to the same maximum value as those of the swimmers and the crawlers. It starts declining at the same time as the other two, and levels off when the crawler signal does, but it does so at a significantly lower value.

The "decision," if we can call it that, to do something rather than nothing seems to be made at stimulus onset and may well be dictated by the pre-stimulus level of the ventral cord electrical activity. The response of the do-nothings to the stimulus is consistently lower than that of the swimmers or the crawlers.

The swim/crawl decision comes later, when the swimmer signal diverges from the crawler signal. It is not clear that this decision could also have been dictated by the pre-stimulus level of the ventral cord activity. Between stimulus onset and the swim/crawl decision, the indistinguishability of the swimmer and crawler signals suggests that these signals do not carry any memory of their pre-stimulus levels. Or, do they?

So, what determines the swim/crawl decision?

The study of nonlinear dynamical systems has shown that for systems capable of what is now called chaotic motion, very small differences in initial conditions can lead to widely divergent futures. Edward Lorenz, one of the pioneers in the study of chaos, is famously quoted as asking, "Can a butterfly flapping its wings in Brazil cause a hurricane in Texas?"

Could it be that this is what’s happening here? Could it be that whether the leech swims or crawls ultimately depends on a cause as seemingly insignificant in global meteorological terms as the flapping of a butterfly’s wings in Brazil?

This is by no means an original speculation. In the mid-1980s, when nonlinear dynamics was becoming a fashionable scientific field, a group of young pioneers – James Crutchfield, Doyne Farmer, Norman Packard, and Robert Shaw – wondered if perhaps "… chaos provides a mechanism that allows for free will within a world governed by deterministic laws."

Crutchfield and his friends were, of course, referring to free will in people … but what about leeches?

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Alfonso M. Albano is Marion Reilly Professor Emeritus of Physics at Bryn Mawr College in Bryn Mawr, Pennsylvania, USA. His research interests are in nonlinear dynamics and the use of nonlinear dynamical techniques in the analysis of complex biological and biomedical signals. He can be reached at [email protected].