Recently, I emailed Catharine Rankin (an acknowledged specialist in learning processes in C. elegans) and asked her about Abramson's restrictive definition of operant conditioning. In response to my query "Do we know if C. elegans is capable of true operant conditioning?", Rankin replied, "No-one has shown this" (personal email, 31 May 2003).
However, there are some very recent studies that suggest that C. elegans may be capable of operant behaviour, after all. It is well-known that C. elegans migrates toward a preferred temperature on a thermal gradient. Zariwala, Miller, Faumont, and Lockery (2003) subjected unrestrained wild-type worms and mutant cryophilic (cold-loving) and thermophilic (heat-loving) worms to sudden temperature "steps" of 3C up or down from the temperature in which they had been raised (20C). An "ethogram" was constructed, and the worms' principal ways of moving (or "behavioural states") were identified - forward locomotion, "reversals" (in which a worm moves backward for several seconds and then goes forward again in a new direction), and "omega turns", (where the worm's head bends around to touch its tail during forward locomotion, momentarily forming a shape like the Greek letter). Statistical analysis had previously shown that reversals and omega turns occur in bursts that have been termed "pirouettes". The researchers tested the hypothesis that worms tend to pirouette more when they are moving away from their preferred temperature (as pirouettes might serve to direct worms back to this temperature), while their tendency to turn should decrease when they are moving toward their preferred temperature. The authors of the study summarised their research as follows:
The authors cautioned that theirs was only the second study of its kind (relating to thermotaxis in C. elegans), and that the previous study (performed in 2002) had produced somewhat different results, possibly because of "significant differences between the temperature stimulus and the definitions of turning behavior used in the two studies" (2003, p. 4376).
Additionally, Nuttley (personal email, 27 August 2003) cites research demonstrating that C. elegans worms are capable of navigating past some aversive barriers of high osmolarity in order to reach an attractive odour. This might indicate some degree of control.
Clearly it would be premature to draw any conclusions from this research, but at least it shows how one might proceed in attempting to verify operant behaviour (in Abramson's sense) in worms. First, it is important to catalogue the patterns of bodily movements of which the test animal is capable (i.e. define an "ethogram"). Second, it is essential to know what attracts it and what repels it. Third, the animal has to control its bodily movements in order to obtain the "reward" or avoid the "punishment".
The real question is: what counts as "control over bodily movements"? An increase in a worm's tendency to turn when it becomes too hot or cold might be a case of controlled behaviour, but it could also be an aversive reaction to change. However, if a worm were able to adjust, say, the rate or degree of its movement as temperature varied, this would be a clearcut case of adjusting a response to fit the contingencies, as Abramson demands.
I would be more convinced that an invertebrate has operant responses if they can adjust their, for example, swimming speed to fit the contingencies. These studies have not been performed (personal email, 2 February 2003, italics mine).
Overall, turning probability was modulated in a manner consistent with a role for turns in thermal migration, although not always as predicted by the pirouette hypothesis in the strict sense (2003, p. 4369).
*** SUMMARY of Conclusions reached