Variability of Swallowing Performance in Intact, Freely Feeding Aplysia

Variability in nervous systems is often taken to be merely "noise." Yet in some cases it may play a positive, active role in the production of behavior. The central pattern generator (CPG) that drives the consummatory feeding behaviors of Aplysia generates large, quasi-random variability in the parameters of the feeding motor programs from one cycle to the next; the variability then propagates through the firing patterns of the motor neurons to the contractions of the feeding muscles. We have proposed that, when the animal is faced with a new, imperfectly known feeding task in each cycle, the variability implements a trial-and-error search through the space of possible feeding movements. Although this strategy will not be successful in every cycle, over many cycles it may be the optimal strategy for feeding in an uncertain and changing environment. To play this role, however, the variability must actually appear in the feeding movements and, presumably, in the functional performance of the feeding behavior. Here we have tested this critical prediction. We have developed a technique to measure, in intact, freely feeding animals, the performance of Aplysia swallowing behavior, by continuously recording with a length transducer the movement of the seaweed strip being swallowed. Simultaneously, we have recorded with implanted electrodes activity at each of the internal levels, the CPG, motor neurons, and muscles, of the feeding neuromusculature. Statistical analysis of a large data set of these recordings suggests that functional performance is not determined strongly by one or a few parameters of the internal activity, but weakly by many. Most important, the internal variability does emerge in the behavior and its functional performance. Even when the animal is swallowing a long, perfectly regular seaweed strip, remarkably, the length swallowed from cycle to cycle is extremely variable, as variable as the parameters of the activity of the CPG, motor neurons, and muscles.