Variability of Swallowing Performance in Intact, Freely FeedingAplysia

Abstract

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.

Behavioral andIn VitroCorrelates of Compulsive-Like Food Seeking Induced by Operant Conditioning inAplysia

“…There is considerable evidence that radula movements, which are organized in an all-or-none action pattern of protraction-retraction mouth closure, constitute a highly variable component of Aplysia feeding behavior (Horn et al, 2004;Jing et al, 2004;Jing and Weiss, 2005;Lum et al, 2005;Zhurov et al, 2005;Ye et al, 2006). We now show that the temporal structure of radula bite cycles during food seeking is also a flexible constituent of this behavior.…”

“…We next analyzed the temporal organization of the more frequent radula biting after appetitive training. It was reported previously that, during active consumption of long strips of seaweed, radula movements are expressed in a rhythmic pattern, i.e., with regular intervals between successive protraction/retraction cycles (Kupfermann, 1974) (but see Lum et al, 2005). During foodseeking behavior that preceded reward stimulation, however, we found that only a small proportion of animals (control, 0 of 10; seaweed, 1 of 10; cellulose, 2 of 10) generated such rhythmic biting (as defined by autocorrelation analysis) and that these proportions were not significantly different among the three animal groups (control vs seaweed, P ϭ 1; seaweed vs cellulose, P ϭ 1; control vs cellulose, P ϭ 0.47).…”

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

“…Conversely, the weak correlation when B64 latencies were negative is consistent with the idea that the B64-independent means of protraction termination may make an important contribution to protraction termination when B64 is hyperpolarized, and these B64-independent actions are not highly correlated with how negative B64 latencies are. Also, if one considers that, under control conditions, B64 latencies are on the order of tens of milliseconds, whereas hyperpolarizations of B64 extend the duration of protractions by Ͼ10 s, it is perhaps not surprising that, given the biological variability in the feeding system of Aplysia (Horn et al, 2004;Lum et al, 2005;Ye et al, 2006;Nargeot et al, 2007), the correlation was weak.…”

A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity

“…In the Aplysia feeding system, these coordinations are well documented at the level of activity in identified interneurons, whereas for turtle scratch and hind limb swimming movements different couplings between pattern-generating modules are postulated. In both cases, however, although distinct switches in coordinations are observed, much emphasis has been placed on the demonstration that intermediate coordination states exist and even grade into one another and that the realization of coordination mode is determined by internal state and sensory stimulation, e.g., seemingly more by the site of irritation in the case of turtle scratch (Stein 2005) and more by internal state (sensory history) in the case of Aplysia feeding (Lum et al 2005;Zhurov et al 2005). Indeed in the hind limb of the turtle even hybrids between scratch and hind limb swimming patterns are observed.…”