Cycle-to-Cycle Variability of Neuromuscular Activity inAplysiaFeeding Behavior

Abstract

Aplysia consummatory feeding behavior, a rhythmic cycling of biting, swallowing, and rejection movements, is often said to be stereotyped. Yet closer examination shows that cycles of the behavior are very variable. Here we have quantified and analyzed the variability at several complementary levels in the neuromuscular system. In reduced preparations, we recorded the motor programs produced by the central pattern generator, firing of the motor neurons B15 and B16, and contractions of the accessory radula closer (ARC) muscle while repetitive programs were elicited by stimulation of the esophageal nerve. In other similar experiments, we recorded firing of motor neuron B48 and contractions of the radula opener muscle. In intact animals, we implanted electrodes to record nerve or ARC muscle activity while the animals swallowed controlled strips of seaweed or fed freely. In all cases, we found large variability in all parameters examined. Some of this variability reflected systematic, slow, history-dependent changes in the character of the central motor programs. Even when these trends were factored out, however, by focusing only on the differences between successive cycles, considerable variability remained. This variability was apparently random. Nevertheless, it too was the product of central history dependency because regularizing merely the high-level timing of the programs also regularized many of the downstream neuromuscular parameters. Central motor program variability thus appears directly in the behavior. With regard to the production of functional behavior in any one cycle, the large variability may indicate broad tolerances in the operation of the neuromuscular system. Alternatively, some cycles of the behavior may be dysfunctional. Overall, the variability may be part of an optimal strategy of trial, error, and stabilization that the CNS adopts in an uncertain environment.

Neuromechanics of Coordination during Swallowing inAplysia californica

“…The 2 statistic was not significant (3.63; p Ͼ 0.05), suggesting that each swallow could be analyzed as an independent response. These results are consistent with recent data suggesting that, during feeding in Aplysia, there is significant variability from response to response (Horn et al, 2004).…”

“…1991; Church and Lloyd, 1994) and in vivo (Horn et al, 2004). Variability could be attributable to the changing biomechanics of food, e.g., changes in mechanical load (Hurwitz and Susswein, 1994), to intrinsic variability within the pattern generator, or to changing stimuli within the buccal cavity during ingestion.…”

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.…”

Identification of a New Neuropeptide Precursor Reveals a Novel Source of Extrinsic Modulation in the Feeding System ofAplysia

“…We used two previously characterized input stimuli to elicit the motor programs: the command-like cerebro-buccal interneuron 2 (CBI-2) Morgan et al, 2000Morgan et al, , 2002Jing and Weiss, 2001) and the esophageal nerve (Chiel et al, 1988;Horn et al, 2004;Proekt et al, 2004). CBI-2 was stimulated to fire action potentials at 8 -12 Hz for the duration of the protraction phase so as to elicit a single motor program every 90 s. The esophageal nerve was stimulated with 3 ms current pulses delivered at 6 -7 Hz.…”