Virtually every neural circuit that generates complex behaviors is a multitasking network: it generates not one but multiple behaviors. The fundamental question that we are addressing in this proposal is what endows a single network (central pattern generator; CPG) with this ability to generate multiple behaviors and to switch between them. We propose to study this problem in the context of three forms of feeding behavior, biting, swallowing, and egestion, in the model system Aplysia. Each of these behaviors is initiated by distinct higher-order neurons that contain different complements of neuropeptides. Using a combination of electrophysiological, biochemical, and molecular techniques we propose to test a series of hypotheses. First, we will test the hypothesis that each of the higher-order neurons elicits a distinct behavior by activating individual interneurons from the same network to a different degree. It follows that the individual interneurons, which form the CPG, must differ from each other in the functional roles they fulfill. We propose a scheme to analyze the role that individual interneurons play in generating different behaviors. We propose to test the hypothesis that differences in these roles stem from the neurons' use of different small-molecule transmitters that exert both fast and slow actions. Finally, we propose to test the hypothesis that a combination of interneuronal firing patterns, plasticity of their synaptic connections, and characteristics of the transmitters they utilize serves to counteract the maladaptive aspects that memory of previous behavior may exert when a new behavior needs to be elicited. Maladaptively persistent forms of memory of previous experiences may underlie such serious behavioral pathologies as the compulsive-obsessive disorders and depression.
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