Neural Mechanisms of Motor Program Switching inAplysia

Abstract

The Aplysia multifunctional feeding central pattern generator (CPG) produces at least two types of motor programs, ingestion and egestion, that involve two sets of radula movements, protraction–retraction and opening–closing movements. In ingestion, the radula closes during retraction to pull food in, whereas in egestion, the radula closes during protraction to push inedible objects out. Thus, radula closure shifts the phase in which it occurs with respect to protraction–retraction in the two programs. To identify the central switching mechanisms, we compared activity of CPG neurons during the two types of motor programs elicited by a higher-order interneuron, cerebral–buccal interneuron-2 (CBI-2). Although CPG elements (B63, B34, and B64) that mediate the protraction–retraction sequence are active in both programs, two other CPG elements, B20 and B4/5, are preferentially active in egestive programs and play a major role in mediating CBI-2-elicited egestive programs. Both B20 and B4/5 control the phasing of radula closure motoneurons (B8 and B16) to ensure that, in egestive programs, these motoneurons fire and produce radula-closing movements only during protraction. Elsewhere, another higher-order interneuron, CBI-3, was shown to convert CBI-2-elicited egestion to ingestion. We show that CBI-3 switches the programs by suppressing the activity of B20 and B4/5. CBI-3, active only during protraction, accomplishes this through fast inhibition of B20 during protraction and slow inhibition of B4/5 during retraction. The slow inhibition is mimicked and occluded by APGWamide, a neuropeptide contained in CBI-3. Thus, fast conventional and slow peptidergic transmissions originating from the same interneuron act in concert to meet specific temporal requirements in pattern switching.