Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern

Abstract

Modulatory interneurons that can drive central pattern generators (CPGs) are considered as good candidates for decision-making roles in rhythmic behaviors. Although the mechanisms by which such neurons activate their target CPGs are known in detail in many systems, their role in the sensory activation of CPG-driven behaviors is poorly understood. In the feeding system of the mollusc Lymnaea, one of the best-studied rhythmical networks, intracellular stimulation of either of two types of neuron, the cerebral ventral 1a (CV1a) and the slow oscillator (SO) cells, leads to robust CPG-driven fictive feeding patterns, suggesting that they might make an important contribution to natural food-activated behavior. In this paper we investigated this contribution using a lip-CNS preparation in which feeding was elicited with a natural chemostimulant rather than intracellular stimulation. We found that despite their CPG-driving capabilities, neither CV1a nor SO were involved in the initial activation of sucrose-evoked fictive feeding, whereas a CPG interneuron, N1M, was active first in almost all preparations. Instead, the two interneurons play important and distinct roles in determining the characteristics of the rhythmic motor output; CV1a by modulating motoneuron burst duration and SO by setting the frequency of the ongoing rhythm. This is an example of a distributed system in which (1) interneurons that drive similar motor patterns when activated artificially contribute differently to the shaping of the motor output when it is evoked by the relevant sensory input, and (2) a CPG rather than a modulatory interneuron type plays the most critical role in initiation of sensory-evoked rhythmic activity.