Functional mapping of neurons that control locomotory behavior in <i>Caenorhabditis elegans</i>

TLDR

In Caenorhabditis elegans, neuronal circuits have been mapped by synaptic connectivity, but the role of interneurons in locomotion remains largely unexplored. The study aims to identify and map interneuron classes (AIY, AIZ, RIB) that modulate locomotion in C. elegans, establishing a framework for future circuit analyses. The authors used mutant analysis and microsurgical mapping to show that AIY neurons tonically suppress a bistable command interneuron switch, thereby modulating reversal frequency. The study demonstrates that AIY neurons suppress a bistable command switch to control reversal frequency, that sensory modalities alter reversal behavior via AIY, and that AIZ and RIB also process odor information, making AIY, AIZ, and RIB the first interneurons linked to chemosensory signaling.

Abstract

Abstract One approach to understanding behavior is to define the cellular components of neuronal circuits that control behavior. In the nematode Caenorhabditis elegans , neuronal circuits have been delineated based on patterns of synaptic connectivity derived from ultrastructural analysis. Individual cellular components of these anatomically defined circuits have previously been characterized on the sensory and motor neuron levels. In contrast, interneuron function has only been addressed to a limited extent. We describe here several classes of interneurons (AIY, AIZ, and RIB) that modulate locomotory behavior in C. elegans . Using mutant analysis as well as microsurgical mapping techniques, we found that the AIY neuron class serves to tonically modulate reversal frequency of animals in various sensory environments via the repression of the activity of a bistable switch composed of defined command interneurons. Furthermore, we show that the presentation of defined sensory modalities induces specific alterations in reversal behavior and that the AIY interneuron class mediates this alteration in locomotory behavior. We also found that the AIZ and RIB interneuron classes process odorsensory information in parallel to the AIY interneuron class. AIY, AIZ, and RIB are the first interneurons directly implicated in chemosensory signaling. Our neuronal mapping studies provide the framework for further genetic and functional dissections of neuronal circuits in C. elegans . © 2003 Wiley Periodicals, Inc. J Neurobiol 56: 178–197, 2003