RRC ID 84123
Author Huo J, Xu T, Liu Q, Polat M, Kumar S, Zhang X, Leifer AM, Wen Q.
Title Hierarchical behavior control by a single class of interneurons.
Journal Proc Natl Acad Sci U S A
Abstract Animal behavior is organized into nested temporal patterns that span multiple timescales. This behavior hierarchy is believed to arise from a hierarchical neural architecture: Neurons near the top of the hierarchy are involved in planning, selecting, initiating, and maintaining motor programs, whereas those near the bottom of the hierarchy act in concert to produce fine spatiotemporal motor activity. In Caenorhabditis elegans, behavior on a long timescale emerges from ordered and flexible transitions between different behavioral states, such as forward, reversal, and turn. On a short timescale, different parts of the animal body coordinate fast rhythmic bending sequences to produce directional movements. Here, we show that Sublateral Anterior A (SAA), a class of interneurons that enable cross-communication between dorsal and ventral head motor neurons, play a dual role in shaping behavioral dynamics on different timescales. On a short timescale, SAA regulate and stabilize rhythmic bending activity during forward movements. On a long timescale, the same neurons suppress spontaneous reversals and facilitate reversal termination by inhibiting Ring Interneuron M (RIM), an integrating neuron that helps maintain a behavioral state. These results suggest that feedback from a lower-level cell assembly to a higher-level command center is essential for bridging behavioral dynamics at different levels.
Volume 121(47)
Pages e2410789121
Published 2024-11-19
DOI 10.1073/pnas.2410789121
PMID 39531495
PMC PMC11588054
MeSH Animals Behavior, Animal* / physiology Caenorhabditis elegans* / physiology Caenorhabditis elegans Proteins / genetics Caenorhabditis elegans Proteins / metabolism Interneurons* / physiology Motor Neurons / physiology
Resource
C.elegans tm3268 tm3219 tm3174