Hierarchical behavior control by a single class of interneurons

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 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 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. Significance StatementIn this study, we reveal the dual role of SAA interneurons in C. elegans, demonstrating their influence over diverse behavior timescales. These neurons not only stabilize short-term rhythmic activities during forward movements, but also modulate long-term behavioral transitions between motor states. This indicates the essential role of feedback from low-level neural assemblies to command centers in a hierarchical neural architecture, emphasizing its significance in orchestrating behavior across scales. Our study offers critical insights into the intricate neural interactions behind organized and adaptive behavior.