A command-like descending neuron that coordinately activates backward and inhibits forward locomotion

Abstract

Command-like descending neurons can induce many behaviors, such as backward locomotion, escape, feeding, courtship, egg-laying, or grooming. In most animals it remains unknown how neural circuits switch between these antagonistic behaviors: via top-down activation/inhibition of antagonistic circuits or via reciprocal inhibition between antagonistic circuits. Here we use genetic screens, intersectional genetics, circuit reconstruction by electron microscopy, and functional optogenetics to identify a bilateral pair of larval \"mooncrawler descending neurons\" (MDNs) with command-like ability to coordinately induce backward locomotion and block forward locomotion; the former by activating a backward-specific premotor neuron, and the latter by disynaptic inhibition of a forward-specific premotor neuron. In contrast, direct reciprocal inhibition between forward and backward circuits was not observed. Thus, MDNs coordinate a transition between antagonistic larval locomotor behaviors. Interestingly, larval MDNs persist into adulthood, where they can trigger backward walking. Thus, MDNs induce backward locomotion in both limbless and limbed animals.\n\nHighlightsO_LIMDN command-like descending neuron induces backward larval locomotion\nC_LIO_LIMDN neurons coordinately regulate antagonistic behaviors (forward/backward locomotion)\nC_LIO_LIMDN-motor circuit validated at structural (TEM) and functional (optogenetic) levels\nC_LIO_LIMDN neurons induce backward locomotion in both limbless larva and limbed adult\nC_LI