Abstract
Animal locomotion requires spatiotemporally coordinated contraction of muscles throughout the body. Here, we investigate how contractions of antagonistic groups of muscles are intersegmentally coordinated during bidirectional crawling of Drosophila larvae. We identify two pairs of higher-order premotor excitatory interneurons present in each abdominal neuromere that intersegmentally provide feedback to the adjacent neuromere during motor propagation. The two feedback neuron pairs are differentially active during either forward or backward locomotion but commonly target a group of premotor interneurons that together provide excitatory inputs to transverse muscles and inhibitory inputs to the antagonistic longitudinal muscles. Inhibition of either feedback neuron pair compromises contraction of transverse muscles in a direction-specific manner. Our results suggest that the intersegmental feedback neurons coordinate contraction of synergistic muscles by acting as delay circuits representing the phase lag between segments. The identified circuit architecture also shows how bidirectional motor networks could be economically embedded in the nervous system.
Highlights
Animal locomotion requires spatiotemporally coordinated contraction of muscles throughout the body
By linking sub-circuits regulating intersegmental activity propagation and synergistic muscle control in a direction-specific manner, these neurons realize intersegmentally coordinated activation of synergistic muscles. They share a group of premotor interneurons as their postsynaptic partners, which in turn connect with groups of antagonistic muscles in a cooperative manner, demonstrating how neural networks coordinating a bidirectional flow of neural activity could coexist in the central nervous system (CNS)
We used reconstructions from a serial section transmission electron microscopy image data set of an entire first instar larval CNS29,30 to investigate the upstream circuits of PMSIs
Summary
Animal locomotion requires spatiotemporally coordinated contraction of muscles throughout the body. Little is known about the mechanism of how bidirectional sub-circuits generate flows of neural activity that recruit similar groups of muscles in opposite directions Dedicated subnetworks including both interneurons and motor neurons (MNs) are known to actuate forward and backward locomotion in the unsegmented Caenorhabditis elegans[13]. By linking sub-circuits regulating intersegmental activity propagation and synergistic muscle control in a direction-specific manner, these neurons realize intersegmentally coordinated activation of synergistic muscles They share a group of premotor interneurons as their postsynaptic partners, which in turn connect with groups of antagonistic muscles in a cooperative manner, demonstrating how neural networks coordinating a bidirectional flow of neural activity could coexist in the CNS
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