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The cerebrospinal fluid (CSF) constitutes an interface through which chemicalcues can reach and modulate the activity of neurons located at the epithelialboundary within the entire nervous system. Here, we investigate the role andfunctional connectivity of a class of GABAergic sensory neurons contacting theCSF in the vertebrate spinal cord and referred to as CSF-cNs. The remoteactivation of CSF-cNs was shown to trigger delayed slow locomotion in thezebrafish larva, suggesting that these cells modulate components of locomotorcentral pattern generators (CPGs). Combining anatomy, electrophysiology, andoptogenetics in vivo, we show that CSF-cNs form active GABAergic synapses ontoV0-v glutamatergic interneurons, an essential component of locomotor CPGs. Weconfirmed that activating CSF-cNs at rest induced delayed slow locomotion inthe fictive preparation. In contrast, the activation of CSF-cNs promptlyinhibited ongoing slow locomotion. Moreover, selective activation of rostralCSF-cNs during ongoing activity disrupted rostrocaudal propagation ofdescending excitation along the spinal cord, indicating that CSF-cNs primarilyact at the premotor level. Altogether, our results demonstrate how a spinalGABAergic sensory neuron can tune the excitability of locomotor CPGs in astate-dependent manner by projecting onto essential components of theexcitatory premotor pool.

State-Dependent Modulation of Locomotion by GABAergic Spinal Sensory Neurons