Intraspinal Sensory Neurons Provide Powerful Inhibition to Motor Circuits Ensuring Postural Control during Locomotion

In the vertebrate spinal cord, cerebrospinal fluid-contacting neurons (CSF-cNs) are GABAergic neurons whose functions are only beginning to unfold. Recent evidence indicates that CSF-cNs detect local spinal bending and relay this mechanosensory feedback information to motor circuits, yet many CSF-cN targets remain unknown. Using optogenetics, patterned illumination, and in vivo electrophysiology, we show here that CSF-cNs provide somatic inhibition to fast motor neurons and excitatory sensory interneurons involved in the escape circuit. Ventral CSF-cNs respond to longitudinal spinal contractions and induce large inhibitory postsynaptic currents (IPSCs) sufficient to silence spiking of their targets. Upon repetitive stimulation, these IPSCs promptly depress, enabling the mechanosensory response to the first bend to be the most effective. When CSF-cNs are silenced, postural control is compromised, resulting in rollovers during escapes. Altogether, our data demonstrate how GABAergic sensory neurons provide powerful inhibitory feedback to the escape circuit to maintain balance during active locomotion. •CSF-contacting neurons are recruited during spontaneous tail muscle contractions•CSF-contacting neurons project onto motor neurons and sensory interneurons of the escape circuit•GABAergic synapses on these targets are large and depress with repetitive stimuli•Silencing CSF-contacting neurons alters balance during fast locomotion Hubbard et al. demonstrate here that GABAergic sensory neurons, referred to as cerebrospinal fluid-contacting neurons, locally project onto the escape circuit within the spinal cord to control posture during active locomotion in the zebrafish larva.