To achieve smooth motor performance in a changing sensory environment, motor outputs must be constantly updated in response to sensory feedback. Inhibitory interneurons in the spinal cord play an essential role in shaping motor activity by gating the transmission of sensory information and setting the pattern and rhythm of motor neurons. Here, in mice, we identify the medial deep dorsal horn of the spinal cord as a “hot zone” of convergent proprioceptive and cutaneous information from the hindlimb, where inhibitory neurons show increased responsiveness to sensory input and are more prominently recruited during locomotion in comparison to excitatory neurons. We identify a novel population of glycinergic inhibitory neurons within the deep dorsal horn that express parvalbumin (dPV) and receive convergent proprioceptive and cutaneous input from the paw. We show that dPVs possess intrinsic properties that support spontaneous discharge, even in the absence of synaptic input. However, a drug cocktail mimicking descending input (5-HT, dopamine, NMDA) amplifies dPV output, while cutaneous and proprioceptive inputs shape the temporal dynamics of dPV activity. These findings suggest dPV-mediated inhibition is modulated by behavioral state and can be fine-tuned by sensory input. Using intersectional genetic strategies, we selectively target spinal cord dPVs and demonstrate their capacity to provide widespread ipsilateral inhibition to both pre-motor and motor networks of the ventral horn, thereby gating sensory-evoked muscle activity. Manipulating the activity of dPVs during treadmill locomotion results in altered limb kinematics at the transition of stance to swing and altered step cycle timing at increased speeds. To investigate the effects of manipulating dPV activity on broader sets of motor behaviors, we used depth vision and machine learning to quantify and scale spontaneous behavior. We find that although sub-movements remain stable, the transitions between sub-movements are reduced, suggesting a role in movement switching. In sum, our study reveals a new model by which sensory convergence and inhibitory divergence produce a surprisingly flexible influence on motor networks to increase the diversity of mechanisms by which sensory input facilitates smooth movement and context-appropriate transitions.
