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Multimodal sensory control of motor performance by glycinergic interneurons of the mouse spinal cord deep dorsal horn

Gradwell, MA;Ozeri-Engelhard, N;Eisdorfer, JT;Laflamme, OD;Gonzalez, M;Upadhyay, A;Medlock, L;Shrier, T;Patel, KR;Aoki, A;Gandhi, M;Abbas-Zadeh, G;Oputa, O;Thackray, JK;Ricci, M;George, A;Yusuf, N;Keating, J;Imtiaz, Z;Alomary, SA;Bohic, M;Haas, M;Hernandez, Y;Prescott, SA;Akay, T;Abraira, VE;

Sensory feedback is integral for contextually appropriate motor output, yet the neural circuits responsible remain elusive. Here, we pinpoint the medial deep dorsal horn of the mouse spinal cord as a convergence point for proprioceptive and cutaneous input. Within this region, we identify a population of tonically active glycinergic inhibitory neurons expressing parvalbumin. Using anatomy and electrophysiology, we demonstrate that deep dorsal horn parvalbumin-expressing interneuron (dPV) activity is shaped by convergent proprioceptive, cutaneous, and descending input. Selectively targeting spinal dPVs, we reveal their widespread ipsilateral inhibition onto pre-motor and motor networks and demonstrate their role in gating sensory-evoked muscle activity using electromyography (EMG) recordings. dPV ablation altered limb kinematics and step-cycle timing during treadmill locomotion and reduced the transitions between sub-movements during spontaneous behavior. These findings reveal a circuit basis by which sensory convergence onto dorsal horn inhibitory neurons modulates motor output to facilitate smooth movement and context-appropriate transitions.