The motor function of the spinal cord requires the computation of the local neuronal circuits within the same segments as well as the long-range coordination of different spinal levels. Implicated players in this process are the propriospinal neurons (PPNs) that project their axons across different levels of the spinal cord. However, their cellular, molecular, and functional properties remain unknown. Here we use a recombinant rabies virus-based method to label a specific type of long-projecting premotor PPNs in the mouse upper spinal cord that are monosynaptically connected to the motor neurons in the lumbar spinal cord. With a whole spinal cord imaging method, we find that these neurons are distributed along the entire length of the upper spinal cord with more in the lower thoracic levels. Among them, a subset of thoracic PPNs receive substantial numbers of sensory inputs, suggesting a function in coordinating the activity of trunk and hindlimb muscles. Although many PPNs in the cervical and thoracic spinal cord receive the synaptic inputs from corticospinal tract or serotonergic axons, limited bouton numbers suggested that these supraspinal inputs might not be major regulators of the PPNs in intact animals. Molecularly, these PPNs appear to be distinct from other known premotor interneurons, but some are derived from Chx10+ lineages. This study provides an anatomical basis for further exploring different functions of PPNs.
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