Spinal interneuronal populations encode static hindlimb posture in the cat

Abstract

Proprioceptive signals from primary afferents reflect changes in single-joint angles, whereas neuronal population in the cerebral cortex represent whole-limb postures. Where and how this transformation emerges along the somatosensory axis from peripheral proprioceptive receptors remains unclear. We simultaneously recorded many lumbosacral spinal neurons in two decerebrate, immobilized cats while a robotic device held the hindlimb at 16 static endpoint positions spanning hip-knee configurations. Using high-density multielectrode recordings, we asked how spinal populations encode static limb state. At the single-neuronal level, activities in a majority of neurons covaried with a single joints angle (hip or knee), a smaller subset showed combined modulation by both joints, and a distinct subset ( single-endpoint neurons) fired selectively at one unique hip-knee configuration near the sampled joint-range limits and was quiescent in adjacent postures. Population analyses revealed a low-dimensional structure: the first two principal components tracked knee and hip angles, respectively, whereas a third component isolated a boundary-aligned, posture-specific pattern, with loadings peaking at the same extreme configurations preferred by single-endpoint neurons. Decoders trained on ensemble activity reconstructed both joint angles and the limbs endpoint position in body-centered coordinates, indicating that the recorded spinal-interneuron populations contain sufficient information to reconstruct whole-limb kinematics. Together, these findings are consistent with a hierarchical organization whereby joint-based representations within spinal-interneuron populations could contribute to the emergence of limb-centered representations in the ascending proprioceptive pathways. The boundary preference of single-endpoint neurons supports a possible categorical coding scheme at workspace limits that may provide spinal "landmarks" for switching control modes, enhancing stability near kinematic extremes, and supporting recalibration of proprioceptive population codes. Key PointsO_LIWe simultaneously recorded many lumbar spinal neurons in two decerebrate, immobilized cats while a robot held the hindlimb at 16 static positions to test how spinal populations encode posture. C_LIO_LIMany neurons varied with a single joint angle (hip or knee), a smaller subset showed combined hip-knee modulation, and a distinct subset was active only at one specific endpoint posture. C_LIO_LIPopulation analyses revealed a low-dimensional structure: the first two principal components tracked knee and hip angles, while a third captured a posture-specific pattern aligned with single-endpoint neurons. C_LIO_LIDecoders trained on ensemble activity reconstructed joint angles and the limbs endpoint, indicating that spinal interneuronal populations contain sufficient information for whole-limb kinematics. C_LIO_LIThese findings are consistent with a hierarchical organization whereby joint-based representations within spinal-interneuron populations could contribute to the emergence of limb-centered representations in the ascending proprioceptive pathways. C_LI