TRANSFORMATION OF HINDLIMB PROPRIOCEPTION ALONG THE EARLY SOMATOSENSORY PATHWAY

Proprioception, first described by Sherrington, refers to the sense of limb position and movement conveyed by sensory inputs from muscles, joints, and tendons. While detailed representations of limb kinematics are often attributed to cortical processing, increasing evidence indicates that substantial proprioceptive transformation occurs at earlier stages of the somatosensory pathway. In particular, the dorsal column nuclei (DCN) are emerging as an active processing hub rather than a simple relay. A central unresolved question is how and where higher-order proprioceptive features—such as movement direction and coordinated population codes—begin to arise. Whether these features are generated de novo in cortex or gradually assembled within subcortical circuits remains unclear. Here, we investigate the transformation of hindlimb proprioceptive signals along the ascending somatosensory pathway, with a primary focus on the DCN. Using in vivo two-photon calcium imaging in mice, we perform terminal recordings in the dorsal root ganglia (DRG) and DCN during precisely controlled limb movements, and chronic imaging in primary somatosensory cortex (S1) for comparison. At the level of the DRG, neuronal activity predominantly reflects muscle length–related signals, consistent with peripheral encoding. In contrast, DCN populations exhibit increasingly structured response patterns, including gradual emergence of direction-selective tuning and context-dependent modulation. These results suggest that proprioceptive representations are progressively transformed along the neuraxis, with the DCN acting as a critical intermediate stage where higher-order kinematic features begin to emerge before cortical integration. Together, this work highlights proprioception as a distributed, hierarchical computation spanning peripheral, subcortical, and cortical levels.