Hierarchical neuronal processing in primary somatosensory cortex during action observation

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Abstract

Voluntary movement requires the central nervous system to transform and integrate visual and somatosensory information into coordinated motor outputs. Although mirror-like neuronal activity during both action execution and observation has been extensively described in premotor, motor, and parietal cortices, it remains unknown whether the primary somatosensory cortex (S1) also participates in the action observation network. Here, we recorded single-unit activity from cytoarchitectonically defined areas 3a, 3b, 1, and 2 in macaque S1 while monkeys either executed or observed grasping movements. Approximately one-third of neurons across S1 modulated their firing during action observation, with the proportion of responsive neurons increasing from area 3 to areas 1 and 2, consistent with the hierarchical organization of somatosensory processing. Most action observation neurons showed congruent activity during action execution and observation, suggesting that these responses may reflect top-down motor-related or integrated visuomotor signals and are unlikely to be explained by visual input alone. The higher prevalence of action observation neurons in areas 1 and 2 suggests that action observation-related signals preferentially influence later stages of somatosensory processing, potentially via cortico-cortical interactions with motor and parietal regions.

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