S1 Employs Feature-Dependent Differential Selectivity of Single Cells and Distributed Patterns of Populations to Encode Mechanosensations

The primary somatosensory (S1) cortex plays an important role in the perception and discrimination of touch and pain mechanosensations. Conventionally, neurons in the somatosensory system including S1 cortex have been classified into low/high threshold (HT; non-nociceptive/nociceptive) or wide dynamic range (WDR; convergent) neurons by their electrophysiological responses to innocuous brush-stroke and noxious forceps-pinch stimuli. Besides this “noxiousness” (innocuous/noxious) feature, each stimulus also includes other stimulus features: “texture” (brush hairs/forceps-steel arm), “dynamics” (dynamic stroke/static press) and “intensity” (weak/strong). However, it remains unknown how S1 neurons inclusively process such diverse features of brushing and pinch at the single-cell and population levels. Using in vivo two-photon Ca2+ imaging in the layer 2/3 neurons of the mouse S1 cortex, we identified clearly separated response patterns of the S1 neural population with distinct tuning properties of individual cells to texture, dynamics and noxiousness features of cutaneous mechanical stimuli. Among cells other than broadly tuned neurons, the majority of the cells showed a highly selective response to the difference in texture, but low selectivity to the difference in dynamics or noxiousness. Between the two low selectivity features, the difference in dynamics was slightly more specific, yet both could be decoded using the response patterns of neural populations. In addition, more neurons are recruited and stronger Ca2+ responses are evoked as the intensity of forceps-pinch is gradually increased. Our results suggest that S1 neurons encode various features of mechanosensations with feature-dependent differential selectivity of single cells and distributed response patterns of populations. Moreover, we raise a caution about describing neurons by a single stimulus feature ignoring other aspects of the sensory stimuli.