A cortical code emerges in Layer5a of S1 through temporal integration of thalamic inputs

Abstract

Tactile representations in the barrel field of the primary somatosensory cortex (wS1) receive input from two thalamic nuclei: ventro-posterior-medial (VPM) and posterior-medial complex (POm). However, how these inputs generate distinct cortical representations remains unclear. Previous work revealed a sweep-stick code in rat wS1 using novel velocity-white noise whisker stimulus. Sticks are high-velocity single-whisker bumps; sweeps are large multi-whisker displacements with extended temporal profiles. We hypothesized that cortex neurons inherit 'stick' responses from VPM and 'sweep' responses from first order POm. We tested this by studying coding strategies in both thalamic nuclei and wS1 in mice, determining where the cortical sweep and stick codes originate. We found a stratified wS1 representation of sweep and stick classes, whereas in our recordings VPM and POm mostly contained stick-responding neurons. Layer 4 'stick' responses are delayed versions of VPM responses, and layer 5b 'sweep' responses come from first order POm. Notably, layer 5a 'sweep' responses arise from temporal integration of 'stick' information from VPM and first order POm. Thus, contrary to our initial hypothesis, sweep responses are not inherited from the VPM or first order POm but are constructed within the cortex. In contrast, higher order POm presented only 'sweep' responses inherited from layer 5b of cortex, with a latency similar to that in layer 5a. Our findings reveal a circuit where fast VPM-encoded 'sticks' allow fine-tuned texture processing, complemented by cortically constructed sweep responses that integrate multi-whisker information.