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

Summary Tactile representations in the barrel field of the primary somatosensory cortex of rodents (wS1) receive inputs from two distinct thalamic nuclei, the ventro-posterior-medial nucleus (VPM) and the posterior medial complex (POm). Previous work has revealed a sweep-stick code in rat wS1 by using a novel whisker velocity-white noise stimulus. Sticks refer to high velocity single whisker bumps, while sweeps correspond to large multiwhisker displacements with extended temporal profiles. We hypothesized that barrel cortex neurons inherit ‘stick’ responses from the VPM and ‘sweep’ responses from the POm. Here we test this hypothesis by studying the coding strategy of both thalamic nuclei and wS1 in mice. We found a stratified wS1 representation of both sweep and stick functional classes, whereas VPM and POm contained mainly stick encoding neurons. Cortical layer 4 ‘stick’ responses are a delayed version from VPM, while layer 5b ‘sweep’ responses come from POm. Notably, layer 5a ‘sweep’ responses result from a temporal integration of ‘stick’ information from VPM and POm. Our results put forward a circuit scheme in which fast encoding stick events from VPM allow a fine-tuned texture processing in the cortex, modulated by sweep-responding cells that integrate multi-whisker information.