Spatiotemporal properties of sensory integration in the mouse barrel cortex

While rodents explore their environment they actively contact surrounding objects with their array of whiskers, resulting in a complex pattern of multiwhisker deflections. Despite this complexity, the whisker system is able to extract relevant information from the spatiotemporal sequence of deflections to generate touch-dependent behavior. The question that arises is: How is global multiwhisker information encoded? Whiskers are mapped onto layer 4 of the primary somatosensory cortex (S1) as discrete units named “barrels”. Each barrel-related vertical column processes information coming primarily from its corresponding principal whisker (PW). Previous experiments in our lab done with extracellular recordings have revealed that neurons in the rat S1 and thalamus not only show a preferred direction for the local deflection of the PW but also for the direction of a global motion across the whisker pad. To further understand how the cortical network processes global tactile scenes, we built a set-up that enables to perform voltage sensitive dye imaging of the mouse barrel cortex while applying precise tactile stimuli using a 24-multi-whisker stimulator. We further developed a technical method to map the recorded functional data onto the cortical structure. We first studied whether local direction selectivity is spatially distributed within the barrel-related column. Responses to different directions were slightly segregated on space close to the barrel center, but the distribution differed from the one previously described in rat S1, namely a pinwheel-like structure. We then showed that global direction selectivity is spatially organized in the barrel cortex. Columns related to rostral whiskers were more selective to the global direction than columns related to caudal whiskers. Moreover, the columns related to dorsal whiskers preferred ventral global directions, while the columns related to ventral whiskers preferred caudal global directions. Overall the responses to the caudo-ventral global directions were the strongest in average for all the columns. We showed that the spatial distribution of the global direction selectivity can be explained neither by the high salience of the starting position of the deflections on the whiskerpad (a border effect), nor by the linear summation of the responses to deflections of several whiskers. Responses to the global motion of the whisker array are indeed highly sublinear independently of the direction of stimulation. In conclusion, we show here that stepping aside from the classical view of the whisker-to-barrel cortex system allows a better understanding of how different features of complex stimuli are processed and how the emergent properties of the cortex, like the global direction selectivity, are built-up.