Layer-Specific Refinement of Sensory Coding in Developing Mouse Barrel Cortex

Rodent rhythmic whisking behavior matures during a critical period around 2 weeks after birth. The functional adaptations of neocortical circuitry during this developmental period remain poorly understood. Here, we characterized stimulus-evoked neuronal activity across all layers of mouse barrel cortex before, during, and after the onset of whisking behavior. Employing multi-electrode recordings and 2-photon calcium imaging in anesthetized mice, we tested responses to rostro-caudal whisker deflections, axial "tapping" stimuli, and their combination from postnatal day 10 (P10) to P28. Within this period, whisker-evoked activity of neurons displayed a general decrease in layer 2/3 (L2/3) and L4, but increased in L5 and L6. Distinct alterations in neuronal response adaptation during the 2-s period of stimulation at ~5 Hz accompanied these changes. Moreover, single-unit analysis revealed that response selectivity in favor of either lateral deflection or axial tapping emerges in deeper layers within the critical period around P14. For superficial layers we confirmed this finding using calcium imaging of L2/3 neurons, which also exhibited emergence of response selectivity as well as progressive sparsification and decorrelation of evoked responses around P14. Our results demonstrate layer-specific development of sensory responsiveness and response selectivity in mouse somatosensory cortex coinciding with the onset of exploratory behavior.