Experience-Dependent Intrinsic Plasticity in Layer IV of Barrel Cortex at Whisking Onset.

The development of motor control over sensory organs is a critical milestone, enabling active exploration and shaping of the sensory environment. Whether the onset of sensory organ motor control directly influences the development of corresponding sensory cortices remains unknown. Here, we confirm and exploit the late onset of whisking behavior in mice to address this question in the somatosensory system. Using ex vivo electrophysiology, we describe a transient increase in the intrinsic excitability of excitatory neurons in layer IV of the barrel cortex, which processes whisker input, immediately following the onset of active whisking on postnatal days 13 and 14. This increase in neuronal gain is specific to layer IV, independent of changes in synaptic strength, and requires prior sensory experience. Further, these effects are not expressed in inhibitory interneurons in barrel cortex. The transient increase in excitability is not evident in layer II/III of barrel cortex or in the visual cortex upon eye opening, suggesting a unique interaction between the development of active sensing and the thalamocortical input layer in the somatosensory iso-cortex. Predictive modeling indicates that, immediately following the onset of active whisking, changes in active membrane conductances alone can reliably distinguish neurons in control but not whisker-deprived hemispheres. Our findings demonstrate an experience-dependent, lamina-specific refinement of neuronal excitability tightly linked to the emergence of active whisking. This transient increase in the gain of the thalamic input layer coincides with a critical period for synaptic plasticity in downstream layers, suggesting a role in cortical maturation and sensory processing. Significance statement Motor control over sensory organs shapes how we explore and perceive our environment. Whether the developmental onset of motor control directly influences the maturation of corresponding sensory brain regions remains poorly understood. Using the mouse whisker-barrel system as a model, we demonstrate that the emergence of active whisking behavior triggers a transient, experience-dependent increase in neuronal excitability in layer IV of barrel cortex—the primary input layer for whisker information. This intrinsic plasticity occurs without accompanying synaptic changes and is absent in other cortical layers and sensory systems. Our findings reveal a novel mechanism by which motor development cooperates with sensory cortical maturation, suggesting that the timing of motor milestones may be critical for brain development and sensory processing capabilities.