Biased inter-columnar communication and short-term plasticity in mouse barrel cortex

The barrel cortex (BC) processes input from whiskers to probe and analyze objects in an environment. This sensory input exhibits a complex phase, direction, and frequency-dependent structure arising from whisking kinematics. Little is known about how BC microcircuits process this information. In particular, it remains unclear how the BC extracts relevant spatiotemporal features by integrating input from multiple whiskers. To investigate communication within and between cortical barrels, we targeted a hybrid voltage sensor (hVOS) to Scnn1a excitatory neurons in BC layer 4 (L4) of male and female mice (mean age 7.8 weeks), and imaged population responses to electrical stimulation. Coronal and sagittal slices presented the laminar structure with barrels aligned along stereotyped whisking directions. Voltage imaging tracked activity along an L4→L2/3→L4 relay during inter-barrel communication. AMPA receptor blockade demonstrated that this relay depends on excitatory synaptic transmission and revealed intra- and inter-barrel feedforward inhibition. Single-pulse responses were isotropic in amplitude, conduction velocity, and half-width, but latency was longer for communication with dorsal and caudal barrels. Furthermore, paired-pulse depression was weakest and recovery slowest for protraction-related directions, especially between caudally adjacent barrels, suggesting preferential enhancement of repetitive inputs in this direction. These results identify direction-dependent synaptic circuitry in the shaping of inter-barrel communication. Anisotropy in short-term plasticity aligns with whisker motion kinematics, suggesting that BC microcircuits are tuned to preserve temporal fidelity and selectively filter inputs according to whisking phase and direction.