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

Each barrel of the barrel cortex (BC) receives thalamic input primarily from a single whisker. Barrels then communicate through intracortical circuitry to integrate input from multiple whiskers and perform processing functions such as spatial filtering, motion sensing, and object localization. To investigate the circuits that enable barrels to communicate independently of extracortical and inter-areal influences we prepared slices of somatosensory cortex from mice of both sexes with a hybrid voltage sensor (hVOS) targeted to Scnn1a excitatory neurons in cortical layer 4 (L4). We then imaged voltage responses of this population of neurons to electrical stimulation. Imaging tracked activity initiated in L4 of one barrel spreading into layer 2/3 (L2/3) and then to L4 of neighboring barrels. AMPA receptor blockade eliminated this spread, suggesting that L4 signaling to neighboring barrels employs an L4→L2/3→L4 excitatory synaptic relay. Blocking AMPA receptors also enhanced some responses, revealing intra- and inter-barrel feedforward inhibition. Both coronal and sagittal slices presented the layout of barrels, which aligned with facial whisker organization. We assessed inter-barrel communication in different directions and found it to be isotropic in response amplitude, half-width, and conduction velocity. However, latency was longest for communication to caudal barrels. Furthermore, paired-pulse depression was strongest and recovery slowest for inter-barrel communication related to exploratory protraction. Such biases have the potential to contribute to direction-sensitive processing. Anisotropy in short-term plasticity can tune BC microcircuits to preserve temporal fidelity and filter selectively according to direction.Significance Statement Sensory processing of spatiotemporal whisking patterns by the barrel cortex depends on complex interactions within the cortex and with extracortical areas. How intracortical circuits contribute to this processing is not well understood. Cell-type-specific voltage imaging in anatomically aligned slices of somatosensory cortex enabled the investigation of how barrels communicate. We identified a layer-specific synaptic circuit that mediates communication between barrels. Response latency and short-term synaptic depression of this inter-barrel relay vary with propagation direction. This direction dependence suggests that intracortical communication is tailored to the processing of natural whisker motion. By linking synaptic properties and circuit connectivity between barrels to anatomically aligned whisker architecture, this work advances our understanding of how neocortical networks process sensory input.