A Non-canonical Feedback Circuit for Rapid Interactions between Somatosensory Cortices

Sensory perception depends on interactions among cortical areas. These interactions are mediated by canonical patterns of connectivity in which higher areas send feedback projections to lower areas via neurons in superficial and deep layers. Here, we probed the circuit basis of interactions among two areas critical for touch perception in mice, whisker primary (wS1) and secondary (wS2) somatosensory cortices. Neurons in layer 4 of wS2 (S2_L4) formed a major feedback pathway to wS1. Feedback from wS2 to wS1 was organized somatotopically. Spikes evoked by whisker deflections occurred nearly as rapidly in wS2 as in wS1, including among putative S2_L4 → S1 feedback neurons. Axons from S2_L4 → S1 neurons sent stimulus orientation-specific activity to wS1. Optogenetic excitation of S2_L4 neurons modulated activity across both wS2 and wS1, while inhibition of S2_L4 reduced orientation tuning among wS1 neurons. Thus, a non-canonical feedback circuit, originating in layer 4 of S2, rapidly modulates early tactile processing.