Functional dynamics and selectivity of two parallel corticocortical pathways from motor cortex to layer 5 circuits in somatosensory cortex.

Long-range corticocortical pathways mediate direct interactions between the primary motor cortex (M1) and the somatosensory cortex (S1) and are likely critical for context-dependent sensory processing and sensorimotor integration. In the rodent whisker system, projections from M1 to S1 may be necessary for interpreting touch signals in the context of ongoing movement to drive behavior. However, understanding the function of these interareal interactions requires knowledge about the physiological properties of the synapses themselves and how specific classes of neurons integrate those signals. Here, we combined optogenetics and retrograde labeling with in vitro electrophysiology to characterize the synaptic properties of the connections between M1 and layer 5 (L5) intratelencephalic (IT) and pyramidal tract (PT) neurons in S1 of the mouse (both sexes) and how these two classes of neurons integrate those inputs. We found that M1 excitatory inputs to L5 IT cells depressed but had slow time courses that resulted in summation at the soma, whereas inputs to L5 PT cells facilitated and had faster time courses, resulting in less temporal summation at the soma. Differences in hyperpolarization-activated current (Ih) could partially explain the differences in subthreshold synaptic responses between L5 neurons. Functionally, we found that high-frequency M1 activity coupled more effectively with backpropagating action potentials within a narrow time window in PT neurons to trigger bursts at the soma. Our findings highlight the synaptic and cellular dynamics of two parallel pathways underlying the interactions between M1 and specific L5 circuits in S1.