Fast-Spike Interneurons in Visual Cortical Layer 5: Heterogeneous Response Properties Are Related to Thalamocortical Connectivity.

Layer 4 (L4) of rabbit V1 contains fast-spike GABAergic interneurons (suspected inhibitory interneurons, SINs) that receive potent synaptic input from the LGN and generate fast, local feedforward inhibition. These cells display receptive fields with overlapping ON/OFF subregions, nonlinear spatial summation, very broad orientation/directional tuning, and high spontaneous and visually driven firing rates. Fast-spike interneurons are also found in Layer 5 (L5), which receives a much sparser input from the LGN, but the response properties and thalamocortical connectivity of L5 SINs are relatively unstudied. Here, we study L5 SINs in awake rabbits (both sexes) and compare their response properties with previously studied SINs of L4. We also assess thalamocortical connectivity of L5 SINs, examining cross-correlation of retinotopically aligned LGN-SIN spike trains and L5 SIN responses to electrical stimulation of the LGN. These analyses confirmed that many L5 SINs, like L4 SINs, receive a strong, fast monosynaptic drive from the LGN. Moreover, these LGN-connected L5 SINs had response properties similar to those of L4 SINs and were predominantly found in the upper half of L5. In contrast, L5 SINs with longer synaptic latencies to LGN stimulation displayed (1) sharper orientation tuning, (2) longer visual response latencies, (3) lower spontaneous and (4) visually driven firing rates, and (5) were found in the deeper half of L5. We suggest that the long-latency synaptic responses in such L5 SINs reflect a multisynaptic intracortical pathway that generates a different constellation of response properties than seen in L5 SINs that are driven directly by LGN input.