Fast-spike interneurons in visual cortical layer 5: Heterogeneous response properties are related to thalamocortical connectivity

Layer 4 of rabbit V1 contains fast-spiking GABAergic interneurons (suspected inhibitory interneurons, SINs) that receive potent synaptic input from the LGN and generate fast, local feed-forward inhibition. These cells display receptive fields with overlapping ON/OFF subregions, non-linear spatial summation, very broad orientation/directional tuning, and high spontaneous and visually-driven firing rates. Such 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 both 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 and fast monosynaptic drive from the LGN. Moreover, these LGN-connected L5 SINs had response properties that were similar to those of L4 SINs and were predominantly found in the upper half of L5. By 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 reflects a multi-synaptic intracortical pathway that generates a different constellation of response properties than seen in L5 SINs that are driven directly by LGN input. Significance Statement Fast-spike GABAergic interneurons are found across the entire depth of the visual cortex but may have very different response properties and functions in each cortical layer depending on a host of factors that are specific to the different layers. In layer 4, they are known to receive potent synaptic input from the thalamus and generate fast, local feed-forward inhibition. In layer 5, they are thought to receive less direct thalamic input and be strongly dominated by intracortical input. Here, we show that some layer-5 interneurons receive powerful monosynaptic input from LGN and have visual response properties more similar to layer 4 interneurons than those receiving little direct LGN input.