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In the classic model of the primary visual cortex, upper-layer complex cells are driven by feedforward inputs from layer 4 simple cells. Based on spike cross-correlation, previous in vivo work has suggested that this connection is strong and dense, with a high probability of connection (50%) and significant strength in connected pairs. A much sparser projection has been found in brain slices, however, with the probability of layer 4 cells connecting to layer 2/3 cells being relatively low (10%). Here, we explore this connection in vivo in the cat primary visual cortex by recording simultaneously spikes of layer 4 simple cells and the membrane potential (V(m)) of layer 2/3 complex cells. By triggering the average of the complex cell's V(m) on the spikes of the simple cell (V(m)-STA), we found functional coupling to be very common during visual stimulation: the simple cell's spikes tended to occur near the troughs of the complex cell's V(m) fluctuations and were, on average, followed by a significant (~1 mV) fast-rising (10 ms) depolarization in the complex cell. In the absence of visual stimulation, however, when single simple cells were activated electrically through the recording electrode, no significant depolarization, or at most a very weak input (0.1-0.2 mV), was detected in the complex cell. We suggest that the functional coupling observed during visual stimulation arises from coordinated or nearly synchronous activity among a large population of simple cells, only a small fraction of which are presynaptic to the recorded complex cell.

Functional Coupling from Simple to Complex Cells in the Visually Driven Cortical Circuit