Functional consequences of neuronal divergence within the retinogeniculate pathway.

The neuronal connections from the retina to the dorsal lateral geniculate nucleus (dLGN) are characterized by a high specificity. Each retinal ganglion cell diverges to connect to a small group of geniculate cells and each geniculate cell receives input from a small number of retinal ganglion cells. Consistent with the high specificity of the connections, geniculate cells sharing input from the same retinal afferent are thought to have very similar receptive fields. However, the magnitude of the receptive-field mismatches, which has not been systematically measured across the different cell types in dLGN, seems to be in contradiction with the functional anatomy of the Y visual pathway: Y retinal afferents in the cat diverge into two geniculate layers (A and C) that have Y geniculate cells (Y(A) and Y(C)) with different receptive-field sizes, response latencies, nonlinearity of spatial summation, and contrast sensitivity. To better understand the functional consequences of retinogeniculate divergence, we recorded from pairs of geniculate cells that shared input from a common retinal afferent across layers and within the same layer in dLGN. We found that nearly all cell pairs that shared retinal input across layers had Y-type receptive fields of the same sign (i.e., both on-center) that overlapped by >70%, but frequently differed in size and response latency. The receptive-field mismatches were relatively small in value (receptive-field size ratio <5; difference in peak response <5 ms), but were robustly correlated with the strength of the synchronous firing generated by the shared retinal connections (R(2) = 0.75). On average, the percentage of geniculate spikes that could be attributed to shared retinal inputs was about 10% for all cell-pair combinations studied. These results are used to provide new estimates of retinogeniculate divergence for different cell classes.