Random wiring in the midget pathway of primate retina

The present study addresses the questions of how topographically organized neuronal populations are connected, and whether there is anatomical evidence for color-selective wiring in retinal pathways for red-green color vision. The connectivity of OFF midget bipolar and OFF midget ganglion cells was studied in the peripheral retina of dichromatic ("red-green color blind") and trichromatic ("color normal") marmosets (Callithrix jacchus). Midget bipolar cells were identified immunohistochemically. Midget ganglion cells were retrogradely labeled from the lateral geniculate nucleus and photofilled. Comparable results were obtained from all retinas studied. Between 3 and 16 bipolar terminals converge onto each ganglion cell. Nearly all bipolar terminals investigated show regions of colocalization (areas of presumed synaptic contacts) with ganglion cell dendrites. This contact area makes up approximately 14% of the axon surface area for a typical midget bipolar cell. The output from individual midget bipolar axons is often shared between midget ganglion cells so that, on average, <70% of the axon terminal area of a midget bipolar cell shows overlap with the dendritic field of a given midget ganglion cell. We conclude that there is no morphological evidence of red-green color selectivity in the connections between midget bipolar and midget ganglion cell mosaics. Furthermore, the results suggest that convergence is based on local interactions between axons and dendrites rather than cell-by-cell recognition between members of each mosaic.