Parallel Circuits from Cones to the On-Beta Ganglion Cell

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Abstract
Neural integration depends critically upon circuit architecture; yet the architecture has never been established quantitatively (numbers of cells and synapses) for any vertebrate local circuit. Here we describe circuits in the cat retina that connect cones to the on-beta ganglion cell. This cell type is important because on- and off-beta cells contribute about 50% of the optic nerve fibres and the major retinal input to the striate cortex. Three adjacent on-beta cells in the area centralis and their bipolar connections to cones were reconstructed from electron micrographs of 279 serial sections. The beta dendritic field is 34 +/- 2-mu-m in diameter and encompasses 35 cones. All of these cones connect to the beta cell via 14 - 17 bipolar cells. These bipolar cells were shown previously by cluster analysis to be of four types (b1 - b4); three of these types (b1, b2 and b3) provided 97% of the bipolar contacts to the beta cell, in the ratio 4:2:1. On average, bipolar cells nearest the centre of the beta dendritic field contribute more synapses than those towards the edge, but the peaked distribution of bipolar synapses across the dendritic field is only slightly broader than the optical pointspread function of the cat's eye, and is narrower by half than the centre of the ganglion cell receptive field. This implies that the distribution of bipolar synapses across the beta cell dendritic field contributes little to the extent or shape of the receptive field. Since all three bipolar circuits connect to the same set of cones, they must carry the same spatial and chromatic information; they might convey different temporal frequencies. The numbers of bipolar synapses (mean +/- SD = 154 +/- 8) and amacrine synapses (59 +/- 5) converging on three adjacent beta cells are remarkably constant (SD almost-equal-to +/- 5% of the mean). Thus, as the circuits repeat locally, the fundamental design is accurately reproduced.