Simulation of an anatomically defined local circuit: the cone-horizontal cell network in cat retina

Abstract

The outer plexiform layer of the retina contains a neural circuit in which cone synaptic terminals are electrically coupled and release glutamate onto wide-field and narrow-field horizontal cells. These are also electrically coupled and feed back through a GABAergic synapse to cones. In cat this circuit's structure is known in some detail, and much of the chemical architecture and neural responses are also known, yet there has been no attempt to synthesize this knowledge. We constructed a large-scale compartmental model (up to 50,000 compartments) to incorporate the known anatomical and biophysical facts. The goal was to discover how the various circuit components interact to form the cone receptive field, and thereby what possible function is implied. The simulation reproduced many features known from intracellular recordings: (1) linear response of cone and horizontal cell to intensity, (2) some aspects of temporal responses of cone and horizontal cell, (3) broad receptive field of the wide-field horizontal cell, and (4) center-surround cone receptive field (derived from a "deconvolution model"). With the network calibrated in this manner, we determined which of its features are necessary to give the cone receptive field a Gaussian center-surround shape. A Gaussian-like center that matches the center derived from the ganglion cell requires both optical blur and cone coupling: blur alone is too narrow, coupling alone gives an exponential shape without a central dome-shaped peak. A Gaussian-like surround requires both types of horizontal cell: the narrow-field type for the deep, proximal region and the wide-field type for the shallow, distal region. These results suggest that the function of the cone-horizontal cell circuit is to reduce the influence of noise by spatio-temporally filtering the cone signal before it passes through the first chemical synapse on the pathway to the brain.