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The ganglion cells of primate retina have center-surround receptive fields. A strong candidate for mediating linear surround circuitry is negative feedback from the H1 horizontal cell onto the cone pedicle. We measured the spatial properties of H1 cell receptive fields in the in vitro macaque monkey retina using sinusoidal gratings, spots, and annuli. Spatial tuning curves ranged in shape from smoothly low pass to prominently notched. The tuning curves of approximately 80% of cells could be well described by a sum of two exponentials, giving a prominent central peak superimposed on a broad shallow skirt. The mean diameter of the combined receptive field decreased with eccentricity from 309 micro m at 11 mm to 122 micro m at 4 mm. We propose that the strong narrow field reflects direct synaptic input from the cones overlying the dendritic tree whereas the weak wide field reflects coupled inputs from neighboring H1 cells. Those cells not well fit by a sum of exponentials had tuning curves with additional peaks at higher spatial frequencies that were likely due to undersampling in the cone-H1 network. Unlike other vertebrates, the macaque H1 network is less strongly coupled, has smaller receptive fields, and shows no functional plasticity. Macaque H1 receptive fields are surprisingly small, suggesting a great reduction in electrical coupling. Because the center of the H1 receptive field gets only a small percentage of its total response from the coupled field, the smallest receptive fields are similar in diameter to the dendritic trees. They are probably small enough to form the surrounds of foveal midget cells. The H1 network is compatible with a mixed-surround model of spectral opponency.

Receptive field structure of H1 horizontal cells in macaque monkey retina