Synergistic center-surround receptive field model of monkey H1 horizontal cells

Horizontal cells typical of the vertebrate retina are strongly coupled by gap junctions. The resulting horizontal cell network has extremely large receptive fields that extend well beyond the boundaries of a single dendritic tree. This network has been modeled as a syncytium of cytoplasm bounded by cell membrane (Lamb 1976; Naka & Rushton, 1967). Horizontal cells in the primate retina are also coupled by gap junctions, but their receptive fields are relatively small and in some cases may approximate the span of the dendritic tree of an individual cell (Packer & Dacey, 2002). The receptive field of the macaque H1 horizontal cell type has been modeled as the sum of two spatial components: a strong but small diameter excitatory center, and a weak but broad excitatory surround. Here we explore the hypothesis that the receptive field center of H1 cells derives from direct cone synaptic input and that the synergistic surround derives from gap-junctional coupling among H1 cell neighbors. We measured the receptive field structure of H1 cells in the presence of carbenoxolone, a gap junction blocker, to determine the effects of uncoupling center and surround components and compared these data to a neural simulation of the H1 network in which gap-junctional conductance could be manipulated. Carbenoxolone reduced the surround component and eliminated irregularities in spatial structure thought to be associated with the surround. The effects of carbenoxolone could be mimicked by manipulating gap-junctional conductance in an H1 cell network simulation. These results provide strong support for the two-component model of H1 receptive field structure. In addition, carbenoxolone eliminated a slow depolarization following light onset thought to be mediated by cone-H1 feedback (Kamermans & Spekreijse, 1999). Low concentrations of cobalt, a calcium channel blocker that spares gap junctions, had an effect similar to that of carbenoxolone but did not affect receptive field structure. These results are consistent with a calcium-mediated mechanism of feedback from H1 cells to cones that is independent of the synergistic two-component model of receptive field organization.