title: Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina.
abstract: Anatomical and physiological approaches are beginning to reveal the synaptic origins of parallel ON- and OFF-pathway retinal circuits for the transmission of short (S-) wavelength sensitive cone signals in the primate retina. Anatomical data suggest that synaptic output from S-cones is largely segregated; central elements of synaptic triads arise almost exclusively from the "blue-cone" bipolar cell, a presumed ON bipolar, whereas triad-associated contacts derive primarily from the "flat" midget bipolar cell, a hyperpolarizing, OFF bipolar. Similarly, horizontal cell connectivity is also segregated, with only the H2 cell-type receiving numerous contacts from S-cones. Negative feedback from long (L-) and middle (M-) wavelength sensitive cones via the H2 horizontal cells elicits an antagonistic surround in S-cones demonstrating that S versus L + M or "blue-yellow" opponency is first established in the S-cone. However, the S-cone output utilizes distinct synaptic mechanisms to create color opponency at the ganglion cell level. The blue-cone bipolar cell is presynaptic to the small bistratified, "blue-ON" ganglion cell. S versus L + M cone opponency arises postsynaptically by converging S-ON and LM-OFF excitatory bipolar inputs to the ganglion cell's bistratified dendritic tree. The common L + M cone surrounds of the parallel S-ON and LM-OFF cone bipolar inputs appear to cancel resulting in "blue-yellow" antagonism without center-surround spatial opponency. By contrast, in midget ganglion cells, opponency arises by the differential weighting of cone inputs to the receptive field center versus surround. In the macula, the "private-line" connection from a midget ganglion cell to a single cone predicts that S versus L + M opponency is transmitted from the S-cone to the S-OFF midget bipolar and ganglion cell. Beyond the macula, OFF-midget ganglion cell dendritic trees enlarge and collect additional input from multiple L and M cones. Thus S-OFF opponency via the midget pathway would be expected to become more complex in the near retinal periphery as L and/or M and S cone inputs sum to the receptive field center. An important goal for further investigation will be to explore the hypothesis that distinct bistratified S-ON versus midget S-OFF retinal circuits are the substrates for human psychophysical detection mechanisms attributed to S-ON versus S-OFF perceptual channels.
authors.affiliation: Department of Biological Structure and The National Primate Research Center, University of Washington, Seattle, Washington.
authors.forename: Dennis M
authors.initials: DM
authors.lastname: Dacey
authors.affiliation: Department of Biological Structure and The National Primate Research Center, University of Washington, Seattle, Washington.
authors.forename: Joanna D
authors.initials: JD
authors.lastname: Crook
authors.affiliation: Department of Biological Structure and The National Primate Research Center, University of Washington, Seattle, Washington.
authors.forename: Orin S
authors.initials: OS
authors.lastname: Packer
mesh_terms: D000818:Animals; D003118:Color Perception / Q000502:physiology; D055253:Color Vision / Q000502:physiology*; D018408:Patch-Clamp Techniques; D011323:Primates / Q000502:physiology*; D051245:Retinal Bipolar Cells / Q000166:cytology; D017949:Retinal Cone Photoreceptor Cells / Q000166:cytology / Q000502:physiology*; D012165:Retinal Ganglion Cells / Q000166:cytology / Q000502:physiology; D055351:Retinal Neurons / Q000166:cytology / Q000502:physiology*; D013569:Synapses / Q000502:physiology*
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