title: Horizontal cell feedback without cone type-selective inhibition mediates "red-green" color opponency in midget ganglion cells of the primate retina.
abstract: The distinctive red-green dimension of human and nonhuman primate color perception arose relatively recently in the primate lineage with the appearance of separate long (L) and middle (M) wavelength-sensitive cone photoreceptor types. "Midget" ganglion cells of the retina use center-surround receptive field structure to combine L and M cone signals antagonistically and thereby establish a "red-green, color-opponent" visual pathway. However, the synaptic origin of red-green opponency is unknown, and conflicting evidence for either random or L versus M cone-selective inhibitory circuits has divergent implications for the developmental and evolutionary origins of trichromatic color vision. Here we directly measure the synaptic conductances evoked by selective L or M cone stimulation in the midget ganglion cell dendritic tree and show that L versus M cone opponency arises presynaptic to the midget cell and is transmitted entirely by modulation of an excitatory conductance. L and M cone synaptic inhibition is feedforward and thus occurs in phase with excitation for both cone types. Block of GABAergic and glycinergic receptors does not attenuate or modify L versus M cone antagonism, discounting both presynaptic and postsynaptic inhibition as sources of cone opponency. In sharp contrast, enrichment of retinal pH-buffering capacity, to attenuate negative feedback from horizontal cells that sum L and M cone inputs linearly and without selectivity, completely abolished both the midget cell surround and all chromatic opponency. Thus, red-green opponency appears to arise via outer retinal horizontal cell feedback that is not cone type selective without recourse to any inner retinal L versus M cone inhibitory pathways.
authors.affiliation: Department of Biological Structure, University of Washington, Seattle, Washington 98195-7420, USA.
authors.forename: Joanna D
authors.initials: JD
authors.lastname: Crook
authors.forename: Michael B
authors.initials: MB
authors.lastname: Manookin
authors.forename: Orin S
authors.initials: OS
authors.lastname: Packer
authors.forename: Dennis M
authors.initials: DM
authors.lastname: Dacey
mesh_terms: D000818:Animals; D003118:Color Perception / Q000502:physiology*; D003712:Dendrites / Q000502:physiology; D056228:Feedback, Sensory; D066298:In Vitro Techniques; D008251:Macaca; D009433:Neural Inhibition / Q000502:physiology*; D009483:Neuropsychological Tests; D010775:Photic Stimulation / Q000379:methods; D012160:Retina / Q000166:cytology; D017949:Retinal Cone Photoreceptor Cells / Q000502:physiology*; D012165:Retinal Ganglion Cells / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*