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The Journal of Neuroscience, May 1, 1998, 18(9):3373-3385

Microcircuitry and Mosaic of a Blue-Yellow Ganglion Cell in the Primate Retina

David J. Calkins1, Yoshihiko Tsukamoto2, and Peter Sterling3

1 The Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland 21218-2685, 2 Department of Anatomy, Hyogo College of Medicine, Hyogo 663, Japan, and 3 Department of Neuroscience, University of Pennsylvania Medical School, Philadelphia, Pennsylvania 19104-6058

Perception of hue is opponent, involving the antagonistic comparison of signals from different cone types. For blue versus yellow opponency, the antagonism is first evident at a ganglion cell with firing that increases to stimulation of short wavelength-sensitive (S) cones and decreases to stimulation of middle wavelength-sensitive (M) and long wavelength-sensitive (L) cones. This ganglion cell, termed blue-yellow (B-Y), has a distinctive morphology with dendrites in both ON and OFF strata of the inner plexiform layer (). Here we report the synaptic circuitry of the cell and its spatial density. Reconstructing neurons in macaque fovea from electron micrographs of serial sections, we identified six ganglion cells that branch in both strata and have similar circuitry. In the ON stratum each cell collects ~33 synapses from bipolar cells traced back exclusively to invaginating contacts from S cones, and in the OFF stratum each cell collects ~14 synapses from bipolar cells (types DB2 and DB3) traced to basal synapses from ~20 M and L cones. This circuitry predicts that spatially coincident blue-yellow opponency arises at the level of the cone output via expression of different glutamate receptors. S cone stimuli suppress glutamate release onto metabotropic receptors of the S cone bipolar cell dendrite, thereby opening cation channels, whereas M and L cone stimuli suppress glutamate release onto ionotropic glutamate receptors of DB2 and DB3 cell dendrites, thereby closing cation channels. Although the B-Y cell is relatively rare (3% of foveal ganglion cells), its spatial density equals that of the S cone; thus it could support psychophysical discrimination of a blue-yellow grating down to the spatial cutoff of the S cone mosaic.

Key words: color opponency; color discrimination; ganglion cell; bipolar cell; S cones; ribbon synapses


Copyright © 1998 Society for Neuroscience  0270-6474/98/1893373-13$05.00/0


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