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J. D. Crook, C. M. Davenport, B. B. Peterson, O. S. Packer, P. B. Detwiler, D. M. Dacey; Spatially Coextensive Receptive Field Structure of Blue-Yellow Ganglion Cells in Primate Retina Established by Parallel ON and OFF Cone Bipolar Inputs. Invest. Ophthalmol. Vis. Sci. 2009;50(13):3474.
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In the primate retina the small bistratified, ‘blue-ON’ color-opponent ganglion cell receives an ON signal from short (S) wavelength sensitive cone photoreceptors and an OFF signal from combined long (L) and middle (M) wavelength sensitive cones (LM). Since the inner and outer dendrites of the small bistratified cells are contacted by S cone- and LM cone-recipient bipolar cells respectively it has been suggesed that S-ON vs LM-OFF opponency arise by converging ON and OFF bipolar pathways; however the underlying circuitry for opponency remains unclear. Our purpose therefore was to test the ON-OFF pathway hypothesis of S vs LM opponency.
Loose patch recordings were made from 52 blue-ON cells in the choroid-rpe-attached in vitro retina of the macaque monkey. S and LM cone isolating stimuli were used to measure input strength, spatial extent, contrast gain and temporal sensitivity of the S-ON and LM-OFF fields. Bath application of L-AP-4, the mGluR6 receptor agonist to block the ON pathway, GABAa/c receptor antagonist picrotoxin and glycine receptor antagonist strychnine to block inner retinal inhbition and HEPES buffer to attenuate outer retinal surround feedback were used to dissect underlying circuitry.
The S-ON and LM-OFF fields were spatially well matched resulting in a remarkably ‘pure’ chromatic signal. L-AP4 abolished the S-ON response but spared the LM-OFF response. The isolated LM component showed a center-surround receptive field structure consistent with an input from an OFF-center, ON-surround ‘diffuse’ cone bipolar cell. Increasing retinal buffering capacity with HEPES attenuated the LM-ON surround component, consistent with an outer retina feedback mechanism for the bipolar surround. The GABAa/c receptor antagonist picrotoxin and the glycine receptor antagonist strychnine did not affect chromatic balance or the basic coextensive receptive field structure suggesting that the LM-OFF field was not generated by an inner retinal inhibitory pathway.
The opponent S-ON and LM-OFF responses originate from the excitatory receptive field centers of S-ON and LM-OFF cone bipolar inputs to the small bistratified dendritic tree in support of the ON-OFF pathway hypothesis. We suggest that LM-OFF- and LM-ON-surrounds of these parallel bipolar inputs largely cancel explaining the small, spatially coextensive but spectrally antagonistic receptive field structure characteristic of the blue-ON ganglion cell.
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