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The Journal of Neuroscience, July 1, 2009, 29(26):8372-8387; doi:10.1523/JNEUROSCI.1218-09.2009

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Behavioral/Systems/Cognitive
Parallel ON and OFF Cone Bipolar Inputs Establish Spatially Coextensive Receptive Field Structure of Blue-Yellow Ganglion Cells in Primate Retina

Joanna D. Crook,^1,3 Christopher M. Davenport,^2,3 Beth B. Peterson,¹ Orin S. Packer,¹ Peter B. Detwiler,² and Dennis M. Dacey^1,4

Departments of ¹Biological Structure and ²Physiology and Biophysics, and ³Neurobiology and Behavior Graduate Program, University of Washington, and ⁴Washington National Primate Research Center, Seattle, Washington 98195

Correspondence should be addressed to Dennis M. Dacey, Department of Biological Structure, University of Washington, Seattle, WA 98195. Email: dmd{at}u.washington.edu

In the primate retina the small bistratified, "blue-yellow" color-opponent ganglion cell receives parallel ON-depolarizing and OFF-hyperpolarizing inputs from short (S)-wavelength sensitive and combined long (L)- and middle (M)-wavelength sensitive cone photoreceptors, respectively. However, the synaptic pathways that create S versus LM cone-opponent receptive field structure remain controversial. Here, we show in the macaque monkey retina in vitro that at photopic light levels, when an identified rod input is excluded, the small bistratified cell displays a spatially coextensive receptive field in which the S-ON-input is in spatial, temporal, and chromatic balance with the LM-OFF-input. ON pathway block with L-AP-4, the mGluR6 receptor agonist, 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 OFF-center, ON-surround "diffuse" cone bipolar cells. Increasing retinal buffering capacity with HEPES attenuated the LM-ON surround component, consistent with a non-GABAergic 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 is not generated by an inner retinal inhibitory pathway. We conclude that the opponent S-ON and LM-OFF responses originate from the excitatory receptive field centers of S-ON and LM-OFF cone bipolar cells, and that the LM-OFF- and ON-surrounds of these parallel bipolar inputs largely cancel, explaining the small, spatially coextensive but spectrally antagonistic receptive field structure of the blue-ON ganglion cell.

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Received March 12, 2009; revised May 18, 2009; accepted May 29, 2009.

Correspondence should be addressed to Dennis M. Dacey, Department of Biological Structure, University of Washington, Seattle, WA 98195. Email: dmd{at}u.washington.edu

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