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The Journal of Neuroscience, October 29, 2008, 28(44):11277-11291; doi:10.1523/JNEUROSCI.2982-08.2008

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Behavioral/Systems/Cognitive
Y-Cell Receptive Field and Collicular Projection of Parasol Ganglion Cells in Macaque Monkey Retina

Joanna D. Crook,^1,2 Beth B. Peterson,¹ Orin S. Packer,¹ Farrel R. Robinson,^1,3 John B. Troy,⁴ and Dennis M. Dacey^1,3

¹Department of Biological Structure, ²Graduate Program in Neurobiology and Behavior, and ³Washington National Primate Research Center, University of Washington, Seattle, Washington 98195, and ⁴Department of Biomedical Engineering, Northwestern University, Evanston, Illinois 60208

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

The distinctive parasol ganglion cell of the primate retina transmits a transient, spectrally nonopponent signal to the magnocellular layers of the lateral geniculate nucleus. Parasol cells show well-recognized parallels with the -Y cell of other mammals, yet two key -Y cell properties, a collateral projection to the superior colliculus and nonlinear spatial summation, have not been clearly established for parasol cells. Here, we show by retrograde photodynamic staining that parasol cells project to the superior colliculus. Photostained dendritic trees formed characteristic spatial mosaics and afforded unequivocal identification of the parasol cells among diverse collicular-projecting cell types. Loose-patch recordings were used to demonstrate for all parasol cells a distinct Y-cell receptive field "signature" marked by a nonlinear mechanism that responded to contrast-reversing gratings at twice the stimulus temporal frequency [second Fourier harmonic (F2)] independent of stimulus spatial phase. The F2 component showed high contrast gain and temporal sensitivity and appeared to originate from a region coextensive with that of the linear receptive field center. The F2 spatial frequency response peaked well beyond the resolution limit of the linear receptive field center, showing a Gaussian center radius of 15 µm. Blocking inner retinal inhibition elevated the F2 response, suggesting that amacrine circuitry does not generate this nonlinearity. Our data are consistent with a pooled-subunit model of the parasol Y-cell receptive field in which summation from an array of transient, partially rectifying cone bipolar cells accounts for both linear and nonlinear components of the receptive field.

Key words: primate; superior colliculus; retina; Y cell; magnocellular; spatial vision

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Received June 27, 2008; revised Sept. 2, 2008; accepted Sept. 7, 2008.

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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The Primate Retina Contains Distinct Types of Y-Like Ganglion Cells

Ari Rosenberg and Vargha Talebi
J. Neurosci. 2009 29: 5048-5050. [Full Text]  

This article has been cited by other articles:

				N. T. Dhruv, C. Tailby, S. H. Sokol, N. J. Majaj, and P. Lennie Nonlinear Signal Summation in Magnocellular Neurons of the Macaque Lateral Geniculate Nucleus J Neurophysiol, September 1, 2009; 102(3): 1921 - 1929. [Abstract] [Full Text] [PDF]

				J. D. Crook, C. M. Davenport, B. B. Peterson, O. S. Packer, P. B. Detwiler, and D. M. Dacey Parallel ON and OFF Cone Bipolar Inputs Establish Spatially Coextensive Receptive Field Structure of Blue-Yellow Ganglion Cells in Primate Retina J. Neurosci., July 1, 2009; 29(26): 8372 - 8387. [Abstract] [Full Text] [PDF]

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				J. D. Crook, B. B. Peterson, O. S. Packer, F. R. Robinson, P. D. Gamlin, J. B. Troy, and D. M. Dacey The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey J. Neurosci., November 26, 2008; 28(48): 12654 - 12671. [Abstract] [Full Text] [PDF]

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