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Center/surround organization of retinal bipolar cells: High correlation of fundamental responses of center and surround to sinusoidal contrasts

Published online by Cambridge University Press:  25 March 2011

DWIGHT A. BURKHARDT ,
THEODORE M. BARTOLETTI  and
WALLACE B. THORESON
DWIGHT A. BURKHARDT*
Affiliation:
Department of Psychology and Graduate Program in Neuroscience, University of Minnesota, Minneapolis, Minnesota
THEODORE M. BARTOLETTI
Affiliation:
Departments of Ophthalmology & Visual Science and Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
WALLACE B. THORESON
Affiliation:
Departments of Ophthalmology & Visual Science and Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
*
*Address correspondence and reprint requests to: Dwight A. Burkhardt, Department of Psychology, n218 Elliott Hall, University of Minnesota, 75 East River Road, Minneapolis, MN 55455. E-mail: burkh001@umn.edu
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Abstract

Receptive field organization of cone-driven bipolar cells was investigated by intracellular recording in the intact light-adapted retina of the tiger salamander (Ambystoma tigrinum). Centered spots and concentric annuli of optimum dimensions were used to selectively stimulate the receptive field center and surround with sinusoidal modulations of contrast at 3 Hz. At low contrasts, responses of both the center and surround of both ON and OFF bipolar cells were linear, showing high gain and thus contrast enhancement relative to cones. The contrast/response curves for the fundamental response, measured by a Fast Fourier Transform, reached half maximum amplitude quickly at 13% contrast followed by saturation at high contrasts. The variation of the normalized amplitude of the center and surround responses was remarkably similar, showing linear regression over the entire response range with very high correlations, r2 = 0.97 for both ON and OFF cells. The contrast/response curves of both center and surround for both ON and OFF cells were well fit (r2 = 0.98) by an equation for single-site binding. In about half the cells studied, the nonlinear waveforms of center and surround could be brought into coincidence by scaling and shifting the surround response in time. This implies that a nonlinearity, common to both center and surround, occurs after polarity inversion at the cone feedback synapse. Evidence from paired whole-cell recordings between single cones and OFF bipolar cells suggests that substantial nonlinearity is not due to transmission at the cone synapse but instead arises from intrinsic bipolar cell and network mechanisms. When sinusoidal contrast modulations were applied to the center and surround simultaneously, clear additivity was observed for small responses in both ON and OFF cells, whereas the interaction was strikingly nonadditive for large responses. The contribution of the surround was then greatly reduced, suggesting attenuation at the cone feedback synapse.

Keywords

Retinal bipolar cellsCenter/surround receptive fieldContrast responses
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 3 , May 2011 , pp. 183 - 192
Copyright
Copyright © Cambridge University Press 2011

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