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The Journal of Neuroscience, November 22, 2006, 26(47):12351-12361; doi:10.1523/JNEUROSCI.1071-06.2006

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Behavioral/Systems/Cognitive
Chromatic Properties of Horizontal and Ganglion Cell Responses Follow a Dual Gradient in Cone Opsin Expression

Lu Yin,¹ Robert G Smith,¹ Peter Sterling,¹ and David H. Brainard²

Departments of ¹Neuroscience and ²Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Dr. David H. Brainard, Department of Psychology, University of Pennsylvania, Suite 302C, 3401Walnut Street, Philadelphia, PA 19104. Email: brainard{at}psych.upenn.edu

In guinea pig retina, immunostaining reveals a dual gradient of opsins: cones expressing opsin sensitive to medium wavelengths (M) predominate in the upper retina, whereas cones expressing opsin sensitive to shorter wavelengths (S) predominate in the lower retina. Whether these gradients correspond to functional gradients in postreceptoral neurons is essentially unknown. Using monochromatic flashes, we measured the relative weights with which M, S, and rod signals contribute to horizontal cell responses. For a background that produced 4.76 log₁₀ photoisomerizations per rod per second (Rh*/rod/s), mean weights in superior retina were 52% (M), 2% (S), and 46% (rod). Mean weights in inferior retina were 9% (M), 50% (S), and 41% (rod). In superior retina, cone opsin weights agreed quantitatively with relative pigment density estimates from immunostaining. In inferior retina, cone opsin weights agreed qualitatively with relative pigment density estimates, but quantitative comparison was impossible because individual cones coexpress both opsins to varying and unquantifiable degrees. We further characterized the functional gradients in horizontal and brisk-transient ganglion cells using flickering stimuli produced by various mixtures of blue and green primary lights. Cone weights for both cell types resembled those obtained for horizontal cells using monochromatic flashes. Because the brisk-transient ganglion cell is thought to mediate behavioral detection of luminance contrast, our results are consistent with the hypothesis that the dual gradient of cone opsins assists achromatic contrast detection against different spectral backgrounds. In our preparation, rod responses did not completely saturate, even at background light levels typical of outdoor sunlight (5.14 log₁₀ Rh*/rod/s).

Key words: cone opsin dual gradient; horizontal cell; brisk-transient ganglion cell; cone weights; light adaptation; spectral sensitivity

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Received March 12, 2006; revised Oct. 18, 2006; accepted Oct. 19, 2006.

Correspondence should be addressed to Dr. David H. Brainard, Department of Psychology, University of Pennsylvania, Suite 302C, 3401Walnut Street, Philadelphia, PA 19104. Email: brainard{at}psych.upenn.edu

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