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The Journal of Neuroscience, March 7, 2007, 27(10):2636-2645; doi:10.1523/JNEUROSCI.4610-06.2007

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Behavioral/Systems/Cognitive
Cellular Basis for Contrast Gain Control over the Receptive Field Center of Mammalian Retinal Ganglion Cells

Deborah L. Beaudoin,¹ Bart G. Borghuis,² and Jonathan B. Demb¹

¹Department of Ophthalmology and Visual Sciences and Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48105, and ²Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Dr. Jonathan B. Demb, Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105. Email: jdemb{at}umich.edu

Retinal ganglion cells fire spikes to an appropriate contrast presented over their receptive field center. These center responses undergo dynamic changes in sensitivity depending on the ongoing level of contrast, a process known as "contrast gain control." Extracellular recordings suggested that gain control is driven by a single wide-field mechanism, extending across the center and beyond, that depends on inhibitory interneurons: amacrine cells. However, recordings in salamander suggested that the excitatory bipolar cells, which drive the center, may themselves show gain control independently of amacrine cell mechanisms. Here, we tested in mammalian ganglion cells whether amacrine cells are critical for gain control over the receptive field center. We made extracellular and whole-cell recordings of guinea pig Y-type cells in vitro and quantified the gain change between contrasts using a linear–nonlinear analysis. For spikes, tripling contrast reduced gain by 40%. With spikes blocked, ganglion cells showed similar levels of gain control in membrane currents and voltages and under conditions of low and high calcium buffering: tripling contrast reduced gain by 20–25%. Gain control persisted under voltage-clamp conditions that minimize inhibitory conductances and pharmacological conditions that block inhibitory neurotransmitter receptors. Gain control depended on adequate stimulation, not of ganglion cells but of presynaptic bipolar cells. Furthermore, horizontal cell measurements showed a lack of gain control in photoreceptor synaptic release. Thus, the mechanism for gain control over the ganglion cell receptive field center, as measured in the subthreshold response, originates in the presynaptic bipolar cells and does not require amacrine cell signaling.

Key words: adaptation; whole-cell recording; amacrine cell; bipolar cell; intracellular recording; vision

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Received Oct. 24, 2006; revised Jan. 19, 2007; accepted Feb. 5, 2007.

Correspondence should be addressed to Dr. Jonathan B. Demb, Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105. Email: jdemb{at}umich.edu

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