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Stimulus discrimination via responses of retinal ganglion cells and dopamine-dependent modulation.

ABSTRACT: Neighboring retinal ganglion cells (RGCs) fire with a high degree of correlation. It has been increasingly realized that visual perception of the environment relies on neuronal population activity to encode and transmit the information contained in stimuli. Understanding how neuronal population activity contributes to visual information processing is essential for understanding the mechanisms of visual coding. Here we simultaneously recorded spike discharges from groups of RGCs in bullfrog retina in response to visual patterns (checkerboard, horizontal grating, and full-field illumination) using a multi-electrode array system. To determine the role of synchronous activity mediated by gap junctions, we measured the correct classification rates of single cells' firing patterns as well as the synchronization patterns of multiple neurons. We found that, under normal conditions, RGC population activity exhibited distinct response features with exposure to different stimulus patterns and had a higher rate of correct stimulus discrimination than the activity of single cells. Dopamine (1 μmol/L) application did not significantly change the performance of single neuron activity, but enhanced the synchronization of the RGC population activity and decreased the rate of correct stimulus pattern discrimination. These findings suggest that the synchronous activity of RGCs plays an important role in the information coding of different types of visual patterns, and a dopamine-induced increase in synchronous activity weakens the population performance in pattern discrimination, indicating the potential role of the dopaminergic pathway in modulating the population coding process.

SUBMITTER: Li H

PROVIDER: S-EPMC5561962 | biostudies-other | 2013 Oct

REPOSITORIES: biostudies-other

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Project description:A small number (<2%) of mammalian retinal ganglion cells express the photopigment melanopsin and are intrinsically photosensitive (ipRGCs). Light depolarizes ipRGCs and increases intracellular calcium levels ([Ca2+]i) but the signaling cascades underlying these responses have yet to be elucidated. To facilitate physiological studies on these rare photoreceptors, highly enriched ipRGC cultures from neonatal rats were generated using anti-melanopsin-mediated plate adhesion (immunopanning). This novel approach enabled experiments on isolated ipRGCs, eliminating the potential confounding influence of rod/cone-driven input. Light induced a rise in [Ca2+]i (monitored using fura-2 imaging) in the immunopanned ipRGCs and the source of this Ca2+ signal was investigated. The Ca2+ responses were inhibited by 2-aminoethoxydiphenyl borate, SKF-96365 (1-2-(4-methoxyphenyl)-2-[3-(4-methoxyphenyl)propoxy]ethyl-1H-imidazole), flufenamic acid, lanthanum, and gadolinium, consistent with the involvement of canonical transient receptor potential (TRP) channels in ipRGC phototransduction. However, the contribution of direct Ca2+ flux through a putative TRP channel to ipRGC [Ca2+]i was relatively small, as most (approximately 90%) of the light-induced Ca2+ responses could be blocked by preventing action potential firing with tetrodotoxin. The L-type voltage-gated Ca2+ channel (VGCC) blockers verapamil and (+)-cis-diltiazem significantly reduced the light-evoked Ca2+ responses, while the internal Ca2+ stores depleting agent thapsigargin had negligible effect. These results indicate that Ca2+ influx through VGCCs, activated after action potential firing, was the primary source for light-evoked elevations in ipRGC [Ca2+]i. Furthermore, concurrent Ca2+ imaging and cell-attached electrophysiological recordings demonstrated that the Ca2+ responses were highly correlated to spike frequency, thereby establishing a direct link between action potential firing and somatic [Ca2+]i in light-stimulated ipRGCs.

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Stimulus discrimination via responses of retinal ganglion cells and dopamine-dependent modulation.

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