Melanopsin Mediates Retrograde Visual Signaling in the Retina

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Abstract

The canonical flow of visual signals proceeds from outer to inner retina (photoreceptors→bipolar cells→ganglion cells). However, melanopsin-expressing ganglion cells are photosensitive and functional sustained light signaling to retinal dopaminergic interneurons persists in the absence of rods and cones. Here we show that the sustained-type light response of retinal dopamine neurons requires melanopsin and that the response is mediated by AMPA-type glutamate receptors, defining a retrograde retinal visual signaling pathway that fully reverses the usual flow of light signals in retinal circuits.

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Most cited references 19

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Dopamine and retinal function.

Paul Witkovsky (2003)

This review summarizes the experimental evidence in support of dopamine's role as a chemical messenger for light adaptation. Dopamine is released by a unique set of amacrine cells and activates D1 and D2 dopamine receptors distributed throughout the retina. Multiple dopamine-dependent physiological mechanisms result in an increased signal flow through cone circuits and a diminution of signal flow through rod circuits. Dopamine also has multiple trophic roles in retinal function related to circadian rhythmicity, cell survival and eye growth. In a reciprocal way, the health of the dopaminergic neurons depends on their receiving light-driven synaptic inputs. Dopamine neurons appear early in development, become functional in advance of the animal's onset of vision and begin to die in aging animals. Some diseases affecting photoreceptor function also diminish day/night differences in dopamine release and turnover. A reduction in retinal dopamine, as occurs in Parkinsonian patients, results in reduced visual contrast sensitivity.

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Retinal dopamine mediates multiple dimensions of light-adapted vision.

P. Iuvone, Richard D. Palmiter, Karen L. Gamble … (2012)

Dopamine is a key neuromodulator in the retina and brain that supports motor, cognitive, and visual function. Here, we developed a mouse model on a C57 background in which expression of the rate-limiting enzyme for dopamine synthesis, tyrosine hydroxylase, is specifically disrupted in the retina. This model enabled assessment of the overall role of retinal dopamine in vision using electrophysiological (electroretinogram), psychophysical (optokinetic tracking), and pharmacological techniques. Significant disruptions were observed in high-resolution, light-adapted vision caused by specific deficits in light responses, contrast sensitivity, acuity, and circadian rhythms in this retinal dopamine-depleted mouse model. These global effects of retinal dopamine on vision are driven by the differential actions of dopamine D1 and D4 receptors on specific retinal functions and appear to be due to the ongoing bioavailability of dopamine rather than developmental effects. Together, our data indicate that dopamine is necessary for the circadian nature of light-adapted vision as well as optimal contrast detection and acuity.

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Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons.

David Berson, B G Pickard, Patricia J. Sollars … (2008)

Retinal dopaminergic amacrine neurons (DA neurons) play a central role in reconfiguring retinal function according to prevailing illumination conditions, yet the mechanisms by which light regulates their activity are poorly understood. We investigated the means by which sustained light responses are evoked in DA neurons. Sustained light responses were driven by cationic currents and persisted in vitro and in vivo in the presence of L-AP4, a blocker of retinal ON-bipolar cells. Several characteristics of these L-AP4-resistant light responses suggested that they were driven by melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs), including long latencies, marked poststimulus persistence, and a peak spectral sensitivity of 478 nm. Furthermore, sustained DA neuron light responses, but not transient DA neuron responses, persisted in rod/cone degenerate retinas, in which ipRGCs account for virtually all remaining retinal phototransduction. Thus, ganglion-cell photoreceptors provide excitatory drive to DA neurons, most likely by way of the coramification of their dendrites and the processes of DA neurons in the inner plexiform layer. This unprecedented centrifugal outflow of ganglion-cell signals within the retina provides a novel basis for the restructuring of retinal circuits by light.

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Author and article information

Contributors

: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2012

Publication date (Electronic): 3 August 2012

Volume: 7

Issue: 8

Electronic Location Identifier: e42647

Affiliations

[1 ]Eye Research Institute, Oakland University, Rochester, Michigan, United States of America

[2 ]Department of Cell and Animal Biology, Hebrew University of Jerusalem, Jerusalem, Israel

[3 ]School of Veterinary Medicine and Biomedical Sciences, University of Nebraska, Lincoln, Nebraska, United States of America

[4 ]Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, Nebraska, United States of America

[5 ]Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America

Dalhousie University, Canada

Author notes

* E-mail: zhang@ 123456oakland.edu (D-QZ); douglas.g.mcmahon@ 123456vanderbilt.edu (DGM)

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: D-QZ GEP DGM. Performed the experiments: D-QZ MAB PJS GEP DGM. Analyzed the data: D-QZ MAB PJS GEP DGM. Contributed reagents/materials/analysis tools: D-QZ MAB PJS GEP DGM. Wrote the paper: DGM D-QZ GEP.

Article

Publisher ID: PONE-D-12-16494

DOI: 10.1371/journal.pone.0042647

PMC ID: 3411794

PubMed ID: 22880066

SO-VID: 8f68f93b-1bdb-41d5-98c9-63ba930e7b3d

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 6 June 2012

Date accepted : 11 July 2012

Page count

Pages: 5

Funding

Supported by NIH R01 EY09256 to DGM, the Vanderbilt Vision Core Grant P30 EY008126, NIH R01 EY017809 to PJS and GEP, Oakland University Research Excellent Fund and Midwest Eye Bank Research Grant Award to D-QZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Melanopsin Mediates Retrograde Visual Signaling in the Retina

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Abstract

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Neuronal Signaling

Most cited references 19

Dopamine and retinal function.

Retinal dopamine mediates multiple dimensions of light-adapted vision.

Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons.

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