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      Retinal output changes qualitatively with every change in ambient illuminance

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          Abstract

          The collective activity pattern of retinal ganglion cells, the retinal code, underlies higher visual processing. How does the ambient illuminance of the visual scene influence this retinal output? We recorded from isolated mouse and pig retina and from mouse dLGN in-vivo at up to seven ambient light levels covering the scotopic to photopic regimes. Across each luminance transition, the majority of ganglion cells exhibited qualitative response changes, while maintaining stable responses within each luminance. Strikingly, we commonly observed the appearance and disappearance of ON responses in OFF cells and vice versa. Such qualitative response changes occurred for a variety of stimuli, including full-field and localized contrast steps, and naturalistic movies. Our results suggest that the retinal code is not fixed but varies with every change of ambient luminance. This finding raises new questions about signal processing within the retina and has intriguing implications for visual processing in higher brain areas.

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          Most cited references58

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          Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration.

          The death of photoreceptor cells caused by retinal degenerative diseases often results in a complete loss of retinal responses to light. We explore the feasibility of converting inner retinal neurons to photosensitive cells as a possible strategy for imparting light sensitivity to retinas lacking rods and cones. Using delivery by an adeno-associated viral vector, here, we show that long-term expression of a microbial-type rhodopsin, channelrhodopsin-2 (ChR2), can be achieved in rodent inner retinal neurons in vivo. Furthermore, we demonstrate that expression of ChR2 in surviving inner retinal neurons of a mouse with photoreceptor degeneration can restore the ability of the retina to encode light signals and transmit the light signals to the visual cortex. Thus, expression of microbial-type channelrhodopsins, such as ChR2, in surviving inner retinal neurons is a potential strategy for the restoration of vision after rod and cone degeneration.
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            A simple white noise analysis of neuronal light responses.

            A white noise technique is presented for estimating the response properties of spiking visual system neurons. The technique is simple, robust, efficient and well suited to simultaneous recordings from multiple neurons. It provides a complete and easily interpretable model of light responses even for neurons that display a common form of response nonlinearity that precludes classical linear systems analysis. A theoretical justification of the technique is presented that relies only on elementary linear algebra and statistics. Implementation is described with examples. The technique and the underlying model of neural responses are validated using recordings from retinal ganglion cells, and in principle are applicable to other neurons. Advantages and disadvantages of the technique relative to classical approaches are discussed.
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              Eye smarter than scientists believed: neural computations in circuits of the retina.

              We rely on our visual system to cope with the vast barrage of incoming light patterns and to extract features from the scene that are relevant to our well-being. The necessary reduction of visual information already begins in the eye. In this review, we summarize recent progress in understanding the computations performed in the vertebrate retina and how they are implemented by the neural circuitry. A new picture emerges from these findings that helps resolve a vexing paradox between the retina's structure and function. Whereas the conventional wisdom treats the eye as a simple prefilter for visual images, it now appears that the retina solves a diverse set of specific tasks and provides the results explicitly to downstream brain areas. Copyright 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                14 November 2014
                08 December 2014
                January 2015
                01 July 2015
                : 18
                : 1
                : 66-74
                Affiliations
                [1 ]Retinal Circuits and Optogenetics, Centre for Integrative Neuroscience and Bernstein Center for Computational Neuroscience, University of Tübingen, Germany
                [2 ]Faculty of Life Science, University of Manchester, Manchester M13 9PT, United Kingdom
                [3 ]Department for General, Visceral and Transplant Surgery, Institute for Experimental Surgery, University Hospital Tübingen, Germany
                [4 ]Current address: Dept. of Neurosurgery and Hansen Experimental Physics Laboratory, Stanford University, Stanford CA 94305, USA
                Author notes
                [§ ]Correspondence address: thomas.muench@ 123456cin.uni-tuebingen.de

                Author contribution: A.T.-H., K.R., and T.A.M. designed the study. MEA recordings and spike sorting were performed by A.T.-H., K.R., H.S. and A.H. and analyzed by A.T.-H., K.R. and T.A.M. Patch-clamp experiments and immunohistochemistry were conducted and analyzed by H.S. and T.A.M. In-vivo experiments were designed by C.A.P., A.E.A. and R.J.L., performed by C.A.P. and A.E.A., and analyzed by C.A.P., A.E.A. and K.R. Pig eyes were provided by M.S. Manuscript was prepared by A.T.-H., K.R. and T.A.M. with the help of H.S., C.A.P., A.E.A. and R.J.L.

                Article
                EMS60943
                10.1038/nn.3891
                4338531
                25485757
                d3bc9e8c-8a8d-4dd5-aaf9-20f0b12624aa
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                Neurosciences
                Neurosciences

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