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      Characterizing the rod pathway in cone-dominant thirteen-lined ground squirrels

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          Abstract

          AII-amacrine cells (AIIs) are widely accepted as a critical element of scotopic pathways mediating night vision in the mammalian retina and have been well-characterized in rod-dominant mice, rabbits, and non-human primates. The rod pathway is characteristic of all mammalian eyes, however, the anatomic and physiologic role of AIIs and the rod pathways in cone dominant thirteen-lined ground squirrels (TLGS) is limited. Here, we employed both immunohistochemistry and electrophysiological approaches to investigate the morphology of AIIs and functional aspects of the rod pathway in TLGS. In all TLGS retinas examined, putative AIIs were calretinin-positive and exhibited connections to rod bipolar cells with decreased cell density and expanded arborization. Notably, AIIs retained connections with each other via gap junctions labeled with Connexin36. Comparisons between single photoreceptor recordings and full-field electroretinograms revealed scotopic ERG responses were mediated by both rods and cones. Thus, the components of the rod pathway are conserved in TLGS and rod signals traverse the retina in these cone-dominant animals. AIIs are sparsely populated, matching the diminished rod and rod bipolar cell populations compared to rod-dominant species. The infrequent distribution and lateral spacing of AII’s indicate that they probably do not play a significant role in cone signaling pathways that encode information at a finer spatial scale. This contrasts with the mouse retina, where they significantly contribute to cone signaling pathways. Therefore, the AII’s original function is likely that of a ‘rod’ amacrine cell, and its role in cone pathways in the mouse retina might be an adaptive feature stemming from its rod dominance.

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          Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision.

          Rod and cone photoreceptors detect light and relay this information through a multisynaptic pathway to the brain by means of retinal ganglion cells (RGCs). These retinal outputs support not only pattern vision but also non-image-forming (NIF) functions, which include circadian photoentrainment and pupillary light reflex (PLR). In mammals, NIF functions are mediated by rods, cones and the melanopsin-containing intrinsically photosensitive retinal ganglion cells (ipRGCs). Rod-cone photoreceptors and ipRGCs are complementary in signalling light intensity for NIF functions. The ipRGCs, in addition to being directly photosensitive, also receive synaptic input from rod-cone networks. To determine how the ipRGCs relay rod-cone light information for both image-forming and non-image-forming functions, we genetically ablated ipRGCs in mice. Here we show that animals lacking ipRGCs retain pattern vision but have deficits in both PLR and circadian photoentrainment that are more extensive than those observed in melanopsin knockouts. The defects in PLR and photoentrainment resemble those observed in animals that lack phototransduction in all three photoreceptor classes. These results indicate that light signals for irradiance detection are dissociated from pattern vision at the retinal ganglion cell level, and animals that cannot detect light for NIF functions are still capable of image formation.
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            Intrinsic properties and functional circuitry of the AII amacrine cell.

            Amacrine cells represent the most diverse class of retinal neuron, comprising dozens of distinct cell types. Each type exhibits a unique morphology and generates specific visual computations through its synapses with a subset of excitatory interneurons (bipolar cells), other amacrine cells, and output neurons (ganglion cells). Here, we review the intrinsic and network properties that underlie the function of the most common amacrine cell in the mammalian retina, the AII amacrine cell. The AII connects rod and cone photoreceptor pathways, forming an essential link in the circuit for rod-mediated (scotopic) vision. As such, the AII has become known as the rod-amacrine cell. We, however, now understand that AII function extends to cone-mediated (photopic) vision, and AII function in scotopic and photopic conditions utilizes the same underlying circuit: AIIs are electrically coupled to each other and to the terminals of some types of ON cone bipolar cells. The direction of signal flow, however, varies with illumination. Under photopic conditions, the AII network constitutes a crossover inhibition pathway that allows ON signals to inhibit OFF ganglion cells and contributes to motion sensitivity in certain ganglion cell types. We discuss how the AII's combination of intrinsic and network properties accounts for its unique role in visual processing. Copyright © Cambridge University Press, 2012
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              Dark light, rod saturation, and the absolute and incremental sensitivity of mouse cone vision.

              Visual thresholds of mice for the detection of small, brief targets were measured with a novel behavioral methodology in the dark and in the presence of adapting lights spanning ∼8 log(10) units of intensity. To help dissect the contributions of rod and cone pathways, both wild-type mice and mice lacking rod (Gnat1(-/-)) or cone (Gnat2(cpfl3)) function were studied. Overall, the visual sensitivity of mice was found to be remarkably similar to that of the human peripheral retina. Rod absolute threshold corresponded to 12-15 isomerized pigment molecules (R*) in image fields of 800 to 3000 rods. Rod "dark light" (intrinsic retinal noise in darkness) corresponded to that estimated previously from single-cell recordings, 0.012 R* s(-1) rod(-1), indicating that spontaneous thermal isomerizations are responsible. Psychophysical rod saturation was measured for the first time in a nonhuman species and found to be very similar to that of the human rod monochromat. Cone threshold corresponded to ∼5 R* cone(-1) in an image field of 280 cones. Cone dark light was equivalent to ∼5000 R* s(-1) cone(-1), consistent with primate single-cell data but 100-fold higher than predicted by recent measurements of the rate of thermal isomerization of mouse cone opsins, indicating that nonopsin sources of noise determine cone threshold. The new, fully automated behavioral method is based on the ability of mice to learn to interrupt spontaneous wheel running on the presentation of a visual cue and provides an efficient and highly reliable means of examining visual function in naturally behaving normal and mutant mice.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/2226108Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2363584Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/179676Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/598355Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role: Role:
                Journal
                Front Ophthalmol (Lausanne)
                Front Ophthalmol (Lausanne)
                Front. Ophthalmol.
                Frontiers in Ophthalmology
                Frontiers Media S.A.
                2674-0826
                16 November 2023
                2023
                : 3
                : 1271882
                Affiliations
                [1] Retinal Neurophysiology Section, National Eye Institute, National Institutes of Health , Bethesda, MD, United States
                Author notes

                Edited by: Christophe P Ribelayga, University of Houston, Houston, United States

                Reviewed by: Nange Jin, University of Houston, Houston, United States; Michael Manookin, University of Washington, Seattle, United States; Erika Eggers, University of Arizona, Tucson, United States

                *Correspondence: Riley Ferguson, fergusonrs@ 123456nih.gov ; Kiyoharu J. Miyagishima, kiyoharu.miyagishima@ 123456nih.gov
                Article
                10.3389/fopht.2023.1271882
                11182244
                38974057
                857aaa02-5365-4ba1-a051-31cc05f20aee
                Copyright © 2023 Ferguson, Miyagishima, Nadal-Nicolas and Li

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 03 August 2023
                : 30 October 2023
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 24, Pages: 9, Words: 4116
                Funding
                Funded by: National Eye Institute , doi 10.13039/100000053;
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported [in part] by the Intramural Research Program of the NIH, National Eye Institute.
                Categories
                Ophthalmology
                Brief Research Report
                Custom metadata
                Retina

                aii-amacrine,bipolar cells,thirteen-lined ground squirrels,scotopic vision,rod pathways

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