What the salamander eye has been telling the vision scientist’s brain

Rozenblit, Fernando; Gollisch, Tim

doi:10.1016/j.semcdb.2020.04.010

Cited by 15 publications

(9 citation statements)

References 189 publications

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“…Visual processing in the retina has been probed for decades by examining the light response properties of retinal ganglion cells (RGCs) in several animal models, including salamander, mouse, rabbit, cat, and monkey. The assembled findings indicate that although the functional organization of RGCs has some broad similarities across species --notably, a subdivision into discrete RGC types that encode different aspects of the visual scene --substantial anatomical and physiological differences between species suggest varying degrees of relevance for understanding human vision [1][2][3][4][5][6]. Among animal models, the macaque monkey is widely considered to be the most relevant for human vision, for several reasons: phylogenetic proximity, similar natural visual environment, similar visual behaviors, similar gross and fine structure of the retina, and similar anatomically identified RGC types [7][8][9][10][11].…”

Section: Introductionmentioning

confidence: 96%

Functional Organization of Midget and Parasol Ganglion Cells in the Human Retina

Kling

Gogliettino

Shah

et al. 2020

Preprint

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The functional organization of diverse retinal ganglion cell (RGC) types, which shape the visual signals transmitted to the brain, has been examined in many species. The unique spatial, temporal, and chromatic properties of the numerically dominant RGC types in macaque monkey retina are presumed to most accurately model human vision. However, the functional similarity between RGCs in macaques and humans has only begun to be tested, and recent work suggests possible differences. Here, the properties of the numerically dominant human RGC types were examined using large-scale multi-electrode recordings with fine-grained visual stimulation in isolated retina, and compared to results from dozens of recordings from macaque retina using the same experimental methods and conditions. The properties of four major human RGC types -- ON-parasol, OFF-parasol, ON-midget, and OFF-midget -- closely paralleled those of the same macaque RGC types, including the spatial and temporal light sensitivity, precisely coordinated mosaic organization of receptive fields, ON-OFF asymmetries, spatial response nonlinearity, and sampling of photoreceptor inputs over space. Putative smooth monostratified cells and polyaxonal amacrine cells were also identified based on similarities to cell types previously identified in macaque retina. The results suggest that recently proposed differences between human and macaque RGCs probably reflect experimental differences, and that the macaque model provides an accurate picture of human RGC function.

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Section: Introductionmentioning

confidence: 96%

Functional Organization of Midget and Parasol Ganglion Cells in the Human Retina

Kling

Gogliettino

Shah

et al. 2020

Preprint

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“…They are again missing in eutherian mammals [ 3 ]. By contrast, blue rods are only present in amphibians [ 21 , 38 ] and therefore probably emerged after their lineage had already diverged from that of subsequent terrestrial species. The origin of double cones is debated, but their anatomical similarity to pairs of ancestral red and green cones in the eyes of fish [ 18 ] points at their joint duplication as a likely candidate.…”

Section: Introductionmentioning

confidence: 99%

From water to land: Evolution of photoreceptor circuits for vision in air

Baden

2024

PLoS Biol

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When vertebrates first conquered the land, they encountered a visual world that was radically distinct from that of their aquatic ancestors. Fish exploit the strong wavelength-dependent interactions of light with water by differentially feeding the signals from up to 5 spectral photoreceptor types into distinct behavioural programmes. However, above the water the same spectral rules do not apply, and this called for an update to visual circuit strategies. Early tetrapods soon evolved the double cone, a still poorly understood pair of new photoreceptors that brought the “ancestral terrestrial” complement from 5 to 7. Subsequent nonmammalian lineages differentially adapted this highly parallelised retinal input strategy for their diverse visual ecologies. By contrast, mammals shed most ancestral photoreceptors and converged on an input strategy that is exceptionally general. In eutherian mammals including in humans, parallelisation emerges gradually as the visual signal traverses the layers of the retina and into the brain.

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“…This raises the question whether there are systematic differences between different classes of ganglion cells. For the salamander retina, a general classification scheme of ganglion cells is still lacking [46], and physiological classifications are typically based on preferred contrast (ON versus OFF) and temporal filtering kinetics [10,41,47,48]. Following these lines, we here divided the recorded OFF ganglion cells into four groups by a cluster analysis (see Materials and Methods), according to their receptive field size and temporal filtering kinetics (Fig.…”

Section: Resultsmentioning

confidence: 99%

Simple Model for Encoding Natural Images by Retinal Ganglion Cells with Nonlinear Spatial Integration

Liu

Gollisch

2021

Preprint

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A central goal in sensory neuroscience is to understand the neuronal signal processing involved in the encoding of natural stimuli. A critical step towards this goal is the development of successful computational models of this encoding. For ganglion cells in the vertebrate retina, the development of satisfactory models for responses to natural visual scenes is an ongoing challenge. Standard models typically apply linear integration of visual stimuli over space, yet many ganglion cells are known to show nonlinear spatial integration in natural stimulus contexts. We here study the encoding of natural images by retinal ganglion cells, using multielectrode-array recordings from isolated salamander retinas. We assess how responses to natural and blurred images depend on first- and second-order statistics of spatial patterns inside the receptive field. This leads us to a simple extension of current standard ganglion cell models, which are based on linear spatial integration. We show that taking not only the weighted average of light intensity inside the receptive field into account but also its variance over space yields substantially improved response predictions of responses to novel images. Finally, we demonstrate how this model framework can be used to assess the spatial scale of nonlinear spatial integration. Our results underscore the importance of nonlinear spatial stimulus integration in the retina in responses to natural images. Furthermore, the introduced model framework provides a simple, yet powerful extension of standard models and may serve as a benchmark for the development of more detailed models of the nonlinear structure of receptive fields.

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What the salamander eye has been telling the vision scientist’s brain

Abstract: Graphical abstract

Cited by 15 publications

References 189 publications

Functional Organization of Midget and Parasol Ganglion Cells in the Human Retina

Functional Organization of Midget and Parasol Ganglion Cells in the Human Retina

From water to land: Evolution of photoreceptor circuits for vision in air

Simple Model for Encoding Natural Images by Retinal Ganglion Cells with Nonlinear Spatial Integration

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