Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina

Dacey, Dennis M.; Crook, Joanna D.; Packer, Orin S.

doi:10.1017/s0952523813000230

Cited by 70 publications

(68 citation statements)

References 96 publications

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“…Giant ipRGCs receive inhibitory input from S cones (12), but it is not immediately clear which synaptic inputs mediate this S-off sensitivity (20). Because there is presently no evidence for an S-off bipolar cell in the primate retina (20), the opponent pupil response we observe to S-cone stimulation seems likely explained by the negative S-cone input to ipRGCs.…”

Section: Discussionmentioning

confidence: 85%

Opponent melanopsin and S-cone signals in the human pupillary light response

Spitschan¹,

Jain

Brainard³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

169

184

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In the human, cone photoreceptors (L, M, and S) and the melanopsincontaining, intrinsically photosensitive retinal ganglion cells (ipRGCs) are active at daytime light intensities. Signals from cones are combined both additively and in opposition to create the perception of overall light and color. Similar mechanisms seem to be at work in the control of the pupil's response to light. Uncharacterized however, is the relative contribution of melanopsin and S cones, with their overlapping, short-wavelength spectral sensitivities. We measured the response of the human pupil to the separate stimulation of the cones and melanopsin at a range of temporal frequencies under photopic conditions. The S-cone and melanopsin photoreceptor channels were found to be low-pass, in contrast to a band-pass response of the pupil to L-and M-cone signals. An examination of the phase relationships of the evoked responses revealed that melanopsin signals add with signals from L and M cones but are opposed by signals from S cones in control of the pupil. The opposition of the S cones is revealed in a seemingly paradoxical dilation of the pupil to greater S-cone photon capture. This surprising result is explained by the neurophysiological properties of ipRGCs found in animal studies. Distinct neural pathways process signals originating in cone photoreceptors for visual perception. Luminance pathways combine signals from separate classes of cones synergistically, providing a spectrally broadband indication of the overall light intensity at each location in the retinal image. Red-green and blue-yellow chromatic channels combine signals from separate classes of cones in an opponent (subtractive) fashion, providing sensitivity to the relative spectral content of light and supporting the perception of color independent of luminance (1).A parallel set of pathways contributes to the response of the pupil of the eye to light. Most familiar is a synergistic cone effect that causes the pupil to constrict in response to increased luminance. Illustrating a commonality of principles that characterize neural mechanisms for perception and pupil response, rectified signals from red-green and blue-yellow opponent channels also contribute to the pupil's light response (2-7).Recently, it has been discovered that mammalian retinas contain an additional photoreceptor class that also operates under daylight conditions. Intrinsically photosensitive retinal ganglion cells (ipRGCs) express the photopigment melanopsin, which has a peak spectral sensitivity (480 nm) between that of S and M cones (8, 9). Among other, "non-image-forming" functions of the eye, melanopsin-containing ipRGCs contribute to a delayed and sustained constriction of the pupil (10). Studies in patients with loss of photoreceptor function (11) suggest that melanopsin may also contribute to conscious visual perception.The discovery of an additional photoreceptor class raises the fundamental question of how melanopsin signals are combined with those from the cones. Do melanopsin signals add to con...

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Section: Discussionmentioning

confidence: 85%

Opponent melanopsin and S-cone signals in the human pupillary light response

Spitschan¹,

Jain

Brainard³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

169

184

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“…31 There is still debate in the literature about the existence of Scone OFF bipolar cells, but if they exist they are very sparse. 32,33 Accordingly, as suggested before, 34 the waveform of the OFF-response in ESCS patients and in our NRL-mutant patients (Fig. 6) reflects mainly the recovery of the S-cones from the light stimulus in the absence of S-cone OFF-center bipolar cells.…”

Section: Discussionmentioning

confidence: 99%

Homozygosity for a Recessive Loss-of-Function Mutation of the NRL Gene Is Associated With a Variant of Enhanced S-Cone Syndrome

Newman

Blumen

Braverman

et al. 2016

Invest. Ophthalmol. Vis. Sci.

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Citation: Newman H, Blumen SC, Braverman I, et al. Homozygosity for a recessive loss-of-function mutation of the NRL gene is associated with a variant of enhanced S-cone syndrome. Invest Ophthalmol Vis Sci. 2016;57:5361-5371. DOI:10.1167/ iovs.16-19505 PURPOSE. To investigate the genetic basis for severe visual complaints by Bukharan Jewish patients with oculopharyngeal muscular dystrophy (OPMD). METHODS.Polymerase chain reaction amplification and direct sequencing were used to test for NRL, PABPN1, and NR2E3 mutations. Complete ophthalmic examination included bestcorrected visual acuity, biomicroscopic examination, optical coherence tomography, and fundus autofluorescence. Detailed electroretinography (ERG) testing was conducted including expanded International Society for Clinical Electrophysiology of Vision protocol for light-adapted and dark-adapted conditions, measurements of S-cone function, and ON-OFF light-adapted ERG.RESULTS. The index patients were homozygotes for both a dominant mutation of the PABPN1 gene, (GCN)13, and a recessive mutation of the NRL gene, p.R31X, on chromosome 14q11.1, leading to early-onset OPMD accompanied by night blindness and reduced visual acuity. No mutations were found in the NR2E3 gene. Both patients were of Bukharan Jewish origin, but from unrelated families. Electroretinography responses of both patients were dominated by short-wavelength-sensitive mechanisms, with no detectable rod function, similar to the ERG responses of individuals with enhanced S-cone syndrome (ESCS) due to NR2E3 mutations. Heterozygotes for the PABPN1 and NRL mutations demonstrated normal fundi and ERG responses.CONCLUSIONS. Homozygosity for the recessive NRL mutation described here appears to be associated with a distinct retinal phenotype, demonstrating ERG characteristics similar to those of ESCS patients. This report expands the spectrum of NRL recessive mutations, as well as the genetic spectrum of ESCS, and indicates a new syndrome of OPMD with an ESCS-like phenotype.

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“…Some bipolar cells, depending on the location in the retina, may only contact a specific subset of cone photoreceptors, and as mentioned earlier, can form a ‘private line’. In macaque retina, signals from L and M cones are integrated by the dendrites of ‘diffuse’ and ‘midget’ bipolar cells (Boycott and Wässle, 1999), whereas ‘S cone’ bipolar cells contact exclusively S cone photoreceptors (Dacey, 2000; Dacey et al, 2014; Kouyama and Marshak, 1992; Miyagishima et al, 2014). An S cone selective bipolar cell has also been observed in mouse retina (Haverkamp et al, 2005) and patch-clamp recordings have demonstrated blue ‘ON’ responses from this bipolar cell subtype (Breuninger et al, 2011).…”

Section: Synapse Structure and Connectivity Of Retinal Neuronsmentioning

confidence: 99%

Functional architecture of the retina: Development and disease

Hoon

Okawa

Santina

et al. 2014

Progress in Retinal and Eye Research

457

385

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Structure and function are highly correlated in the vertebrate retina, a sensory tissue that is organized into cell layers with microcircuits working in parallel and together to encode visual information. All vertebrate retinas share a fundamental plan, comprising five major neuronal cell classes with cell body distributions and connectivity arranged in stereotypic patterns. Conserved features in retinal design have enabled detailed analysis and comparisons of structure, connectivity and function across species. Each species, however, can adopt structural and/or functional retinal specializations, implementing variations to the basic design in order to satisfy unique requirements in visual function. Recent advances in molecular tools, imaging and electrophysiological approaches have greatly facilitated identification of the cellular and molecular mechanisms that establish the fundamental organization of the retina and the specializations of its microcircuits during development. Here, we review advances in our understanding of how these mechanisms act to shape structure and function at the single cell level, to coordinate the assembly of cell populations, and to define their specific circuitry. We also highlight how structure is rearranged and function is disrupted in disease, and discuss current approaches to re-establish the intricate functional architecture of the retina.

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Distinct synaptic mechanisms create parallel S-ON and S-OFF color opponent pathways in the primate retina

Cited by 70 publications

References 96 publications

Opponent melanopsin and S-cone signals in the human pupillary light response

Opponent melanopsin and S-cone signals in the human pupillary light response

Homozygosity for a Recessive Loss-of-Function Mutation of the NRL Gene Is Associated With a Variant of Enhanced S-Cone Syndrome

Functional architecture of the retina: Development and disease

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