Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells

1990 ◽  
Vol 4 (1) ◽  
pp. 75-93 ◽  
Author(s):  
Keith Purpura ◽  
Daniel Tranchina ◽  
Ehud Kaplan ◽  
Robert M. Shapley

AbstractThe responses of monkey retinal ganglion cells to sinusoidal stimuli of various temporal frequencies were measured and analyzed at a number of mean light levels. Temporal modulation tuning functions (TMTFs) were measured at each mean level by varying the drift rate of a sine-wave grating of fixed spatial frequency and contrast. The changes seen in ganglion cell temporal responses with changes in adaptation state were similar to those observed in human subjects and in turtle horizontal cells and cones tested with sinusoidally flickering stimuli; “Weber's Law” behavior was seen at low temporal frequencies but not at higher temporal frequencies. Temporal responses were analyzed in two ways: (1) at each light level, the TMTFs were fit by a model consisting of a cascade of low- and high-pass filters; (2) the family of TMTFs collected over a range of light levels for a given cell was fit by a linear negative feedback model in which the gain of the feedback was proportional to the mean light level. Analysis (1) revealed that the temporal responses of one class of monkey ganglion cells (M cells) were more phasic at both photopic and mesopic light levels than the responses of P ganglion cells. In analysis (2), the linear negative feedback model accounted reasonably well for changes in gain and dynamics seen in three P cells and one M cell. From the feedback model, it was possible to estimate the light level at which the dark-adapted gain of the cone pathways in the primate retina fell by a factor of two. This value was two to three orders of magnitude lower than the value estimated from recordings of isolated monkey cones. Thus, while a model which includes a single stage of negative feedback can account for the changes in gain and dynamics associated with light adaptation in the photopic and mesopic ranges of vision, the underlying physical mechanisms are unknown and may involve elements in the primate retina other than the cone.

2016 ◽  
Vol 49 (1) ◽  
pp. 16-32 ◽  
Author(s):  
UC Besenecker ◽  
JD Bullough

Short-wavelength (<500 nm) output of light sources enhances scene brightness perception in the low-to-moderate photopic range. This appears to be partially explained by a contribution from short-wavelength cones. Recent evidence from experiments on humans suggests that intrinsically photosensitive retinal ganglion cells (ipRGCs) containing the photopigment melanopsin might also contribute to spectral sensitivity for scene brightness perception. An experiment was conducted to investigate this possibility at two different light levels, near 10 lx and near 100 lx. Subjects provided forced-choice brightness judgments and relative brightness magnitude judgments when comparing two different amber-coloured stimuli with similar chromaticities. A provisional brightness metric including an ipRGC contribution was able to predict the data with substantially smaller errors than a metric based on cone input only.


Neuron ◽  
2018 ◽  
Vol 100 (1) ◽  
pp. 216-228.e6 ◽  
Author(s):  
Xiaoyang Yao ◽  
Jon Cafaro ◽  
Amanda J. McLaughlin ◽  
Friso R. Postma ◽  
David L. Paul ◽  
...  

2019 ◽  
Author(s):  
Manuel Spitschan

AbstractThe size of the pupil depends on light level. Watson & Yellott (2012) developed a unified formula to predict pupil size from luminance, field diameter, age, and number of eyes. Luminance reflects input from the L and M cones in the retina but ignores the contribution of intrinsically photosensitive retinal ganglion cells (ipRGCs) expressing the photopigment melanopsin, which are known to control the size of the pupil. We discuss the role of melanopsin in controlling pupil size by reanalysing an extant data set. We confirm that melanopsin-weighted quantities, in conjunction with Watson & Yellott’s formula, adequately model intensity-dependent pupil size. We discuss the contributions of other photoreceptors into pupil control.


1992 ◽  
Vol 8 (5) ◽  
pp. 483-486 ◽  
Author(s):  
Ethan A. Benardete ◽  
Ehud Kaplan ◽  
Bruce W. Knight

AbstractPrimate retinal ganglion cells that project to the magnocellular layers of the lateral geniculate nucleus (M) are much more sensitive to luminance contrast than those ganglion cells projecting to the parvocellular layers (P). We now report that increasing contrast modifies the temporal-frequency response of M cells, but not of P cells. With rising contrast, the M cells' responses to sinusoidal stimuli show an increasing attenuation at low temporal frequencies while the P cells' responses scale uniformly. The characteristic features of M-cell dynamics are well described by a model originally developed for the X and Y cells of the cat, where the hypothesized nonlinear feedback mechanism responsible for this behavior has been termed the contrast gain control (Shapley & Victor, 1978, 1981; Victor, 1987, 1988). These data provide further physiological evidence that the M-cell pathway differs from the P-cell pathway with regard to the functional elements in the retina. Furthermore, the similarity in dynamics between primate M cells and cat X and Y retinal ganglion cells suggests the possibility that P cells, being different from either group, are a primate specialization not found in the retinae of lower mammals.


2020 ◽  
Author(s):  
Jared N. Levine ◽  
Gregory W. Schwartz

AbstractIn the mouse, retinal output is computed by over 40 distinct types of retinal ganglion cells (RGCs) (Baden et al., 2016). Determining which of these many RGC types project to a retinorecipient region is a key step in elucidating the role that region plays in visually-mediated behaviors. Combining retrograde viral tracing and single-cell electrophysiology, we identify the RGC types which project to the olivary pretectal nucleus (OPN), a major visual structure. We find that retinal input to the OPN consists of a variety of intrinsically-photosensitive and conventional RGC types, the latter a diverse set of mostly ON RGCs. Surprisingly, while the OPN is most associated with the pupillary light reflex (PLR) pathway, requiring information about absolute luminance, we show that the majority of the retinal input to the OPN is from single cell type which transmits information unrelated to luminance. This ON-transient RGC accounts for two-thirds of the input to the OPN, and responds to small objects across a wide range of speeds. This finding suggests a role for the OPN in visually-mediated behaviors beyond the PLR.Significance statementThe olivary pretectal nucleus is a midbrain structure which receives direct input from retinal ganglion cells (RGC), and modulates pupil diameter in response to changing absolute light level. In the present study, we combine viral tracing and electrophysiology to identify the RGC types which project to the OPN. Surprisingly, the majority of its input comes from a single type which does not encode absolute luminance, but instead responds to small objects across a wide range of speeds. These findings are consistent with a role for the OPN apart from pupil control and suggest future experiments to elucidate its full role in visually-mediated behavior.


2020 ◽  
Author(s):  
Michael D. Flood ◽  
Erika D. Eggers

AbstractAdaptation of ganglion cells to increasing light levels is a crucial property of the retina. The retina must respond to light intensities that vary by 10-12 orders of magnitude, but the dynamic range of ganglion cell responses only covers ~1000 orders of magnitude. Dopamine is a crucial neuromodulator for light adaptation and activates receptors in the D1 family – D1Rs that are expressed on horizontal cells and some bipolar and ganglion cells- and the D2 family – D2Rs that are expressed on dopaminergic amacrine cells and D4Rs that are primarily expressed on photoreceptors. However, how these receptors change the synaptic properties of the inputs to ganglion cells is not yet clear. Here we used single cell retinal patch-clamp recordings from the mouse retina to determine how activating D1Rs and D4Rs changed the light-evoked and spontaneous excitatory inputs to ON-sustained (ON-s) ganglion cells. We found that both D1R and D4R activation decrease the light-evoked excitatory inputs to ON-s ganglion cells, but that only the sum of activating the two receptors was similar to the effect of light adaptation to a rod-saturating background. The largest effects on spontaneous excitatory activity of both D1R and D4R agonists was on the frequency of events, suggesting that D1Rs and D4Rs are acting upstream of the ganglion cells.


1982 ◽  
Vol 48 (4) ◽  
pp. 968-980 ◽  
Author(s):  
G. W. Balkema ◽  
L. H. Pinto

1. The organization of the receptive fields of retinal ganglion cells in te normal mouse was studied qualitatively in recordings from 43 single axons in the optic nerve and optic tract, and the light sensitivity was studied quantitatively in 26 of these cells by measuring incremental sensitivity. 2. The receptive fields of normal animals were elliptical, had concentric center and peripheral subdivisions, and had an antagonistic center/surround organization; the receptive-field centers ranged from 1.95 to 83 degrees in diameter, with a median of 7 degrees. 3. The incremental sensitivity to white light was measured using a criterion response of 10 extra spikes; the most sensitive dark-adapted cell required a stimulus luminance of 3.5 x 10(-3) cd/m2 to generate a criterion response. 4. The action spectrum measured at seven different wavelengths (433-619 nm) from ganglion cells in the normally pigmented mouse resembled the CIE (International Commission on Illumination, CIE 1957 (11)) relative scotopic luminous efficiency function (41) and is consistent with a curve having a peak around 500 nm. 5. On light adaptation with blue light (less than 460 nm), the sensitivity to longer wavelength stimuli increased by 0.2-0.5 log units relative to the sensitivity to the shorter wavelengths; these results are compatible with the presence of a photoreceptor sensitive to long wavelengths in the normally pigmented mouse (C57BL/6J+/+). 6. The organization of the receptive fields of 48 retinal ganglion cells from the hypopigmentation mutant pearl (C57BL/6J-pe) was also studied qualitatively; the receptive field organization was similar to that of the normally pigmented mouse. 7. In 25 cells from dark-adapted pearl mice, the incremental sensitivity to white light was, on the average, 1.6 log units less than that for normal mice. 8. The dark-adapted action spectrum of pearl mice was similar to that of normally pigmented mice. However, a shift in sensitivity to longer wavelengths did not occur on selective light adaptation with the most luminous blue light (less than 460 nm) background that we could produce. 9. We conclude that pearl is one of the mammalian genes that codes for functions that affect dark-adapted retinal sensitivity. The results of this study and past studies suggest that the pearl gene's action on light sensitivity is predominantly within the retina and before (distal to) the ganglion cells.


eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
William N Grimes ◽  
Logan R Graves ◽  
Mathew T Summers ◽  
Fred Rieke

Visual perception across a broad range of light levels is shaped by interactions between rod- and cone-mediated signals. Because responses of retinal ganglion cells, the output cells of the retina, depend on signals from both rod and cone photoreceptors, interactions occurring in retinal circuits provide an opportunity to link the mechanistic operation of parallel pathways and perception. Here we show that rod- and cone-mediated responses interact nonlinearly to control the responses of primate retinal ganglion cells; these nonlinear interactions, surprisingly, were asymmetric, with rod responses strongly suppressing subsequent cone responses but not vice-versa. Human psychophysical experiments revealed a similar perceptual asymmetry. Nonlinear interactions in the retinal output cells were well-predicted by linear summation of kinetically-distinct rod- and cone-mediated signals followed by a synaptic nonlinearity. These experiments thus reveal how a simple mechanism controlling interactions between parallel pathways shapes circuit output and perception.


2021 ◽  
Author(s):  
Allie C. Hexley ◽  
Takuma Morimoto ◽  
Hannah E. Smithson ◽  
Manuel Spitschan

AbstractColour gamuts describe the chromaticity reproduction capabilities of a display, i.e. its ability to reproduce the relative cone excitations from real-world radiance spectra. While the cones dominate “canonical” visual function (i.e. perception of colour, space, and motion) under photopic light levels, they are not the only photoreceptors in the human retina. Rods and melanopsin-containing intrinsically photosensitive retinal ganglion cells (ipRGCs) also respond to light and contribute to both visual and non-visual light responses, including circadian rhythms, sleep-wake control, mood, pupil size, and alertness. Three-primary display technologies, with their focus on reproducing colour, are not designed to reproduce the rod and melanopsin excitations. Moreover, conventional display metrics used to characterize three-primary displays fail to describe the display’s ability (or inability) to reproduce rod and melanopsin excitations, and thus do not capture the display’s ability to reproduce the full human physiological response to light. In this paper, three novel physiologically relevant metrics are proposed for quantifying the reproduction and distortion of the photoreceptor signals by visual displays. A novel equal-luminance photoreceptor excitation diagram is proposed, extending the well-known MacLeod-Boynton chromaticity diagram, to allow visualizations of the five-dimensional photoreceptor signal space in a three-dimensional projection.


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