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Melanopsin- and L-cone-induced pupil constriction is inhibited by S- and M-cones in humans.

ABSTRACT: The human retina contains five photoreceptor types: rods; short (S)-, mid (M)-, and long (L)-wavelength-sensitive cones; and melanopsin-expressing ganglion cells. Recently, it has been shown that selective increments in M-cone activation are paradoxically perceived as brightness decrements, as opposed to L-cone increments. Here we show that similar effects are also observed in the pupillary light response, whereby M-cone or S-cone increments lead to pupil dilation whereas L-cone or melanopic illuminance increments resulted in pupil constriction. Additionally, intermittent photoreceptor activation increased pupil constriction over a 30-min interval. Modulation of L-cone or melanopic illuminance within the 0.25-4-Hz frequency range resulted in more sustained pupillary constriction than light of constant intensity. Opposite results were found for S-cone and M-cone modulations (2 Hz), mirroring the dichotomy observed in the transient responses. The transient and sustained pupillary light responses therefore suggest that S- and M-cones provide inhibitory input to the pupillary control system when selectively activated, whereas L-cones and melanopsin response fulfill an excitatory role. These findings provide insight into functional networks in the human retina and the effect of color-coding in nonvisual responses to light, and imply that nonvisual and visual brightness discrimination may share a common pathway that starts in the retina.

SUBMITTER: Woelders T

PROVIDER: S-EPMC5789936 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundIntrinsically photosensitive retinal ganglion cells (ipRGCs) drive an array of non-image-forming (NIF) visual responses including circadian photoentrainment and the pupil light reflex. ipRGCs integrate extrinsic (rod/cone) and intrinsic (melanopsin) photoreceptive signals, but the contribution of cones to ipRGC-dependent responses remains incompletely understood. Given recent data revealing that cone-derived colour signals influence mouse circadian timing and pupil responses in humans, here we set out to investigate the role of colour information in pupil control in mice.ResultsWe first recorded electrophysiological activity from the pretectal olivary nucleus (PON) of anaesthetised mice with a red-shifted cone population (Opn1mwR) and mice lacking functional cones (Cnga3-/-) or melanopsin (Opn1mwR; Opn4-/-). Using multispectral stimuli to selectively modulate the activity of individual opsin classes, we show that PON cells which receive ipRGC input also exhibit robust S- and/or L-cone opsin-driven activity. This population includes many cells where the two cone opsins drive opponent responses (most commonly excitatory/ON responses to S-opsin stimulation and inhibitory/OFF responses to L-opsin stimulation). These cone inputs reliably tracked even slow (0.025 Hz) changes in illuminance/colour under photopic conditions with melanopsin contributions becoming increasingly dominant for higher-contrast/lower temporal frequency stimuli. We also evaluated consensual pupil responses in awake animals and show that, surprisingly, this aspect of physiology is insensitive to chromatic signals originating with cones. Instead, by contrast with the situation in humans, signals from melanopsin and both cone opsins combine in a purely additive manner to drive pupil constriction in mice.ConclusionOur data reveal a key difference in the sensory control of the mouse pupil relative to another major target of ipRGCs-the circadian clock. Whereas the latter uses colour information to help estimate time of day, the mouse pupil instead sums signals across cone opsin classes to provide broadband spectral sensitivity to changes in illumination. As such, while the widespread co-occurrence of chromatic responses and melanopsin input in the PON supports a close association between colour discrimination mechanisms and NIF visual processing, our data suggest that colour opponent PON cells in the mouse contribute to functions other than pupil control.

Project description:Signals from cones are recombined in postreceptoral channels [luminance, L + M; red-green, L - M; blue-yellow, S - (L + M)]. The melanopsin-containing retinal ganglion cells are also active at daytime light levels and recent psychophysical results suggest that melanopsin contributes to conscious vision in humans. Here, we measured BOLD fMRI responses to spectral modulations that separately targeted the postreceptoral cone channels and melanopsin. Responses to spatially uniform (27.5° field size, central 5° obscured) flicker at 0.5, 1, 2, 4, 8, 16, 32, and 64 Hz were recorded from areas V1, V2/V3, motion-sensitive area MT, and the lateral occipital complex. In V1 and V2/V3, higher temporal sensitivity was observed to L + M + S (16 Hz) compared with L - M flicker (8 Hz), consistent with psychophysical findings. Area MT was most sensitive to rapid (32 Hz) flicker of either L + M + S or L - M. We found S cone responses only in areas V1 and V2/V3 (peak frequency: 4-8 Hz). In addition, we studied an L + M modulation and found responses that were effectively identical at all temporal frequencies to those recorded for the L + M + S modulation. Finally, we measured the cortical response to melanopsin-directed flicker and compared this response with control modulations that addressed stimulus imprecision and the possibility of stimulation of cones in the shadow of retinal blood vessels (penumbral cones). For our stimulus conditions, melanopsin flicker did not elicit a cortical response exceeding that of the control modulations. We note that failure to control for penumbral cone stimulation could be mistaken for a melanopsin response.The retina contains cone photoreceptors and ganglion cells that contain the photopigment melanopsin. Cones provide brightness and color signals to visual cortex. Melanopsin influences circadian rhythm and the pupil, but its contribution to cortex and perception is less clear. We measured the response of human visual cortex with fMRI using spectral modulations tailored to stimulate the cones and melanopsin separately. We found that cortical responses to cone signals vary systematically across visual areas. Differences in temporal sensitivity for achromatic, red-green, and blue-yellow stimuli generally reflect the known perceptual properties of vision. We found that melanopsin signals do not produce a measurable response in visual cortex at temporal frequencies between 0.5 and 64 Hz at daytime light levels.

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Melanopsin- and L-cone-induced pupil constriction is inhibited by S- and M-cones in humans.

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