Melanopsin and Cone Photoreceptor Inputs to the Afferent Pupil Light Response

Zele, Andrew J.; Adhikari, Prakash; Cao, Dingcai; Feigl, Beatrix

doi:10.3389/fneur.2019.00529

Cited by 44 publications

(38 citation statements)

References 55 publications

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“…In the current study, we find that melanopsin and cone signals are combined approximately additively in control of the pupil, consistent with prior reports 24,37 .…”

Section: Distinct Iprgc Classessupporting

confidence: 93%

“…The Minkowski exponent for the combination of melanopsin and cone signals in the pupil response is ~0.8, compared to its value of ~1.75 for the discomfort ratings. The value of ~0.8 indicates a combination rule for cone and melanopsin signals that is reasonably close to linear, consistent with prior observations of the additivity of cone and melanopsin signals in the pupil response 24,37 . The fact that the stage 1 parameters differ between the model fits to the two measures indicates that discomfort and pupil control are mediated by mechanisms that combine signals from melanopsin and the cones in different ways.…”

Section: Migraine Groups Do Not Have Enhanced Pupil Responses Indicasupporting

confidence: 86%

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Selective amplification of ipRGC signals accounts for interictal photophobia in migraine

McAdams

Kaiser

Igdalova

et al. 2020

Preprint

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Second only to headache, photophobia is the most debilitating symptom reported by people with migraine. While the melanopsin-containing, intrinsically photosensitive retinal ganglion cells (ipRGCs) are thought to play a role, how cone and melanopsin signals are integrated in this pathway to produce visual discomfort is poorly understood.We studied 60 people: 20 without headache and 20 each with interictal photophobia from migraine with or without aura. Participants viewed pulses of spectral change that selectively targeted melanopsin, the cones, or both, and rated the degree of visual discomfort produced by these stimuli while we also recorded pupil responses.We examined the data within a model that describes how cone and melanopsin signals are weighted and combined at the level of the retina, and how this combined signal is transformed into a rating of discomfort or pupil response. Our results indicate that people with migraine do not differ from headache-free controls in the manner in which melanopsin and cone signals are combined. Instead, people with migraine demonstrate an amplification of integrated ipRGC signals for discomfort.This effect of migraine is selective for ratings of visual discomfort, in that an amplification of pupil responses was not seen in the migraine group, nor were group differences found in surveys of other behaviors putatively linked to ipRGC function (chronotype, seasonal sensitivity, presence of a photic sneeze reflex).By revealing a dissociation in the amplification of discomfort versus pupil response, our findings suggest a post-retinal alteration in processing of ipRGC signals for photophobia in migraine. SignificanceThe melanopsin-containing, intrinsically photosensitive retinal ganglion cells (ipRGCs) may contribute to photophobia in migraine. We measured visual discomfort and pupil responses to cone and melanopsin stimulation-the photoreceptor inputs to the ipRGCs-in people with and without migraine. We find that people with migraine do not differ from those without headaches in how cone and melanopsin signals are weighted and combined to produce visual discomfort.Instead, migraine is associated with an amplification of ipRGC signals for discomfort. This effect of migraine upon ipRGC signals is limited to photophobia, as we did not find an enhancement of pupil responses or a change in other behaviors linked to ipRGC function. Our findings suggest a post-retinal amplification of ipRGC signals for photophobia in migraine.

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“…In the current study, we find that melanopsin and cone signals are combined approximately additively in control of the pupil, consistent with prior reports 24,37 .…”

Section: Distinct Iprgc Classessupporting

confidence: 93%

Section: Migraine Groups Do Not Have Enhanced Pupil Responses Indicasupporting

confidence: 86%

Selective amplification of ipRGC signals accounts for interictal photophobia in migraine

McAdams

Kaiser

Igdalova

et al. 2020

Preprint

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“…The proportion varies with stimulus intensity, spectral distribution and change over exposure time. Classical outer photoreceptors mediate the transient pupil constriction 5 whereby an intrinsic melanopsin activation of ipRGCs 28,73,74 mainly drives the sustained photopic adapted pupil response. All receptor signals contribute complementary 75 to the afferent pupil constriction control path with varied proportions until a steady-state of equilibrium is reached, in which the melanopsin activated ipRGC signals are dominating.…”

mentioning

confidence: 99%

Prediction accuracy of L- and M-cone based human pupil light models

Zandi

Klabes

Khanh

2020

Sci Rep

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Multi-channel LED luminaires offer a powerful tool to vary retinal receptor signals while keeping visual parameters such as color or brightness perception constant. This technology could provide new fields of application in indoor lighting since the spectrum can be enhanced individually to the users' favor or task. One possible application would be to optimize a light spectrum by using the pupil diameter as a parameter to increase the visual acuity. A spectral-and time-dependent pupil model is the key requirement for this aim. We benchmarked in our work selected Land M-cone based pupil models to find the estimation error in predicting the pupil diameter for chromatic and polychromatic spectra at 100 cd/m 2. We report an increased estimation error up to 1.21 mm for 450 nm at 60-300 s exposure time. At short exposure times, the pupil diameter was approximately independent of the used spectrum, allowing to use the luminance for a pupil model. Polychromatic spectra along the Planckian locus showed at 60-300 s exposure time, a prediction error within a tolerance range of ± 0.5 mm. The time dependency seems to be more essential than the spectral dependency when using polychromatic spectra. The pupil aperture is an essential factor in photometric and visual investigations because of its direct influence on both retinal illumination and the retinal image quality 1. A smaller pupil diameter can ensure a larger depth of field 2 and achieve a decrease of optical aberrations 3,4 , which has positive effects on the visual acuity of the eye 4,5. Visual acuity is relevant in the interior lighting of workplaces or production facilities since an enhanced visual performance leads to fewer accidents or human injuries 6. Various studies have shown that the optimal pupil diameter is approximately between two and three millimeters for visual tasks in the photopic luminance range 1,4,7-11. With today's technology of multi-channel LED luminaires, it is possible to optimize artificial light spectra to influence the pupil aperture, color perception, brightness perception or other lighting metrics 12,13. The number of narrow-band light-emitting diodes in such a system determines the degree of freedom, which allows keeping specific parameters constant while changing others. The first step to actively optimize the pupil aperture through illumination without influencing other image-forming vision parameters such as brightness or color perception is the construction of an accurate model which predicts the spectral and time-dependent pupil diameter. Such a model can be used in a heuristic or gradient-based optimization procedure as an objective or constraint function to design the desired light spectrum for visual tasks. Eight empirical models are proposed in the literature with different dependent parameters and test conditions. The most famous models are from Holladay 14 , Crawford 15 , Moon and Spencer 16 , De Groot and Gebhard 17 , Stanley and Davies 18 , Barten 19 and Blackie and Howland 20. In 2012, Watson and Yellot 21 reviewed these pup...

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“… 70 No activity attributed to S-cones after light offset appears to be prolonged, neither spikes recorded from the olivary pretectal nucleus of mice lacking melanopsin nor human pupillary constriction using a silent substitution paradigm. 68 , 71 Therefore, the enhanced pupillary constriction and slower post-stimulus redilation resulting from repeated short-wavelength stimulation seems more likely due to changes in the melanopsin-driven pathway than in S-cone inputs. This discussion assumes that the source of the adaptation in pupillary responses to multiple short-wavelength light exposures is local at the retinal level, but adaptation at the level of the olivary pretectal nucleus cannot be ruled out.…”

Section: Discussionmentioning

confidence: 99%

The Effect of Refractive Error on Melanopsin-Driven Pupillary Responses

Mutti

Mulvihill²,

Orr

et al. 2020

Invest. Ophthalmol. Vis. Sci.

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Purpose Human and animal studies suggest that light-mediated dopamine release may underlie the protective effect of time outdoors on myopia development. Melanopsin-containing retinal ganglion cells may be involved in this process by integrating ambient light exposure and regulating retinal dopamine levels. The study evaluates this potential involvement by examining whether melanopsin-driven pupillary responses are associated with adult refractive error. Methods Subjects were 45 young adults (73% female, 24.1 ± 1.8 years) with refractive errors ranging from –6.33 D to +1.70 D. The RAPDx (Konan Medical) pupillometer measured normalized pupillary responses to three forms of square-wave light pulses alternating with darkness at 0.1 Hz: alternating long wavelength (red, peak at 608 nm) and short wavelength (blue, peak at 448 nm), followed by red only and then blue only. Results Non-myopic subjects displayed greater pupillary constriction in the blue-only condition and slower redilation following blue light offset than subjects with myopia ( P = 0.011). Pupillary responses were not significantly different between myopic and non-myopic subjects in the red-only condition ( P = 0.15). More hyperopic/less myopic refractive error as a continuous variable was linearly related to larger increases in pupillary constriction in response to blue-only stimuli ( r = 0.48, P = 0.001). Conclusions Repeated light exposures to blue test stimuli resulted in an adaptation in the pupillary response (more constriction and slower redilation), presumably due to increased melanopsin-mediated input in more hyperopic/less myopic adults. This adaptive property supports a possible role for these ganglion cells in the protective effects of time outdoors on myopia development.

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Melanopsin and Cone Photoreceptor Inputs to the Afferent Pupil Light Response

Cited by 44 publications

References 55 publications

Selective amplification of ipRGC signals accounts for interictal photophobia in migraine

Selective amplification of ipRGC signals accounts for interictal photophobia in migraine

Prediction accuracy of L- and M-cone based human pupil light models

The Effect of Refractive Error on Melanopsin-Driven Pupillary Responses

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