Melanopsin Contributions to the Representation of Images in the Early Visual System

Abstract

SummaryMelanopsin photoreception enhances retinal responses to variations in ambient light (irradiance) and drives non-image-forming visual reflexes such as circadian entrainment [1, 2, 3, 4, 5, 6]. Melanopsin signals also reach brain regions responsible for form vision [7, 8, 9], but melanopsin’s contribution, if any, to encoding visual images remains unclear. We addressed this deficit using principles of receptor silent substitution to present images in which visibility for melanopsin versus rods+cones was independently modulated, and we recorded evoked responses in the mouse dorsal lateral geniculate nucleus (dLGN; thalamic relay for cortical vision). Approximately 20% of dLGN units responded to patterns visible only to melanopsin, revealing that melanopsin signals alone can convey spatial information. Spatial receptive fields (RFs) mapped using melanopsin-isolating stimuli had ON centers with diameters ∼13°. Melanopsin and rod+cone responses differed in the temporal domain, and responses to slow changes in radiance (<0.9 Hz) and stationary images were deficient when stimuli were rendered invisible for melanopsin. We employed these data to devise and test a mathematical model of melanopsin’s involvement in form vision and applied it, along with further experimental recordings, to explore melanopsin signals under simulated active view of natural scenes. Our findings reveal that melanopsin enhances the thalamic representation of scenes containing local correlations in radiance, compensating for the high temporal frequency bias of cone vision and the negative correlation between magnitude and frequency for changes in direction of view. Together, these data reveal a distinct melanopsin contribution to encoding visual images, predicting that, under natural view, melanopsin augments the early visual system’s ability to encode patterns over moderate spatial scales.

Pupil responses to hidden photoreceptor–specific modulations in movies

“…However, this study and a recent one [17] employing a similar system find that non-visual responses can be manipulated with a modified VDU with more than three primaries. Additionally, there is more and more evidence that melanopsin contributes to “classical” visual functions such as the perception of brightness [22, 37], colour [9, 38], space (humans: [9]; mice: [39]), and other visual attributes (humans: [24], mice: [40–42]). It remains an interesting question to what extent the classical colour matching functions, which are the basis of our current cone fundamentals, reflect the activity of melanopsin (though the amount of rod contributions have been discussed extensively [43]).…”

The human visual cortex response to melanopsin-directed stimulation is accompanied by a distinct perceptual experience

“…The appearance was curiously unpleasant. 292 The diffuse, even blurry, property of the percept might be related to the broad receptive 293 fields of neurons driven by melanopsin stimulation, 28 consistent with the extensive dendritic 294 arbors of the ipRGCs. 29 In a prior study, subjects reported that lights appear brighter when 295 melanopsin contrast is added to the stimulation of the cone-based luminance channel.…”

“…25 Visual stimuli 26 We used the method of silent substitution with a digital light synthesis engine (OneLight Spec-27 tra) to stimulate targeted photoreceptors. Our device produces stimulus spectra as mixtures 28 Human cortical responses to melanopsin 1/14 of 56 independent,~16 nm full-width half-max primaries under digital control, and can modu- 29 late between these spectra at 256 Hz. Details regarding the device, stimulus generation, and 30 estimates of precision have been previously reported.…”

Light modulates oscillatory alpha activity in the occipital cortex of totally visually blind individuals with intact non-visual photoreception

“…This photic response is then transferred to nonvisual brain areas, including hypothalamic nuclei notably involved in circadian rhythmicity, and sleep-wake regulation 14,15 . IpRGC signals also reaches parts of brain primarily mediating vision, such as the lateral geniculate nucleus of the thalamus 13,15 and studies suggest that ipRGCs contribute to crude vision, brightness detection, and adjustment of rod and cones sensitivities [16][17][18][19][20][21] . Similarly to animal models, many human non-visual responses to light are more sensitive to shorter wavelength (blue) light exposures making them likely to be under ipRGC influence 5,[22][23][24][25][26] .…”

“…Similarly to animal models, many human non-visual responses to light are more sensitive to shorter wavelength (blue) light exposures making them likely to be under ipRGC influence 5,[22][23][24][25][26] . Isolating ipRGCs and melanopsin roles from those of rods, cones and other RGCs can be achieved in animals by knocking down, amplifying, or modifying part of the photoreception system 19,27,28 . The exact role of ipRGCs remains difficult to isolate in humans, however, where specific genotypes perturbing the different parts of the retinal photoreception system are not available.…”