Melanopsin photoreception contributes to human visual detection, temporal and colour processing

The visual consequences of melanopsin photoreception in humans are not well understood. Here we studied melanopsin photoreception using a technique of photoreceptor silent substitution with five calibrated spectral lights after minimising the effects of individual differences in optical pre-receptoral filtering and desensitising penumbral cones in the shadow of retinal blood vessels. We demonstrate that putative melanopsin-mediated image-forming vision corresponds to an opponent S-OFF L + M-ON response property, with an average temporal resolution up to approximately 5 Hz, and >10x higher thresholds than red-green colour vision. With a capacity for signalling colour and integrating slowly changing lights, melanopsin-expressing intrinsically photosensitive retinal ganglion cells maybe the fifth photoreceptor type for peripheral vision.

[1]  Riccardo Storchi,et al.  Melanopsin Contributions to the Representation of Images in the Early Visual System , 2017, Current Biology.

[2]  Dingcai Cao,et al.  Contributions of rhodopsin, cone opsins, and melanopsin to postreceptoral pathways inferred from natural image statistics. , 2014, Journal of the Optical Society of America. A, Optics, image science, and vision.

[3]  V C Smith,et al.  Evaluation of single-pigment shift model of anomalous trichromacy. , 1977, Journal of the Optical Society of America.

[4]  Andrew J. Zele,et al.  Melanopsin-Expressing Intrinsically Photosensitive Retinal Ganglion Cells in Retinal Disease , 2014, Optometry and vision science : official publication of the American Academy of Optometry.

[5]  D. H. Kelly.  Sine waves and flicker fusion , 2004, Documenta Ophthalmologica.

[6]  Joel Pokorny,et al.  Sequential processing in vision: The interaction of sensitivity regulation and temporal dynamics , 2008, Vision Research.

[7]  Annette E. Allen,et al.  Melanopsin-Based Brightness Discrimination in Mice and Humans , 2012, Current Biology.

[8]  Dingcai Cao,et al.  Cone and melanopsin contributions to human brightness estimation. , 2018, Journal of the Optical Society of America. A, Optics, image science, and vision.

[9]  A V Hill,et al.  The nature of oxyhæmoglobin, with a note on its molecular weight , 1910, The Journal of physiology.

[10]  D. L. Adams,et al.  Shadows Cast by Retinal Blood Vessels Mapped in Primary Visual Cortex , 2002, Science.

[11]  Dingcai Cao,et al.  A five-primary photostimulator suitable for studying intrinsically photosensitive retinal ganglion cell functions in humans. , 2015, Journal of vision.

[12]  J. Pokorny,et al.  Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm , 1975, Vision Research.

[13]  Manuel Spitschan,et al.  The human visual cortex response to melanopsin-directed stimulation is accompanied by a distinct perceptual experience , 2017, Proceedings of the National Academy of Sciences.

[14]  K. Yau,et al.  Photon capture and signalling by melanopsin retinal ganglion cells , 2008, Nature.

[15]  M. Moseley,et al.  Short-Wavelength Light Sensitivity of Circadian, Pupillary, and Visual Awareness in Humans Lacking an Outer Retina , 2007, Current Biology.

[16]  Joel Pokorny,et al.  Photostimulator allowing independent control of rods and the three cone types , 2004, Visual Neuroscience.

[17]  C. Cierpka,et al.  Particle imaging techniques for volumetric three-component (3D3C) velocity measurements in microfluidics , 2011, Journal of Visualization.

[18]  Andrew J. Zele,et al.  The Post-Illumination Pupil Response (PIPR). , 2015, Investigative ophthalmology & visual science.

[19]  Kwoon Y. Wong,et al.  Synaptic influences on rat ganglion‐cell photoreceptors , 2007, The Journal of physiology.

[20]  A. Hill,et al.  The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves , 1910 .

[21]  Thomas Young,et al.  On the theory of light and colours , 1967 .

[22]  D. Berson,et al.  Phototransduction by Retinal Ganglion Cells That Set the Circadian Clock , 2002, Science.

[23]  D. Snodderly,et al.  Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis) , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Andrew J. Zele,et al.  The Circadian Response of Intrinsically Photosensitive Retinal Ganglion Cells , 2011, PloS one.

[25]  Qasim Zaidi,et al.  The effects of prolonged temporal modulation on the differential response of color mechanisms , 1992, Vision Research.

[26]  Victoria Revell,et al.  A “Melanopic” Spectral Efficiency Function Predicts the Sensitivity of Melanopsin Photoreceptors to Polychromatic Lights , 2011, Journal of biological rhythms.

[27]  Paul D. Gamlin,et al.  Primate pupillary light reflex: receptive field characteristics of pretectal luminance neurons. , 2003, Journal of neurophysiology.

[28]  K. Yau,et al.  Melanopsin-Containing Retinal Ganglion Cells: Architecture, Projections, and Intrinsic Photosensitivity , 2002, Science.

[29]  Paul D. Gamlin,et al.  Melanopsin‐expressing ganglion cells on macaque and human retinas form two morphologically distinct populations , 2016, The Journal of comparative neurology.

[30]  J. Pokorny,et al.  Human and macaque pupil responses driven by melanopsin-containing retinal ganglion cells , 2007, Vision Research.

[31]  Thomas Young,et al.  II. The Bakerian Lecture. On the theory of light and colours , 1802, Philosophical Transactions of the Royal Society of London.

[32]  P. Walraven.  Fundamental chromaticity diagram with physiological axes , 1999 .

[33]  R. Foster,et al.  Vertebrate ancient opsin and melanopsin: divergent irradiance detectors , 2010, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[34]  Paul R. Martin,et al.  Melanopsin‐expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections , 2019, The Journal of comparative neurology.

[35]  Andrew J. Zele,et al.  Rhodopsin and Melanopsin Contributions to the Early Redilation Phase of the Post-Illumination Pupil Response (PIPR) , 2016, PloS one.

[36]  H. Spekreijse,et al.  The “silent substitution” method in visual research , 1982, Vision Research.

[37]  Andrew J. Zele,et al.  Correlated and uncorrelated invisible temporal white noise alters mesopic rod signaling. , 2016, Journal of the Optical Society of America. A, Optics, image science, and vision.

[38]  Andrew J. Zele,et al.  A Temporal White Noise Analysis for Extracting the Impulse Response Function of the Human Electroretinogram , 2017, Translational vision science & technology.

[39]  Satchidananda Panda,et al.  Melanopsin Contributions to Irradiance Coding in the Thalamo-Cortical Visual System , 2010, PLoS biology.

[40]  Joel Pokorny,et al.  The design and use of a cone chromaticity space: A tutorial , 1996 .

[41]  D. Brainard,et al.  Opponent melanopsin and S-cone signals in the human pupillary light response , 2014, Proceedings of the National Academy of Sciences.

[42]  Glen T. Prusky,et al.  Melanopsin-Expressing Retinal Ganglion-Cell Photoreceptors: Cellular Diversity and Role in Pattern Vision , 2010, Neuron.

[43]  H. D. L. Dzn,et al.  Experiments on flicker and some calculations on an electrical analogue of the foveal systems , 1952 .

[44]  J. Pokorny,et al.  Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN , 2005, Nature.

[45]  J. Mollon.  "Tho' she kneel'd in that place where they grew..." The uses and origins of primate colour vision. , 1989, The Journal of experimental biology.

[46]  Joel Pokorny,et al.  Rod contributions to color perception: Linear with rod contrast , 2007, Vision Research.

[47]  V C Smith,et al.  Cone-rod receptor spaces with illustrations that use CRT phosphor and light-emitting-diode spectra. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[48]  B. Wandell,et al.  Human trichromacy revisited , 2012, Proceedings of the National Academy of Sciences.

[49]  D. Brainard,et al.  Selective Stimulation of Penumbral Cones Reveals Perception in the Shadow of Retinal Blood Vessels , 2015, PloS one.