Phosphenes, retinal discrete dark noise, negative afterimages and retinogeniculate projections: A new explanatory framework based on endogenous ocular luminescence

Progress in Retinal and Eye Research - Tập 60 - Trang 101-119 - 2017
Vahid Salari1, Felix Scholkmann2,3, Ram Lakhan Pandey Vimal4, Noémi Császár5,6, Mehdi Aslani1, István Bókkon4,5
1Department of Physics, Isfahan University of Technology, Isfahan 84156-83111, Iran
2Biomedical Optics Research Laboratory, Department of Neonatology, University Hospital Zurich, University of Zurich, 8091, Zurich, Switzerland
3Research Office for Complex Physical and Biological Systems, 8038 Zurich, Switzerland
4Vision Research Institute, 25 Rita Street, Lowell, MA 01854, USA
5Psychoszomatic Outpatient Department, Montevideo 5, H-1037, Budapest, Hungary
6Gaspar Karoly University Psychological Institute, H-1091 Budapest, Hungary

Tài liệu tham khảo

Ackman, 2012, Retinal waves coordinate patterned activity throughout the developing visual system, Nature, 490, 219, 10.1038/nature11529 Agte, 2011, Müller glial cell-provided cellular light guidance through the vital Guinea-pig retina, Biophys. J., 101, 2611, 10.1016/j.bpj.2011.09.062 Ala-Laurila, 2004, Thermal activation and photoactivation of visual pigments, Biophys. J., 86, 3653, 10.1529/biophysj.103.035626 Albertini, 1998, Monitoring of low density lipoprotein oxidation by low-level chemiluminescence, Free Radic. Res., 29, 75, 10.1080/10715769800300091 Albertini, 1999, Mechanistic aspects of the relationship between low-level chemilumines- cence and lipidperoxides in oxidation of low-density lipoprotein, FEBS Lett., 459, 47, 10.1016/S0014-5793(99)01217-X Ashtari, 2014, fMRI of retina-originated phosphenes experienced by patients with Leber congenital amaurosis, PLoS One, 9, e86068, 10.1371/journal.pone.0086068 Assali, 2014, Activity dependent mechanisms of visual map formation–from retinal waves to molecular regulators, Semin. Cell Dev. Biol., 35, 136, 10.1016/j.semcdb.2014.08.008 Augustin, 2008, The physiology of scotopic vision, contrast vision, color vision, and circadian rhythmicity: can these parameters be influenced by blue-light-filter lenses?, Retina, 28, 1179, 10.1097/IAE.0b013e3181835885 Auld, 2003, Glial cells and neurotransmission: an inclusive view of synaptic function, Neuron, 40, 389, 10.1016/S0896-6273(03)00607-X Autrum, 1943, Über kleinste Reize bei Sinnesorganen, Biol. Zentralblatt, 66, 209 Baker, 1991, Direct observation of singlet oxygen phosphorescence at 1270 nm from L1210 leukemia cells exposed to polyporphyrin and light, Arch. Biochem. Biophys., 286, 70, 10.1016/0003-9861(91)90009-8 Barlow, 1956, Retinal noise and absolute threshold, J. Opt. Soc. Am., 46, 634, 10.1364/JOSA.46.000634 Barlow, 1993, On the molecular origin of photoreceptor noise, Nature, 366, 64, 10.1038/366064a0 Barrionuevo, 2014, Contributions of rhodopsin, cone opsins, and melanopsin to postreceptoral pathways inferred from natural image statistics, J. Opt. Soc. Am. A. Opt. Image Sci. Vis., 31, A131, 10.1364/JOSAA.31.00A131 Baylor, 1979, Responses of retinal rods to single photons, J. Physiol., 288, 613, 10.1113/jphysiol.1979.sp012716 Baylor, 1980, Two components of electrical dark noise in toad retinal rod outer segments, J. Physiol., 309, 591, 10.1113/jphysiol.1980.sp013529 Birge, 1995, On the molecular origins of thermal noise in vertebrate and invertebrate photoreceptors, Biophys. Chem., 55, 115, 10.1016/0301-4622(94)00145-A Blake, 2011, Biophoton emissions from cell cultures: biochemical evidence for the plasma membrane as the primary source, Gen. Physiol. Biophys., 30, 301 Bókkon, 2008, Phosphene phenomenon: a new concept, BioSystems, 92, 168, 10.1016/j.biosystems.2008.02.002 Bókkon, 2009, Retinal phosphenes and discrete dark noises in rods: a new biophysical framework, J. Photochem. Photobiol. B Biol., 96, 255, 10.1016/j.jphotobiol.2009.07.002 Bókkon, 2013, Theoretical implications on (color) visual representation and cytochrome oxidase blobs, Activ. Nerv. Super., 55, 15, 10.1007/BF03379594 Bókkon, 2010, Estimation of the number of biophotons involved in the visual perception of a single-object image: biophoton intensity can be considerably higher inside cells than outside, J. Photochem. Photobiol. B Biol., 100, 160, 10.1016/j.jphotobiol.2010.06.001 Bókkon, 2011, Visible light induced ocular delayed bioluminescence as a possible origin of negative afterimage. Journal of photochemistry and photobiology, B. Biol., 103, 192 Bókkon, 2016, Endogenous spontaneous ultra-weak photon emission in the formation of eye-specific retinogeniculate projections before birth, Rev. Neurosci., 27, 411, 10.1515/revneuro-2015-0051 Boulland, 2002, Cell-specific expression of the glutamine transporter SN1 suggests differences in dependence on the glutamine cycle, Eur. J. Neurosci., 15, 1615, 10.1046/j.1460-9568.2002.01995.x Bouman, 1961, History and present status of quantum theory of vision, 377 Boveris, 1980, Low-level chemiluminescence of lipoxy, Photochem. Photobiophys., 1, 175 Brandstätter, 1998, Diversity of glutamate receptors in the mammalian retina, Vis. Res., 38, 1385, 10.1016/S0042-6989(97)00176-4 Brennan, 2009, NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation, Nat. Neurosci., 12, 857, 10.1038/nn.2334 Brigatti, 2005, Reproducibility of self-measured intraocular pressure with the phosphene tonometer in patients with ocular hypertension and early to advanced glaucoma, J. Glaucoma, 14, 36, 10.1097/01.ijg.0000146374.59119.42 Brindley, 1962, Two new properties of foveal afterimages and a photochemical hypothesis to explain them, J. Physiol. Lond., 164, 168, 10.1113/jphysiol.1962.sp007011 Brindley, 1968, The sensations produced by electrical stimulation of the visual cortex, J. Physiol., 196, 479, 10.1113/jphysiol.1968.sp008519 Bringmann, 2009, Role of retinal glial cells in neurotransmitter uptake and metabolism, Neurochem. Int., 54, 143, 10.1016/j.neuint.2008.10.014 Bringmann, 2013, GABA and glutamate uptake and metabolism in retinal glial (Müller) cells, Front. Endocrinol. (Lausanne), 4, 48, 10.3389/fendo.2013.00048 Brown, 1964, Visual pigments in single rods and cones of the human retina. Direct measurements reveal mechanisms of human night and color vision, Science, 144, 45, 10.1126/science.144.3614.45 Burbridge, 2014, Visual circuit development requires patterned activity mediated by retinal acetylcholine receptors, Neuron, 84, 1049, 10.1016/j.neuron.2014.10.051 Burgos, 2016, Tracking biochemical changes correlated with ultra-weak photon emission using metabolomics, J. Photochem. Photobiol. B. Biol., 163, 237, 10.1016/j.jphotobiol.2016.08.030 Busse, 1996, vol. 4, 159 Catalá, 2006, An overview of lipid peroxidation with emphasis in outer segments of photoreceptors and the chemiluminescence assay, Int. J. Biochem. Cell Biol., 38, 1482, 10.1016/j.biocel.2006.02.010 Cervetto, 2007, Cellular mechanisms underlying the pharmacological induction of phosphenes, Br. J. Pharmacol., 150, 383, 10.1038/sj.bjp.0706998 Chalupa, 2007, A reassessment of the role of activity in the formation of eye-specific retinogeniculate projections, Brain Res. Rev., 55, 228, 10.1016/j.brainresrev.2007.03.003 Chalupa, 2009, Retinal waves are unlikely to instruct the formation of eye-specific retinogeniculate projections, Neural. Dev., 4, 25, 10.1186/1749-8104-4-25 Chan, 2011, In vivo retinotopic mapping of superior colliculus using manganese-enhanced magnetic resonance imaging, Neuroimage, 54, 389, 10.1016/j.neuroimage.2010.07.015 Chang, 2008, Localization and functional mapping of AMPA receptor subunits in the developing rabbit retina, Invest. Ophthalmol. Vis. Sci., 49, 5619, 10.1167/iovs.07-1565 Chang, 2010, Visual experience-independent functional expression of NMDA receptors in the developing rabbit retina, Invest. Ophthalmol. Vis. Sci., 51, 2744, 10.1167/iovs.09-4217 Cifra, 2014, Ultra-weak photon emission from biological samples: definition, mechanisms, properties, detection and applications, J. Photochem. Photobiol. B. Biol., 139, 2, 10.1016/j.jphotobiol.2014.02.009 Cowey, 2000, Magnetically induced phosphenes in sighted, blind and blindsighted observers, Neuroreport, 11, 3269, 10.1097/00001756-200009280-00044 Craik, 1940, Origin of afterimages, Nature, 148, 512, 10.1038/145512a0 Crowley, 2000, Early development of ocular dominance columns, Science, 290, 1321, 10.1126/science.290.5495.1321 Császár, 2016, Phosphene perception is due to the ultra-weak photon emission produced in various parts of the visual system: glutamate in the focus, Rev. Neurosci., 27, 291, 10.1515/revneuro-2015-0039 Davis, 1976, Movement phosphenes in optic neuritis: a new clinical sign, Neurology, 26, 1100, 10.1212/WNL.26.11.1100 de Melo Reis, 2008, Müller glia as an active compartment modulating nervous activity in the vertebrate retina: neurotransmitters and trophic factors, Neurochem. Res., 33, 1466, 10.1007/s11064-008-9604-1 De Valois, 1990 Devaraj, 1991, Ultraweak light emission from rat liver Nuclei, Photochem. Photobiol., 54, 289, 10.1111/j.1751-1097.1991.tb02018.x Do, 2010, Intrinsically photosensitive retinal ganglion cells, Physiol. Rev., 90, 1547, 10.1152/physrev.00013.2010 Do, 2009, Photon capture and signalling by melanopsin retinal ganglion cells, Nature, 457, 281, 10.1038/nature07682 Dotta, 2012, Increased photon emission from the head while imagining light in the dark is correlated with changes in electroencephalographic power: support for Bokkon's Biophoton Hypothesis, Neurosci. Lett., 513, 151, 10.1016/j.neulet.2012.02.021 Dreher, 1998, Müller cell endfeet at the inner surface of the retina: light microscopy, Vis. Neurosci., 1, 169, 10.1017/S0952523800001449 Emmert, 1881, Größenverhältnisse der Nachbilder, Klin. Monatsblatter Augenheilkd. Augenarztl. Fortbild., 19, 443 Erskine, 2014, Connecting the retina to the brain, ASN Neuro, 6, 10.1177/1759091414562107 Favreau, 1977, Gli effetti consecutivi negativi nella percezione visiva, Le. Sci., 103, 30 Feinbloom, 1939, Quantitative study of the visual-after-image, Am. J. Optom., 16, 199, 10.1097/00006324-193905000-00005 Feldheim, 2010, Visual map development: bidirectional signaling, bifunctional guidance molecules, and competition, Cold Spring Harb. Perspect. Biol., 2, a001768, 10.1101/cshperspect.a001768 Feller, 2009, Retinal waves are likely to instruct the formation of eye-specific retinogeniculate projections, Neural. Dev., 4, 24, 10.1186/1749-8104-4-24 Field, 2005, Retinal processing near absolute threshold: from behavior to mechanism, Annu. Rev. Physiol., 67, 491, 10.1146/annurev.physiol.67.031103.151256 Firsov, 2002, pH and rate of “dark” events in toad retinal rods: test of a hypothesis on the molecular origin of photoreceptor noise, J. Physiol., 539, 837, 10.1113/jphysiol.2001.013207 Fischer, 2001, Müller glia are a potential source of neural regeneration in the postnatal chicken retina, Nat. Neurosci., 4, 247, 10.1038/85090 Fountain, 2002, Before you blame the morphine: visual hallucinations in palliative care, CME Cancer Med., 1, 23 Franze, 2007, Muller cells are living optical fibers in the vertebrate retina, Proc. Natl. Acad. Sci. U. S. A., 104, 8287, 10.1073/pnas.0611180104 Fuglesang, 2006, Phosphenes in low earth orbit: survey responses from 59 astronauts, Aviat. Space Environ. Med., 77, 449 Gjorgjieva, 2011, Modeling developmental patterns of spontaneous activity, Curr. Opin. Neurobiol., 21, 679, 10.1016/j.conb.2011.05.015 Goldsmith, 2006, What birds see, Sci. Am., 295, 69, 10.1038/scientificamerican0706-68 Golstev, 2009, Delayed fluorescence in photosynthesis, Photosynth. Res., 101, 217, 10.1007/s11120-009-9451-1 Gozem, 2012, The molecular mechanism of thermal noise in rod photoreceptors, Science, 337, 1225, 10.1126/science.1220461 Grimes, 2015, A simple retinal mechanism contributes to perceptual interactions between rod- and cone-mediated responses in primates, eLife, 4, e08033, 10.7554/eLife.08033 Grüsser, 1990, On the history of deformation phosphenes and the idea of internal light generated in the eye for the purpose of vision, Doc. Ophthalmol., 74, 57, 10.1007/BF00165665 Güler, 2008, Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision, Nature, 453, 102, 10.1038/nature06829 Guo, 2014, Unusual kinetics of thermal decay of dim-light photoreceptors in vertebrate vision, Proc. Natl. Acad. Sci. U. S. A., 111, 10438, 10.1073/pnas.1410826111 Guo, 2017, Probing the remarkable thermal kinetics of visual rhodopsin with E181Q and S186A mutants, J. Chem. Phys., 146, 215104, 10.1063/1.4984818 Haberecht, 1995, Immature neurons in the rabbit retina are protected against nitric oxide mediated glutamate toxicity, Invest. Ophthalmol. Vis. Sci., 36, S934 Hamon, 2016, Müller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems, Dev. Dyn., 245, 727, 10.1002/dvdy.24375 Hecht, 1942, Energy, quanta, and vision, J. Gen. Physiol., 25, 819, 10.1085/jgp.25.6.819 Hensch, 2004, Critical period regulation, Annu. Rev. Neurosci., 27, 549, 10.1146/annurev.neuro.27.070203.144327 Hering, 1874, Zur Lehre vom Lichtsinn. IV. Ü ber die sogenannte Intensitä t der Lichtempfindung und ü ber die Empfindung des Schwarzen, Sitzungsberichte Kais. Akad. Wiss. Matematisch-Naturwissenschaftliche Cl. Abth. III, 69, 85 Hering, 1878 Hofmann, 2015, Advances in understanding the molecular basis of the first steps in color vision, Prog. Retin. Eye Res., 49, 46, 10.1016/j.preteyeres.2015.07.004 Hofstoetter, 2004, Motion-induced blindness does not affect the formation of negative afterimages, Conscious. Cogn., 13, 691, 10.1016/j.concog.2004.06.007 Holcombe, 2008, The effects of acute intraocular pressure elevation on rat retinal glutamate transport, Acta Ophthalmol. Scand., 86, 408, 10.1111/j.1600-0420.2007.01052.x Huberman, 2008, Mechanisms underlying development of visual maps and receptive fields, Annu. Rev. Neurosci., 31, 479, 10.1146/annurev.neuro.31.060407.125533 Hunt, 2009, Evolution and spectral tuning of visual pigments in birds and mammals, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 364, 2941, 10.1098/rstb.2009.0044 Inayat, 2015, Chemical stimulation of rat retinal neurons: feasibility of an epiretinal neurotransmitter-based prosthesis, J. Neural. Eng., 12, 016010, 10.1088/1741-2560/12/1/016010 Isojima, 1995, Ultraweak biochemiluminescence detected from rat hippocampal slices, Neuroreport, 6, 658, 10.1097/00001756-199503000-00018 Ives, 2014, Ultraweak photon emission as a non-invasive health assessment: a systematic review, PLoS One, 9, e87401, 10.1371/journal.pone.0087401 Jagannathan, 2016, Oxidative stress under ambient and physiological oxygen tension in tissue culture, Curr. Pharmacol. Rep., 2, 64, 10.1007/s40495-016-0050-5 Juliusson, 1994, Complementary cone fields of the rabbit retina, Invest. Ophthalmol. Vis. Sci., 35, 811 Kamal, 2015, Involvement of reactive oxygen species and mitochondrial proteins in biophoton emission in roots of soybean plants under flooding stress, J. Proteom. Res., 14, 2219, 10.1021/acs.jproteome.5b00007 Kapócs, 2017, Possible role of biochemiluminescent photons for lysergic acid diethylamide (LSD)-induced phosphenes and visual hallucinations, Rev. Neurosci., 28, 77, 10.1515/revneuro-2016-0047 Kar, 2012, Transcranial electrical stimulation over visual cortex evokes phosphenes with a retinal origin, J. Neurophysiol., 108, 2173, 10.1152/jn.00505.2012 Kataoka, 2001, Activity-dependent neural tissue oxidation emits intrinsic ultraweak photons, Biochem. Biophys. Res. Commun., 285, 1007, 10.1006/bbrc.2001.5285 Kefalov, 2003, Role of visual pigment properties in rod and cone phototransduction, Nature, 425, 526, 10.1038/nature01992 Kelbsch, 2016, Analysis of retinal function using chromatic pupillography in retinitis pigmentosa and the relationship to electrically evoked phosphene thresholds, Acta Ophthalmol. Khan, 1970, Chemiluminescence arising from simultaneous transitions in pairs of singlet oxygen molecules, J. Am. Chem. Soc., 92, 3293, 10.1021/ja00714a010 Kim, 2005, Spontaneous photon emission and delayed luminescence of two types of human lung cancer tissues: adenocarcinoma and squamous cell carcinoma, Cancer Lett., 229, 283, 10.1016/j.canlet.2005.04.038 Kirchhoff, 1860, On the relation between the radiating and absorbing powers of different bodies for light and heat, Phil. Mag., 20, 1, 10.1080/14786446008642901 Kobayashi, 1999, In vivo imaging of spontaneous ultraweak photon emission from a rat's brain correlated with cerebral energy metabolism and oxidative stress, Neurosci. Res., 34, 103, 10.1016/S0168-0102(99)00040-1 Kojima, 2017, Adaptation of cone pigments found in green rods for scotopic vision through a single amino acid mutation, Proc. Natl. Acad. Sci. U. S. A., 114, 5437, 10.1073/pnas.1620010114 Kukura, 2005, Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman, Science, 310, 1006, 10.1126/science.1118379 Kumar, 2013, Muller glia in retinal innate immunity: a perspective on their roles in endophthalmitis, Crit. Rev. Immunol., 33, 119, 10.1615/CritRevImmunol.2013006618 Kumar, 2016, Possible existence of optical communication channels in the brain, Sci. Rep., 6, 6508, 10.1038/srep36508 Labin, 2010, Retinal glial cells enhance human vision acuity, Phys. Rev. Lett., 104, 158102, 10.1103/PhysRevLett.104.158102 Labin, 2014, Color sorting by retinal waveguides, Opt. Express., 22, 32208, 10.1364/OE.22.032208 Labin, 2014, Müller cells separate between wavelengths to improve day vision with minimal effect upon night vision, Nat. Commun., 5, 4319, 10.1038/ncomms5319 Lack, 1978, Selective attention and the control of binocular rivalry, vol. 11, 117 Lee, 2005 Lee, 2004, Delayed luminescence imaging system and its application, J. Int. Soc. Life Inf. Sci., 22, 445 Lewis-Williams, 1988, The signs of all times: entoptic phenomena in upper palaeolithic art, Curr. Anthropol., 29, 201, 10.1086/203629 Li, 2016, Biophotons contribute to retinal dark noise, Neurosci. Bull., 32, 246, 10.1007/s12264-016-0029-6 Liu, 2009, Thermal decay of rhodopsin: role of hydrogen bonds in thermal isomerization of 11-cis retinal in the binding site and hydrolysis of protonated Schiff base, J. Am. Chem. Soc., 131, 8750, 10.1021/ja903154u Liu, 2011, Thermal properties of rhodopsin: insight into the molecular mechanism of dim-light vision, J. Biol. Chem., 286, 27622, 10.1074/jbc.M111.233312 Loomis, 1972, The photopigment bleaching hypothesis of complementary after-images: a psychophysical test, Vis. Res., 12, 1587, 10.1016/0042-6989(72)90031-4 Lorenz-Fonfria, 2010, Protein fluctuations as the possible origin of the thermal activation of rod photoreceptors in the dark, J. Am. Chem. Soc., 132, 5693, 10.1021/ja907756e Lórenz-Fonfría, 2010, Protein fluctuations as the possible origin of the thermal activation of rod photoreceptors in the dark, J. Am. Chem. Soc., 132, 5693, 10.1021/ja907756e Lukáts, 2005, Photopigment coexpression in mammals: comparative and developmental aspects, Histol. Histopathol., 20, 551 Luo, 2014, A review and update on the current status of retinal prostheses (bionic eye), Br. Med. Bull., 109, 31, 10.1093/bmb/ldu002 Luo, 2011, Activation of visual pigments by light and heat, Science, 332, 1307, 10.1126/science.1200172 MacLeod, 1974, Rod origin of prolonged afterimages, Science, 185, 1171, 10.1126/science.185.4157.1171 Marcus, 1952, Unimolecular dissociations and free radical recombination reactions, J. Chem. Phys., 20, 359, 10.1063/1.1700424 Martinac, 2004, Mechanosensitive ion channels: molecules of mechanotransduction, J. Cell. Sci., 117, 2449, 10.1242/jcs.01232 McLaughlin, 2005, Molecular gradients and development of retinotopic maps, Annu. Rev. Neurosci., 28, 327, 10.1146/annurev.neuro.28.061604.135714 Merabet, 2003, Transcranial magnetic stimulation as an investigative tool in the study of visual function, Optom. Vis. Sci., 80, 356, 10.1097/00006324-200305000-00010 Milder, 1991, Correlation between absorption maxima and thermal isomerization rates in bacteriorhodopsin, Biophys. J., 60, 440, 10.1016/S0006-3495(91)82070-7 Moreno, 2004, Retinal oxidative stress induced by high intraocular pressure, Free Radic. Biol. Med., 37, 803, 10.1016/j.freeradbiomed.2004.06.001 Mrosovsky, 2003, Impaired masking responses to light in melanopsin-knockout mice, Chronobiol. Int., 20, 989, 10.1081/CBI-120026043 Müller, 1930, Über die Farbenempfindungen, Zeitschrift für Psychologie und Physiologie der Sinnesorgane, Ergänzungsband, 17, 1 Nakano, 2005, Low-level chemiluminescence during lipid peroxidations and enzymatic reactions, J. Biolumin. Chemilum., 4, 231, 10.1002/bio.1170040133 Nakano, 1977, Mechanism of chemiluminescence from the linoleate-lipoxygenase system, Arch. Biochem. Biophys., 181, 371, 10.1016/0003-9861(77)90242-9 Nakano, 1976, Spectroscopic evidence for the generation of singlet oxygen in self-reaction of sec-peroxy radicals, J. Am. Chem. Soc., 98, 1974, 10.1021/ja00423a060 Narici, 2009, Radicals excess in the retina: a model for light flashes in space, Radiat. Meas., 44, 203, 10.1016/j.radmeas.2009.01.005 Narici, 2012, Bovine rod rhodopsin. 1. Bleaching by luminescence in vitro by recombination of radicals from polyunsaturated fatty acids, Free Radic. Biol. Med., 53, 482, 10.1016/j.freeradbiomed.2012.05.030 Narici, 2013, Bovine rod rhodopsin: 2. Bleaching in vitro upon 12C ions irradiation as source of effects as light flash for patients and for humans in space, Int. J. Radiat. Biol., 89, 765, 10.3109/09553002.2013.800245 Naycheva, 2012, Phosphene thresholds elicited by transcorneal electrical stimulation in healthy subjects and patients with retinal diseases, Invest. Ophthalmol. Vis. Sci., 53, 7440, 10.1167/iovs.12-9612 Nikonov, 2005, Photoreceptors of Nrl -/- mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms, J. Gen. Physiol., 125, 287, 10.1085/jgp.200409208 Oster, 1970, Phosphenes, Sci. Am., 222, 82, 10.1038/scientificamerican0270-82 Parry, 2002, Visual pigment coexpression in Guinea pig cones: a microspectrophotometric study, Invest. Ophthalmol. Vis. Sci., 43, 1662 Penn, 2001, Early brain wiring: activity-dependent processes, Schizophr. Bull., 27, 337, 10.1093/oxfordjournals.schbul.a006880 Perlman, 1999, Free radical generation following pressure-induced retinal ischemia in the rat, Retina, 19, 255, 10.1097/00006982-199903000-00016 Plataniotis, 2000 Polli, 2010, Conical intersection dynamics of the primary photoisomerization event in vision, Nature, 467, 440, 10.1038/nature09346 Polli, 2014, Wavepacket splitting and two-pathway deactivation in the photoexcited visual pigment isorhodopsin, Angew. Chem. Int. Ed., 53, 2504, 10.1002/anie.201309867 Pospisil, 2014, Role of reactive oxygen species in ultra-weak photon emission in biological systems, J. Photochem. Photobiol. B, 139, 11, 10.1016/j.jphotobiol.2014.02.008 Powell, 2012, Making the incredible credible: afterimages are modulated by contextual edges more than real stimuli, J. Vis., 12 Prasad, 2011, Linoleic acid-induced ultra-weak photon emission from Chlamydomonas reinhardtiias a tool for monitoring of lipid peroxidation in the cell membranes, PLoS One, 6, e22345, 10.1371/journal.pone.0022345 Prasad, 2013, Towards the two-dimensional imaging of spontaneous ultra-weak photon emission from microbial, plant and animal cells, Sci. Rep., 3, 1211, 10.1038/srep01211 Puro, 1996, Activation of NMDA receptor-channels in human retinal Müller glial cells inhibits inward-rectifying potassium currents, Vis. Neurosci., 13, 319, 10.1017/S0952523800007562 Rahnama, 2011, Emission of mitochondrial biophotons and their effect on electrical activity of membrane via microtubules, J. Integr. Neurosci., 10, 65, 10.1142/S0219635211002622 Récasens, 2007, Metabotropic glutamate receptors as drug targets, Curr. Drug. Targets, 8, 651, 10.2174/138945007780618544 Reichenbach, 2010 Reichenbach, 2013, New functions of Müller cells, Glia, 61, 651, 10.1002/glia.22477 Reichenbach, 1995, Phylogenetic constraints on retinal organisation and development, Prog. Retin. Eye Res., 15, 139, 10.1016/1350-9462(95)00008-9 Rieke, 1996, Molecular origin of continuous dark noise in rod photoreceptors, Biophys. J., 71, 2553, 10.1016/S0006-3495(96)79448-1 Rizzo, 2016, Detecting presence of cardiovascular disease through mitochondria respiration as depicted through biophotonic emission, Redox Biol., 8, 11, 10.1016/j.redox.2015.11.014 Rohlich, 1994, Two different visual pigments in one retinal cone cell, Neuron, 13, 1159, 10.1016/0896-6273(94)90053-1 Rushton, 1968, Bleaching and regeneration of cone pigments in man, Vis. Res., 8, 617, 10.1016/0042-6989(68)90040-0 Ruzafa, 2015, Effect of Müller cells on the survival and neuritogenesis in retinal ganglion cells, Arch. Soc. Esp. Oftalmol., 90, 522, 10.1016/j.oftal.2015.03.009 Salari, 2015, Ultraweak photon emission in the brain, J. Integr. Neurosci., 14, 419, 10.1142/S0219635215300012 Salari, 2016, The physical mechanism for retinal discrete dark noise: thermal activation or cellular ultraweak photon emission?, PLoS One, 11, e0148336, 10.1371/journal.pone.0148336 Salari, 2016, Relationship between intelligence and spectral characteristics of brain biophoton emission: correlation does not automatically imply causation, Proc. Natl. Acad. Sci. U. S. A., 113, E5540, 10.1073/pnas.1612646113 San Giovanni, 2005, The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina, Prog. Retin. Eye Res., 24, 87, 10.1016/j.preteyeres.2004.06.002 Sand, 2012, Diverse types of ganglion cell photoreceptors in the mammalian retina, Prog. Retin. Eye Res., 31, 287, 10.1016/j.preteyeres.2012.03.003 Sandell, 2011, A review of in-vivo optical properties of human tissues and its impact on PDT, J. Biophot., 4, 773, 10.1002/jbio.201100062 Schmidt, 2011, Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions, Trends Neurosci., 34, 572, 10.1016/j.tins.2011.07.001 Scholkmann, 2015, Two emerging topics regarding long-range physical signaling in neurosystems: membrane nanotubes and electromagnetic fields, J. Integr. Neurosci., 14, 135, 10.1142/S0219635215300115 Scholkmann, 2016, Long range physical cell-to-cell signalling via mitochondria inside membrane nanotubes: a hypothesis, Theor. Biol. Med. Model, 13, 1, 10.1186/s12976-016-0042-5 Scholkmann, 2014, A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology, Neuroimage, 85, 6, 10.1016/j.neuroimage.2013.05.004 Scott, 1991, Monitoring a mammalian nuclear membrane phase transition by intrinsic ultraweak light emission, FEBS Lett., 285, 97, 10.1016/0014-5793(91)80733-J Sexton, 2015, G-protein coupled receptor kinase 2 minimally regulates melanopsin activity in intrinsically photosensitive retinal ganglion cells, PLoS One, 10, e0128690, 10.1371/journal.pone.0128690 Shichida, 2009, Evolution of opsins and phototransduction, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 364, 2881, 10.1098/rstb.2009.0051 Speer, 2014, Eye-specific retinogeniculate segregation proceeds normally following disruption of patterned spontaneous retinal activity, Neural Dev., 9, 25, 10.1186/1749-8104-9-25 Sperandio, 2012, Retinotopic activity in V1 reflects the perceived and not the retinal size of an afterimage, Nat. Neurosci., 15, 540, 10.1038/nn.3069 Sperry, 1963, Chemoaffinity in the orderly growth of nerve fiber patterns and connections, Proc. Natl. Acad. Sci. U. S. A., 50, 703, 10.1073/pnas.50.4.703 Sun, 2010, Biophotons as neural communication signals demonstrated by in situ biophoton autography, Photochem. Photobiol. Sci., 9, 315, 10.1039/b9pp00125e Suzuma, 2007, Cyclic stretch-induced reactive oxygen species generation enhances apoptosis in retinal pericytes through c-jun NH2-terminal kinase activation, Hypertension, 49, 347, 10.1161/01.HYP.0000253535.26659.2f Tang, 2013, Biophoton signal transmission and processing in the brain, J. Photochem. Photobiol. B. Biol., 139, 71, 10.1016/j.jphotobiol.2013.12.008 Tang, 2014, Spatiotemporal imaging of glutamate-induced biophotonic activities and transmission in neural circuits, PLoS One, 9, e85643, 10.1371/journal.pone.0085643 Tehovnik, 2009, Microstimulation of visual cortex to restore vision, Prog. Brain Res., 175, 347, 10.1016/S0079-6123(09)17524-6 Tinsley, 2016, Direct detection of a single photon by humans, Nat. Commun., 7, 12172, 10.1038/ncomms12172 Tong, 2006, Neural bases of binocular rivalry, Trends Cogn. Sci., 10, 502, 10.1016/j.tics.2006.09.003 van Boxtel, 2010, Opposing effects of attention and consciousness on afterimages, Proc. Natl. Acad. Sci. U. S. A., 107, 8883, 10.1073/pnas.0913292107 van der Velden, 1946, The number of quanta necessary for the perception of light in the human eye, Ophthalmologica, 111, 321, 10.1159/000300352 van Lier, 2009, Filling-in afterimage colors between the lines, Curr. Biol., 19, R323, 10.1016/j.cub.2009.03.010 van Wijk, 2013, Imaging of ultra-weak photon emission in a rheumatoid arthritis mouse model, PLoS One, 8, e84579, 10.1371/journal.pone.0084579 Vimal, 2008, Proto-experiences and subjective experiences: classical and quantum concepts, J. Integr. Neurosci., 7, 49, 10.1142/S0219635208001757 Vimal, 2010, Matching and selection of a specific subjective experience: conjugate matching and subjective experience, J. Integr. Neurosci., 9, 193, 10.1142/S0219635210002214 Vimal, 1987, Appearance of steadily viewed light, Vis. Res., 27, 1309, 10.1016/0042-6989(87)90208-2 von Helmholtz, 1852, Ueber die Theorie der zusammengesetzten Farben, Ann. Phys. Chem., 87, 45, 10.1002/andp.18521630904 von Wright, 1963, A note on interocular transfer and the colour of visual after-images, Scand. J. Psychol., 4, 241, 10.1111/j.1467-9450.1963.tb01329.x Wang, 2011, Spontaneous and visible light-induced ultra-weak photon emission from rat eyes, Brain Res., 1369, 1, 10.1016/j.brainres.2010.10.077 Wiesel, 1963, Single-cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol., 26, 1003, 10.1152/jn.1963.26.6.1003 Willard, 2013, Glutamate, glutamate receptors, and downstream signaling pathways, Int. J. Biol. Sci., 9, 948, 10.7150/ijbs.6426 Williams, 1979, Interchangeable backgrounds for cone afterimages, Vis. Res., 19, 867, 10.1016/0042-6989(79)90020-8 Wong, 2012, A retinal ganglion cell that can signal irradiance continuously for 10 hours, J. Neurosci., 32, 11478, 10.1523/JNEUROSCI.1423-12.2012 Wu, 2009, A multi-stage neural network model for human color vision, vol. 5553, 504 Yanagawa, 2015, Origin of the low thermal isomerization rate of rhodopsin chromophore, Sci. Rep., 5, 11081, 10.1038/srep11081 Young, 1802, Bakerian lecture: on the theory of light and colours, Phil. Trans. R. Soc. Lond, 92, 12, 10.1098/rstl.1802.0004 Zhang, 1997, Spontaneous and light-induced photon emission from intact brains of chick embryos, Sci. China C Life Sci., 40, 43, 10.1007/BF02879106 Zueva, 2014, Müller cell alignment in bird fovea: possible role in vision, J. Neurosci. Neuroeng, 3, 85, 10.1166/jnsne.2014.1104