Abstract
We address the question of how fundamental photon fluctuations are perceived by a live visual system. The discussion is focused on specific type of photoreceptor cells within the eye , known as retinal rod cells. Rod cells provide vision under low light conditions and they are sensitive at a single photon level. We review experiments on interaction of the rod cells with light sources of different photon statistics, including coherent , pseudo-thermal , and single-photon sources . Accurate control over photon statistics of light stimuli, combined with technique for the readout of rod cells response, enable precise and unambiguous characterization of intrinsic features of the visual system at single and discrete photon levels.
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J.E. Dowling, The Retina: An Approachable Part of the Brain (Belknap Press of Harvard University Press, Cambridge, MA, 2012). Revised Edition
C.R. Braekevelt, S.A. Smith, B.J. Smith, Fine structure of the retinal photoreceptors of the barred owl (Strix varia). Histol. Histopathol. 11(1), 79–88 (1996)
M. Joseph, A. Corless, Minimum diameter limit for retinal rod outer segment disks. Development of Order in the Visual System, ed. by S.R. Hilfer et al. (Springer, New York Inc., 1986), pp. 127–142
K. Palczewski, G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75, 743–767 (2006)
M.L. Woodruff, M.D. Bownds, Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3′,5′-cyclic monophosphate in frog photoreceptor membranes. J. Gen. Physiol. 73(5), 629–653 (1979)
H.W. Choe, Y.J. Kim, J.H. Park, T. Morizumi, E.F. Pai, N. Krauss, K.P. Hofmann, P. Scheerer, O.P. Ernst, Crystal structure of metarhodopsin II. Nature 471, 651–655 (2011)
K. Palczewski, T. Kumasaka, T. Hori, C.A. Behnke, H. Motoshima, B.A. Fox, I. Le Trong, D.C. Teller, T. Okada, R.E. Stenkamp et al., Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739–745 (2000)
L. Stryer, Exploring light and life. J. Biol. Chem. 287, 15164–15173 (2012)
T.D. Lamb, Gain and kinetics of activation in the G-protein cascade of phototransduction. Proc. Natl. Acad. Sci. U.S.A. 93, 566–570 (1996)
T.D. Lamb, E.N. Pugh Jr., Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture. Invest. Ophthalmol. Vis. Sci. 47, 5138–5152 (2006)
E.N. Pugh Jr., T.D. Lamb, Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vis. Res. 30, 1923–1948 (1990)
R.H. Cote, M.A. Brunnock, Intracellular cGMP concentration in rod photoreceptors is regulated by binding to high and moderate affinity cGMP binding sites. Biol. Chem. 268(23), 17190–17198 (1993)
X. Zhang, R.H. Cote, cGMP signaling in vertebrate retinal photoreceptor cells. Front Biosci. 10, 1191–1204 (2005)
E.E. Fesenko, S.S. Kolesnikov, A.L. Lyubarsky, Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310–313 (1985)
W.H. Cobbs, E.N. Pugh Jr., Cyclic GMP can increase rod outer-segment light-sensitive current 10-fold without delay of excitation. Nature 313, 585–587 (1985)
K. Matulef, W.N. Zagotta, Cyclic nucleotide-gated ion channels. Annu. Rev. Cell Dev. Biol. 19, 23–44 (2003)
R.R. Birge, Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin. Biochim. Biophys. Acta 1016, 293–327 (1990)
B.K.-K. Fung, J.B. Hurley, L. Stryer, Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc. Natl. Acad. Sci. U.S.A. 78, 152–156 (1981)
N. Sim, M.F. Cheng, D. Bessarab, C.M. Jones, L.A. Krivitsky, Measurement of photon statistics with live photoreceptor cells. Phys. Rev. Lett. 109, 113601 (2012)
M.E. Burns, E.N. Pugh Jr., Lessons from photoreceptors: turning off G-protein signaling in living cells. Physiology (Bethesda) 25, 72–84 (2010)
C.M. Krispel, D. Chen, N. Melling, Y.J. Chen, K.A. Martemyanov, N. Quillinan, V.Y. Arshavsky, T.G. Wensel, C.K. Chen, M.E. Burns, RGS expression rate-limits recovery of rod photoresponses. Neuron 51, 409–416 (2006)
C.K. Chen, M.L. Woodruff, F.S. Chen, D. Chen, G.L. Fain, Background light produces a recoverin-dependent modulation of activated-rhodopsin lifetime in mouse rods. J. Neurosci. 30, 1213–1220 (2010)
W.H. Cobbs, E.N. Pugh Jr., Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. J. Physiol. 394, 529–572 (1987)
P. Bisegna, G. Caruso, D. Andreucci, L. Shen, V.V. Gurevich, H.E. Hamm, E. DiBenedetto, Diffusion of the second messengers in the cytoplasm acts as a variability suppressor of the single photon response in vertebrate phototransduction. Biophys. J. 94, 3363–3383 (2008)
F. Rieke, D.A. Baylor, Origin of reproducibility in the responses of retinal rods to single photons. Biophys. J. 75, 1836–1857 (1998)
U.B. Kaupp, R. Seifert, Cyclic nucleotide-gated ion channels. Physiol. Rev. 82(3), 769–824 (2002)
E. Eismann, F. Müller, S.H. Heinemann, U.B. Kaupp, A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. Proc. Natl. Acad. Sci. U.S.A. 91(3), 1109–1113 (1994)
K.W. Yau, D.A. Baylor, Cyclic GMP activated conductance of retinal photoreceptor cells. Annu. Rev. Neurosci. 12, 289–327 (1989)
F. Rieke, D.A. Baylor, Single photon detection by rod cells of the retina. Rev. Mod. Phys. 70, 1027–1036 (1998)
T. Doan, A. Mendez, P.B. Detwiler, J. Chen, F. Rieke, Multiple phosphorylation sites confer reproducibility of the rod’s single-photon responses. Science 313, 530–533 (2006). PMID: 16873665, http://dx.doi.org/10.1126/science.1126612
A.W. Azevedo, T. Doan, H. Moaven, I. Sokal, F. Baameur, S.A. Vishnivetskiy, K.T. Homan, J.J. Tesmer, V.V. Gurevich, J. Chen, F. Rieke, C-terminal threonines and serines play distinct roles in the desensitization of rhodopsin, a G protein-coupled receptor. Elife 4 (2015). https://doi.org/10.7554/elife.05981
V. Torre, H.R. Matthews, T.D. Lamb, Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc. Natl. Acad. Sci. U.S.A. 83(18), 7109–7113 (1986)
M. Capovilla, L. Cervetto, V. Torre, The effect of phosphodiesterase inhibitors on the electrical activity of toad rods. J. Physiol. 343, 277–294 (1983)
M. Capovilla, L. Cervetto, V. Torre, Effects of changing external potassium and chloride concentrations on the photoresponses of Bufo bufo rods. J. Physiol. 307, 529–551 (1980)
E.N. Pugh Jr., T.D. Lamb, Amplification and kinetics of the activation steps in phototransduction. Biochim. Biophys. Acta 1141(2–3), 111–149 (1993)
D.A. Baylor, B.J. Nunn, J.L. Schnapf, The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. 357, 575–607 (1984)
S. Asteriti, S. Grillner, L. Cangiano, A Cambrian origin for vertebrate rods. eLife 4, e07166 (2015). https://doi.org/10.7554/elife.07166
J.R. Sanes, S.L. Zipursky, Design principles of insect and vertebrate visual systems. Neuron 66(1), 15–36 (2010). https://doi.org/10.1016/j.neuron.2010.01.018
C. Montell, Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol. 15, 231–268 (1999)
C. Montell, Drosophila visual transduction. Trends Neurosci. 35, 356–363 (2012)
R.C. Hardie, M. Juusola, Phototransduction in Drosophila. Curr. Opin. Neurobiol. 34C, 37–45 (2015)
R.C. Hardie, Phototransduction in Drosophila melanogaster. J. Exp. Biol. 204(Pt 20), 3403–3409 (2001)
A. Auerbach, F. Sachs, Flickering of a nicotinic ion channel to a subconductance state. Biophys. J. 42(1), 1–10 (1983)
O. Alvarez, C. Gonzalez, R. Latorre, Counting channels: a tutorial guide on ion channel fluctuation analysis. Adv. Physiol. Educ. 26(1–4), 327–341 (2002)
I. Lestas, G. Vinnicombe, J. Paulsson, Fundamental limits on the suppression of molecular fluctuations. Nature 467, 174–178 (2010)
D.G. Spiller, C.D. Wood, D.A. Rand, M.R. White, Measurement of single-cell dynamics. Nature 465, 736–745 (2010)
P.N. Steinmetz, R.L. Winslow, Optimal detection of flash intensity differences using rod photocurrent observations. Neural Comput. 11(5), 1097–1111 (1999)
R.A. Yotter, D.M. Wilson, A review of photodetectors for sensing light-emitting reporters in biological systems. IEEE Sens. J. 3, 288–303 (2003)
G.N. Gol’tsman, O. Okunev, G. Chulkova, A. Lipatov, A. Semenov, K. Smirnov, B. Voronov, A. Dzardanov, Picosecond superconducting single-photon optical detector. Appl. Phys. Lett. 79(6), 705–707 (2001)
M. Dandin, P. Abshire, High signal-to-noise ratio avalanche photodiodes with perimeter field gate and active readout. IEEE Electron Device Lett. 33(4), 570–572 (2012)
K. Kolb, Signal-to-noise ratio of Geiger-mode avalanche photodiode single-photon counting detectors. Opt. Eng. 53(8), 081904 (2014)
J.E. Sulston, E. Schierenberg, J.G. White, J.N. Thomson, The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100(1), 64–119 (1983)
A.S. Chiang, C.Y. Lin, C.C. Chuang, H.M. Chang, C.H. Hsieh, C.W. Yeh, C.T. Shih, J.J. Wu, G.T. Wang, Y.C. Chen, C.C. Wu, G.Y. Chen, Y.T. Ching, P.C. Lee, C.Y. Lin, H.H. Lin, C.C. Wu, H.W. Hsu, Y.A. Huang, J.Y. Chen, H.J. Chiang, C.F. Lu, R.F. Ni, C.Y. Yeh, J.K. Hwang, Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21(1), 1–11 (2011)
L. Chittka, J. Niven, Are bigger brains better? Curr. Biol. 19, R995–R1008 (2009)
S. Herculano-Houzel, The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proc. Natl. Acad. Sci. U.S.A. 109(Suppl 1), 10661–10668 (2012)
S.M. Wu, Synaptic transmission in the outer retina. Annu. Rev. Physiol. 56, 141–168 (1994)
W. Bialek, W.G. Owen, Temporal filtering in retinal bipolar cells. Elements of an optimal computation? Biophys. J. 58(5), 1227–1233 (1990)
H. Markram, E. Muller, S. Ramaswamy, M.W. Reimann, M. Abdellah, C.A. Sanchez, A. Ailamaki, L. Alonso-Nanclares, N. Antille, S. Arsever, G.A. Kahou, T.K. Berger, A. Bilgili, N. Buncic, A. Chalimourda, G. Chindemi, J.D. Courcol, F. Delalondre, V. Delattre, S. Druckmann, R. Dumusc, J. Dynes, S. Eilemann, E. Gal, M.E. Gevaert, J.P. Ghobril, A. Gidon, J.W. Graham, A. Gupta, V. Haenel, E. Hay, T. Heinis, J.B. Hernando, M. Hines, L. Kanari, D. Keller, J. Kenyon, G. Khazen, Y. Kim, J.G. King, Z. Kisvarday, P. Kumbhar, S. Lasserre, J.V. Le Bé, B.R. Magalhães, A. Merchán-Pérez, J. Meystre, B.R. Morrice, J. Muller, A. Muñoz-Céspedes, S. Muralidhar, K. Muthurasa, D. Nachbaur, T.H. Newton, M. Nolte, A. Ovcharenko, J. Palacios, L. Pastor, R. Perin, R. Ranjan, I. Riachi, J.R. Rodríguez, J.L. Riquelme, C. Rössert, K. Sfyrakis, Y. Shi, J.C. Shillcock, G. Silberberg, R. Silva, F. Tauheed, M. Telefont, M. Toledo-Rodriguez, T. Tränkler, W. Van Geit, J.V. Díaz, R. Walker, Y. Wang, S.M. Zaninetta, J. DeFelipe, S.L. Hill, I. Segev, F. Schürmann, Reconstruction and simulation of neocortical microcircuitry. Cell 163(2), 456–492 (2015)
R.G. Boothe, Perception of the Visual Environmen. Psychology (Springer Science & Business Media, 2001), 408 pages. ISBN: 978-0-387-98790-3 (Print) 978-0-387-21650-8 (Online)
A.P. Sampath, F. Rieke, Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41(3), 431–443 (2004)
D. Attwell, S. Borges, S.M. Wu, M. Wilson, Signal clipping by the rod output synapse. Nature 328(6130), 522–524 (1987)
S. Barnes, V. Merchant, F. Mahmud, Modulation of transmission gain by protons at the photoreceptor output synapse. Proc. Natl. Acad. Sci. U.S.A. 90(21), 10081–10085 (1993)
A.J. Mercer, W.B. Thoreson, The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis. Neurosci. 28(6), 453–471 (2011)
A. Bharioke, D.B. Chklovskii, Automatic adaptation to fast input changes in a time-invariant neural circuit. PLoS Comput. Biol. 11(8), e1004315 (2015). https://doi.org/10.1371/journal.pcbi.1004315
S.P. Langley, The bolometer and radiant energy, in Proceedings of the American Academy of Arts and Science, vol. 16 (American Academy of Arts & Sciences, May 1880–Jun 1881), pp. 342–358. https://doi.org/10.2307/25138616, http://www.jstor.org/stable/25138616
J. von Kries, J.A.E. Eyster, Über die zur Erregung des Sehorgans efforderlichen Energiemenzen. Z. Sinnesphysiol. 41, 373–394 (1907)
A. Verkhratsky, O.A. Krishtal, O.H. Petersen, From Galvani to patch clamp: the development of electrophysiology. Pflugers Arch. 453(3), 233–247 (2006)
T. Tomita, A. Funaishi, Studies on intraretinal action potential with low-resistance microelectrode. J. Neurophysiol. 15(1), 75–84 (1952)
G.S. Brindley, Responses to illumination recorded by microelectrodes from the frog’s retina. J. Physiol. 134(2), 360–384 (1956)
A.L. Byzov, Functional properties of different cells in the retina of cold-blooded vertebrates. Cold Spring Harb. Symp. Quant. Biol. 30, 547–558 (1965)
S.R. Grabowski, L.H. Pinto, W.L. Pak, Adaptation in retinal rods of axolotl: intracellular recordings. Science 176(4040), 1240–1243 (1972)
R.D. Penn, W.A. Hagins, Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223(5202), 201–204 (1969)
D.A. Baylor, T.D. Lamb, K.W. Yau, The membrane current of single rod outer segments. J. Physiol. 288, 589–611 (1979)
D.A. Baylor, T.D. Lamb, K.W. Yau, Responses of retinal rods to single photons. J. Physiol. 288, 613–634 (1979)
R.B. Barnes, M. Czerny, Läßt sich ein Schroteffekt der Photonen mit dem Auge beobachten? Zeitschrift für Physik 79(7), 436–449 (1932)
S. Hecht, S. Shlaer, M.H. Pirenne, Energy, quanta, and vision. J. Gen. Physiol. 25(6), 819–840 (1942)
E. Brumberg, S. Vavilov, Visuelle Messungen der statistischen Photonenschwankungen. Bull. Acad. Sci. U.R.S.S. 7, 919–941 (1933)
E.M. Brumberg, S.I. Vavilov, Z.M. Sverdlov, Visual measurements of quantum fluctuations. I. The threshold of vision as compared with the results of fluctuation measurements. J. Phys. 7(1), 1–8 (1943)
S.I. Vavilov, T.V. Timofeeva, Visual measurements of quantum fluctuations. II. Fluctuations when the eye is light-adapted. J. Phys. 7(1), 9–11 (1943)
S.I. Vavilov, T.V. Timofeeva, Visual measurements of quantum fluctuations. III. The dependence of the visual fluctuations on the wave-length. J. Phys. 7(1), 12–17 (1943)
S.I. Vavilov, The Microstructure of Light (Academy of Sciences, Moscow, 1950), p. 198. (in Russian)
S. Hecht, S. Shlaer, M.H. Pirenne, Energy at the threshold of vision. Science 93(2425), 585–587 (1941)
R. Gunter, The absolute threshold for vision in the cat. J. Physiol. 114(1–2), 8–15 (1951)
S. Hecht, M.H. Pirenne, The sensibility of the nocturnal long-eared owl in the spectrum. J. Gen. Physiol. 23(6), 709–717 (1940)
M.C. Teich, P.R. Prucnal, G. Vannucci, M.E. Breton, W.J. McGill, Multiplication noise in the human visual system at threshold: 1. Quantum fluctuations and minimum detectable energy. J. Opt. Soc. Am. 72, 419–431 (1982)
P.R. Prucnal, M.C. Teich, Multiplication noise in the human visual system at threshold: 2. Probit estimation of parameters. Biol. Cybern. 43, 87–96 (1982)
M.C. Teich, P.R. Prucnal, G. Vannucci, M.E. Breton, W.J. McGill, Multiplication noise in the human visual system at threshold: 3. The role of non-poisson quantum fluctuations. Biol. Cybern. 44, 157–165 (1982)
K.W. Yau, T.D. Lamb, D.A. Baylor, Light-induced fluctuations in membrane current of single toad rod outer segments. Nature 269(5623), 78–80 (1977)
P.B. Detwiler, J.D. Conner, R.D. Bodoia, Gigaseal patch clamp recordings from outer segments of intact retinal rods. Nature 300(5887), 59–61 (1982)
R.D. Bodoia, P.B. Detwiler, Patch-clamp recordings of the light-sensitive dark noise in retinal rods from the lizard and frog. J. Physiol. 367, 183–216 (1985)
J. Toyoda, H. Hashimoto, H. Anno, T. Tomita, The rod response in the frog and studies by intracellular recording. Vis. Res. 10(11), 1093–1100 (1970)
T. Tomita, Electrical activity of vertebrate photoreceptors. Q. Rev. Biophys. 3(2), 179–222 (1970)
J.E. Brown, L.H. Pinto, Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus. J. Physiol. 236(3), 575–591 (1974)
R.R. Birge, R.B. Barlow, On the molecular origins of thermal noise in vertebrate and invertebrate photoreceptors. Biophys. Chem. 55, 115–126 (1995)
N.M. Phan, M.F. Cheng, D.A. Bessarab, L.A. Krivitsky, Interaction of fixed number of photons with retinal rod cells. Phys. Rev. Lett. 112, 213601 (2014)
L. Mandel, E. Wolf, Optical Coherence and Quantum Optics (Cambridge University Press, Cambridge, England, 1995)
F.T. Arecchi, Measurement of the statistical distribution of Gaussian and laser sources. Phys. Rev. Lett. 15, 912 (1965)
D.N. Klyshko, Physical Foundations of Quantum Electronics (World Scientific, Singapore, 2011)
N. Sim, D. Bessarab, C.M. Jones, L. Krivitsky, Method of targeted delivery of laser beam to isolated retinal rods by fiber optics. Biomed. Opt. Express 2, 2926–2933 (2011)
A.A. Malygin, A.N. Penin, A.V. Sergienko, Absolute calibration of the sensitivity of photodetectors using a biphotonic field. Sov. Phys. JETP Lett. 33, 477–481 (1981)
H. Mutoh, W. Akemann, T. Knöpfel, Genetically engineered fluorescent voltage reporters. ACS Chem. Neurosci. 3, 585–592 (2012)
K.D. Piatkevich, F.V. Subach, V.V. Verkhusha, Engineering of bacterial phytochromes for near-infrared imaging, sensing, and light-control in mammals. Chem. Soc. Rev. 42(8), 3441–3452 (2013)
T. Tolmachova, O.E. Tolmachov, A.R. Barnard, S.R. de Silva, D.M. Lipinski, N.J. Walker, R.E. Maclaren, M.C. Seabra, Functional expression of Rab escort protein 1 following AAV2-mediated gene delivery in the retina of choroideremia mice and human cells ex vivo. J. Mol. Med. (Berl) 91(7), 825–837 (2013)
E. Pomarico, B. Sanguinetti, N. Gisin, R. Thew, H. Zbinden, G. Schreiber, A. Thomas, W. Sohler, Waveguide-based OPO source of entangled photon pairs. New J. Phys. 11, 113042 (2009)
V. Volkov, Discovering electrophysiology in photobiology: a brief overview of several photobiological processes with an emphasis on electrophysiology. Commun. Integr. Biol. 7, e28423 (2014)
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Krivitsky, L., Volkov, V. (2019). The Role of Photon Statistics in Visual Perception. In: Boyd, R., Lukishova, S., Zadkov, V. (eds) Quantum Photonics: Pioneering Advances and Emerging Applications. Springer Series in Optical Sciences, vol 217. Springer, Cham. https://doi.org/10.1007/978-3-319-98402-5_6
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