Dynamical Adaptation in Photoreceptors

PLoS Computational Biology

Volumn 9, Issue 11, 2013, Pages

  Clark, Damon A ^a,d   Benichou, Raphael ^a,e   Meister, Markus ^b,f   Azeredo da Silveira, Rava ^a,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b HARVARD UNIVERSITY   (United States)

^c CNRS   (France)

^d YALE UNIVERSITY   (United States)

^e Capital Fund Management   (France)

^f CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL RESEARCH; PHYSIOLOGICAL MODELS;

ADAPTATION MODELS; ANALYTICAL APPROACH; LIGHT RESPONSE; NON LINEAR; NUMERICAL APPROACHES; QUANTITATIVE RESULT; SIMPLE++; TEMPORAL STRUCTURES; TIME-SCALES; VISUAL-PROCESSING;

VISION;

ARTICLE; CALCULATION; DARK ADAPTATION; HUMAN; HYPERPOLARIZATION; LIGHT ADAPTATION; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; NONHUMAN; PHOTORECEPTOR; PHOTORECEPTOR MEMBRANE; PHOTOTRANSDUCTION; RETINA CONE; STIMULUS RESPONSE; VISUAL STIMULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; COMPUTATIONAL BIOLOGY; HUMANS; LIGHT; LIGHT SIGNAL TRANSDUCTION; MODELS, BIOLOGICAL; PHOTORECEPTOR CELLS;

EID: 84888273304     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003289     Document Type: Article

References (93)

1. Shapley R, Victor J, (1978) The Effect of Constrast on the Transfer Properties of Cat Retinal Ganglion Cells. Journal of Physiology 285: 275-298.
2. Shapley R, Enroth-Cugell C, (1984) Visual adaptation and retinal gain controls. Prog Ret Res 3: 263-346.
3. Tranchina D, Gordon J, Shapley R, (1984) Retinal light adaptation-evidence for a feedback mechanism. Nature 310: 314-316.
4. Laughlin S, (1989) The role of sensory adaptation in the retina. Journal of Experimental Biology 146: 39-62.
5. Smirnakis S, Berry M, Warland D, Bialek W, Meister M, (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386: 69-73.
6. Fairhall A, Lewen G, Bialek W, van Steveninck R, (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412: 787-792.
7. Kim K, Rieke F, (2001) Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J Neurosci 21: 287-299.
8. Baccus S, Meister M, (2002) Fast and Slow Contrast Adaptation in Retinal Circuitry. Neuron 36: 909-919.
9. Lee B, (2003) Dynamics of sensitivity regulation in primate outer retina: The horizontal cell network. Journal of Vision 3: 513-526.
10. Borst A, Flanagin V, Sompolinsky H, (2005) Adaptation without parameter change: Dynamic gain control in motion detection. Proceedings of the National Academy of Sciences 102: 6172.
11. Dunn F, Lankheet M, Rieke F, (2007) Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449: 603-606.
12. Fuortes M, Hodgkin A, (1964) Changes in time scale and sensitivity in the ommatidia of Limulus. The Journal of Physiology 172: 239.
13. Baylor D, Hodgkin A, (1974) Changes in time scale and sensitivity in turtle photoreceptors. The Journal of Physiology 242: 729-758.
14. Baylor D, Hodgkin A, Lamb T, (1974) The electrical response of turtle cones to flashes and steps of light. The Journal of Physiology 242: 685-727.
15. Baylor D, Hodgkin A, Lamb T, (1974) Reconstruction of the electrical responses of turtle cones to flashes and steps of light. The Journal of Physiology 242: 759-791.
16. Daly S, Normann R, (1985) Temporal information processing in cones: effects of light adaptation on temporal summation and modulation. Vision Res 25: 1197-206.
17. Tranchina D, Sneyd J, Cadenas I, (1991) Light adaptation in turtle cones. Testing and analysis of a model for phototransduction. Biophysical Journal 60: 217-237.
18. Burkhardt D, (1994) Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. Journal of Neuroscience 14: 1091.
19. Juusola M, Kouvalainen E, Järvilehto M, Weckström M, (1994) Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. The Journal of general physiology 104: 593.
20. Schneeweis D, Schnapf J, (1999) The Photovoltage of Macaque Cone Photoreceptors: Adaptation, Noise, and Kinetics. Journal of Neuroscience 19: 1203.
21. Juusola M, Hardie R, (2001) Light Adaptation in Drosophila Photoreceptors II. Rising Temperature Increases the Bandwidth of Reliable Signaling. The Journal of General Physiology 117: 27-42.
22. Fain G, Matthews H, Cornwall M, Koutalos Y, (2001) Adaptation in Vertebrate Photoreceptors. Physiological Reviews 81: 117-151.
23. van Hateren J, (2005) A cellular and molecular model of response kinetics and adaptation in primate cones and horizontal cells. Journal of Vision 5: 331-347.
24. van Hateren J, Snippe H, (2006) Phototransduction in primate cones and blowfly photoreceptors: different mechanisms, different algorithms, similar response. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 192: 187-197.
25. Soo F, Detwiler P, Rieke F, (2008) Light adaptation in salamander L-cone photoreceptors. Journal of Neuroscience 28: 1331.
26. Pasino E, Marchiafava P, (1976) Transfer properties of rod and cone cells in the retina of the tiger salamander. Vision Res 16: 381-6.
27. Seung H (2003) Amplification, Attenuation, and Integration. In: M A Arbib, Editor. Handbook of Brain Theory and Neural Networks: Second Edition.
28. Pugh E Jr, Lamb T, (1993) Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1141: 111-49.
29. Yau K, (1994) Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 35: 9-32.
30. Pugh E, Nikonov S, Lamb T, (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Current Opinion in Neurobiology 9: 410-418.
31. Ebrey T, Koutalos Y, (2001) Vertebrate Photoreceptors. Progress in Retinal and Eye Research 20: 49-94.
32. Carpenter G, Grossberg S, (1981) Adaptation and Transmitter Gating in Vertebrate Photoreceptors. J Theoret Neurobiol 1: 1-42.
33. Levchenko A, Iglesias P, (2002) Models of Eukaryotic Gradient Sensing: Application to Chemotaxis of Amoebae and Neutrophils. Biophysical Journal 82: 50-63.
34. Tyson J, Chen K, Novak B, (2003) Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Current Opinion in Cell Biology 15: 221-231.
35. Yang L, Iglesias P, (2005) Feedback induced biphasic response in the chemotaxis pathway of Dictyostelium. IEEE Proc American Control Conference 6: 4393-4398.
36. Friedlander T, Brenner N, (2009) Adaptive response by state-dependent inactivation. Proc Nat Ac Sci 106: 22558-22563.
37. Sontag E, (2010) Remarks on feedforward circuits, adaptation, and pulse memory. IET Syst Biol 4: 39-51.
38. Friedlander T, Brenner N, (2011) Adaptive response and enlargement of dynamic range. Mathem Biosci Eng 8: 515-528.
39. Baylor D, Fuortes M, Bryan PO, (1971) Receptive fields of cones in the retina of the turtle. The Journal of Physiology 214: 265-294.
40. Srinivasan M, Laughlin S, Dubs A, (1982) Predictive Coding: A Fresh View of Inhibition in the Retina. Proceedings of the Royal Society of London Series B, Biological Sciences 216: 427-459.
41. van Hateren J, (1992) Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation. Journal of Comparative Physiology A 171: 157-170.
42. Poot L, Snippe H, van Hateren J, (1997) Dynamics of adaptation at high luminances: Adaptation is faster after luminance decrements than after luminance increments. Journal of the Optical Society of America A 14: 2499-2508.
43. Korenberg M, Hunter I, (1986) The identification of nonlinear biological systems: LNL cascade models. Biological Cybernetics 55: 125-134.
44. Hunter I, Korenberg M, (1986) The identification of nonlinear biological systems: Wiener and Hammerstein cascade models. Biological Cybernetics 55: 135-144.
45. Chichilnisky E, (2001) A simple white noise analysis of neuronal light responses. Network: Computation in Neural Systems 12: 199-213.
46. Hong S, Lundstrom B, Fairhall A, (2008) Intrinsic Gain Modulation and Adaptive Neural Coding. PLoS Computational Biology 4: e1000119.
47. Gaudry K, Reinagel P, (2007) Benefits of Contrast Normalization Demonstrated in Neurons and Model Cells. J Neurosci 27: 8071-8079.
48. Rodieck R (1998) The first steps in seeing. Sinauer Associates Sunderland, Mass.
49. Endeman D, Kamermans M, (2010) Cones perform a non-linear transformation on natural stimuli. Journal of Physiology 588: 435-446.
50. van Hateren J, (1997) Processing of natural time series of intensities by the visual system of the blowfly. Vision Research 37: 3407-3416.
51. Hamer R, Nicholas S, Tranchina D, Lamb TD, Jarvinen JL, (2005) Toward a unified model of vertebrate rod phototransduction. Vis Neurosci 22: 417-436.
52. Tachibanaki S, Tsushima S, Kawamura S, (2001) Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses. Proc Natl Acad Sci U S A 98: 14044-14049.
53. Gray-Keller M, Detwiler P, (1996) Ca Dependence of Dark- and Light-Adapted Flash Responses in Rod Photoreceptors. Neuron 17: 323-331.
54. Gray-Keller M, Detwiler P, (1994) The Calcium Feedback Signal in the Phototransduction Cascade of Vertebrate Rods. Neuron 13: 849-861.
55. Cilluffo M, Matthews H, Brockerhoff S, Fain G, (2004) Light-induced Ca release in the visible cones of the zebrafish Visual Neuroscience. 21: 599-609.
56. Victor J, (1987) The Dynamics of the Cat Retinal X Cell Centre. J Physiol 386: 219-246.
57. Safran M, Flanagin V, Borst A, Sompolinsky H, (2007) Adaptation and Information Transmission in Fly Motion Detection. Journal of Neurophysiology 98: 3309-3320.
58. Gaudry K, Reinagel P, (2007) Contrast Adaptation in a Nonadapting LGN Model. J Neurophysiol 98: 1287-1296.
59. Lundstrom B, Higgs M, Spain W, Fairhall A, (2008) Fractional differentiation by neocortical pyramidal neurons. Nature Neuroscience 11: 1335-1342.
60. Juusola M, Uusitalo R, Weckstrom M, (1995) Transfer of Graded Potentials at the Photoreceptor-Interneuron Synapse. J Gen Physiol 105: 117-148.
61. Land M, Nilsson D (2002) Animal Eyes. Oxford: Oxford University Press.
62. Müller J, Metha A, Krauskopf J, Lennie P, (1999) Rapid adaptation in visual cortex to the structure of images. Science 285: 1405-1408.
63. Carandini M, (2000) Visual cortex: Fatigue and adaptation. Current Biology 10: R605-R607.
64. Dragoi V, Sharma J, Sur M, (2000) Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28: 287-298.
65. Solomon S, Peirce J, Dhruv N, Lennie P, (2004) Profound contrast adaptation early in the visual pathway. Neuron 42: 155-162.
66. Gardner J, Sun P, Waggoner R, Ueno K, Tanaka K, et al. (2005) Contrast adaptation and representation in human early visual cortex. Neuron 47: 607-620.
67. Kohn A, (2007) Visual adaptation: physiology, mechanisms, and functional benefits. Journal of Neurophysiology 97: 3155-3164.
68. Fain G, (2003) Sensory Transduction. Sinauer Associates.
69. Baylor D, Hodgkin A, (1973) Detection and resolution of visual stimuli by turtle photoreceptors. The Journal of Physiology 234: 163-198.
70. Hateren J, (1992) Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 171: 157-170.
71. Juusola M, Uusitalo R, Weckstrom M, (1995) Transfer of graded potentials at the photoreceptor-interneuron synapse. Journal of General Physiology 105: 117.
72. Brown J, Coles J, (1979) Saturation of the response to light in Limulus ventral photoreceptor. The Journal of Physiology 296: 373.
73. Dorlöchter M, Stieve H, (1997) The Limulus ventral photoreceptor: Light response and the role of calcium in a classic preparation. Progress in Neurobiology 53: 451-515.
74. Lisman J, Brown J, (1975) Light-induced changes of sensitivity in limulus ventral photoreceptors. The Journal of general physiology 66: 473-488.
75. Payne R, (1986) The initial response of Limulus ventral photoreceptors to bright flashes. Released calcium as a synergist to excitation. The Journal of General Physiology 87: 243-269.
76. Contzen K, Nagy K, (1996) A mathematical model for the components of the receptor current in Limulus ventral nerve photoreceptors. Journal of Photochemistry & Photobiology, B: Biology 35: 123-132.
77. Pinter R, (1966) Sinusoidal and Delta Function Responses of Visual Cells of the Limulus Eye. The Journal of General Physiology 49: 565-593.
78. Kaplan E, (1975) Properties of visual cells in the lateral eye of Limulus in situ. The Journal of General Physiology 66: 303-326.
79. Howard J, (1981) Temporal resolving power of the photoreceptors ofLocusta migratoria. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 144: 61-66.
80. Howard J, Dubs A, Payne R, (1984) The dynamics of phototransduction in insects. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 154: 707-718.
81. Pinter R, (1972) Frequency and time domain properties of retinular cells of the desert locust (Schis-tocerca gregaria) and the house cricket (Acheta domesticus). Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 77: 383-397.
82. Leutscher-Hazelhoff J, (1975) Linear and non-linear performance of transducer and pupil in Calliphora retinula cells. The Journal of Physiology 246: 333-350.
83. Leutscher-Hazelhoff J, Kuiper J, (1964) Responses of the blowfly (Calliphora erythrocephala) to light.ashes and to sinusoidally modulated light. Documenta Ophthalmologica 18: 275-283.
84. Baylor D, Fuortes M, (1970) Electrical responses of single cones in the retina of the turtle. The Journal of Physiology 207: 77-92.
85. Donner K, Hemilä S, Koskelainen A, (1998) Light adaptation of cone photoresponses studied at the photoreceptor and ganglion cell levels in the frog retina. Vision Research 38: 19-36.
86. Pluvinage V, Green D, (1990) Evidence for a power law intensity code in the coupled cones of the turtle. Vision Res 30: 673-82.
87. Matthews H, Fain G, Murphy R, Lamb T, (1990) Light adaptation in cone photoreceptors of the salamander: a role for cytoplasmic calcium. The Journal of Physiology 420: 447.
88. Normann R, Anderton P, (1983) The incremental sensitivity curve of turtle cone photoreceptors. Vision Res 23: 1731-3.
89. Rieke F, Baylor D, (2000) Origin and Functional Impact of Dark Noise in Retinal Cones. Neuron 26: 181-186.
90. Kraft T, (1988) Photocurrents of cone photoreceptors of the golden-mantled ground squirrel. The Journal of Physiology 404: 199.
91. Nikonov S, Kholodenko R, Lem J, Pugh E, (2006) Physiological Features of the S-and M-cone Photoreceptors of Wild-type Mice from Single-cell Recordings. The Journal of General Physiology 127: 359-374.
92. Boynton R, Whitten D, (1970) Visual Adaptation in Monkey Cones: Recordings of Late Receptor Potentials.
93. Schnapf J, Nunn B, Meister M, Baylor D, (1990) Visual transduction in cones of the monkey Macaca fascicularis. The Journal of Physiology 427: 681.