Interactions between light-induced currents, voltage-gated currents, and input signal properties in Drosophila photoreceptors

Journal of Neurophysiology

Volumn 91, Issue 6, 2004, Pages 2696-2706

  Niven, Jeremy E ^a   Vähäsöyrinki, Mikko ^b   Juusola, Mikko ^a   French, Andrew S ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF OULU   (Finland)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; BIOLOGICAL MODEL; CHANNEL GATING; CONTROLLED STUDY; DROSOPHILA; FEEDBACK SYSTEM; FLOW RATE; HODGKIN HUXLEY EQUATION; LIGHT; MEMBRANE CURRENT; MEMBRANE POTENTIAL; MOLECULAR INTERACTION; NONHUMAN; NONLINEAR SYSTEM; NONPARAMETRIC TEST; PARAMETRIC TEST; PHOTORECEPTOR MEMBRANE; POTASSIUM CURRENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SIMULATION; WILD TYPE;

ANIMALS; DARKNESS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; LIGHTING; MUTATION, MISSENSE; PHOTORECEPTORS, INVERTEBRATE; POTASSIUM CHANNELS; POTASSIUM CHANNELS, VOLTAGE-GATED; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS;

EID: 2442472945     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01163.2003     Document Type: Article

References (65)

1. Baylor DA, Lamb TD, and Yau KW. Responses of retinal rods to single photons. J Physiol 288: 613-634, 1979.
2. Burns ME and Baylor DA. Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci 24: 779-805, 2001.
3. Burton BG. Long-term light adaptation in photoreceptors of the housefly, Musca domestica. J Comp Physiol A Sens Neural Behav Physiol 188: 527-538, 2002.
4. Burton BG and Laughlin SB. Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica. J Exp Biol 15: 3963-3977, 2003.
5. Burton BG, Tatler BW, and Laughlin SB. Variations in photoreceptor response dynamics across the fly retina. J Neurophysiol 86: 950-960, 2001.
6. Burton GJ and Moorhead IR. Visual form perception and the spatial phase transfer function. J Opt Soc Am 71: 1056-1063, 1981.
7. Chacron MJ, Doiron B, Maler L, Longtin A, and Bastian J. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423: 77-81, 2003.
8. Connor JA and Stevens CF. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21-30, 1971.
9. Dan Y, Atick JJ, and Reid RC. Efficient coding of natural scenes in the lateral geniculate nucleus: experimental test of a computational theory. J Neurosci 16: 3351-3362, 1996.
10. David CT. The relationship between body angle and flight speed in free-flying Drosophila. Physiol Ent 3: 191-195, 1978.
11. Fain GL, Matthews HR, Cornwall MC, and Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev 81: 117-151, 2001.
12. Field DJ. Relations between the statistics of natural images and the response properties of cortical cells. J Opt Soc Am A 4: 2379-2394, 1987.
13. French AS. Phototransduction in the fly compound eye exhibits temporal resonances and a pure time delay. Nature 283: 200-202, 1980.
14. French AS and Korenberg MJ. A nonlinear cascade model for action potential encoding in an insect sensory neuron. Biophys J 55: 655-661, 1989.
15. French AS, Korenberg MJ, Järvilehto M, Kouvalainen E, Juusola M, and Weckström, M. The dynamic nonlinear behavior of fly photoreceptors evoked by a wide range of light intensities. Biophys J 65: 832-839, 1993.
16. French AS and Marmarelis VZ. Nonlinear analysis of neuronal systems. In: Modern Techniques in Neuroscience Research, edited by Windhorst U and Johansson H. Berlin: Springer-Verlag, 1999, p. 627-640.
17. French AS, Sekizawa S, Höger U, and Torkkeli PH. Predicting the responses of mechanoreceptor neurons to physiological inputs by nonlinear system identification. Ann Biomed Eng 29: 187-194, 2001.
18. Fry SN, Sayaman R, and Dickinson MH. The aerodynamics of free flight maneuvers in Drosophila. Science 300: 495-498, 2003.
19. +/Ca(2+)-exchange in blowfly Calliphora photoreceptors. Vision Res 37: 2477-2485, 1997.
20. +-pump activity in photoreceptors of the blowfly Calliphora: a model analysis based on membrane potential measurements. J Comp Physiol A Sens Neural Behav Physiol 180: 113-122, 1997.
21. Hardie RC. Voltage-sensitive potassium channels in Drosophila photoreceptors. J Neurosci 11: 3079-3095, 1991.
22. 2+ and TRP. Cell Calcium 18: 256-274, 1995.
23. Hardie RC, Voss D, Pongs O, and Laughlin SB. Novel potassium channels encoded by the Shaker locus in Drosophila photoreceptors. Neuron 6: 477-486, 1991.
24. 2+. J Physiol 524: 179-194, 2000.
25. Hevers W and Hardie RC. Serotonin modulates the voltage dependence of delayed rectifier and Shaker potassium channels in Drosophila photoreceptors. Neuron 14: 845-856, 1995.
26. Juusola M and de Polavieja GG. The rate of information transfer of naturalistic stimulation by graded potentials. J Gen Physiol 122: 191-206, 2003.
27. Juusola M and Hardie RC. Light adaptation in Drosophila photoreceptors. I. Response dynamics and signaling efficiency at 25 degrees C. J Gen Physiol 117: 3-25, 2001.
28. Juusola M, Kouvalainen E, Järvilehto M, and Weckström M. Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. J Gen Physiol 104: 593-621, 1994.
29. + channels contribute early nonlinear amplification to the light response in Drosophila photoreceptors. J Neurophysiol 90: 2014-2021, 2003.
30. Kaplan WD and Trout WE. The behavior of four neurological mutants of Drosophila. Genetics 61: 399-409, 1961.
31. Katz LC and Shatz CJ. Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138, 1996.
32. Korenberg MJ. Parallel cascade identification and kernel estimation for nonlinear systems. Ann Biomed Eng 19: 429-455, 1991.
33. Korenberg MJ and Hunter IW. The identification of nonlinear biological systems: LNL cascade models. Biol Cybern 55: 125-134, 1986.
34. Laughlin SB and Hardie RC. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J Comp Physiol 128: 319-340, 1978.
35. Lewen GD, Bialek W, and de Ruyter van Steveninck RR. Neural coding of naturalistic motion stimuli. Network 12: 317-329, 2001.
36. Marmarelis PZ and Marmarelis VZ. Analysis of Physiological Systems: The White-Noise Approach. New York: Plenum Press, 1978.
37. Montell C. Visual transduction in Drosophila. Annu Rev Cell Dev Biol 15: 231-268, 1999.
38. Niven JE and Burrows M. Spike width reduction modifies the dynamics of short-term depression at a central synapse in the locust. J Neurosci 23: 7461-7469, 2003.
39. Niven JE, Vähäsöyrinki M, and Juusola M. Shaker K(+)-channels are predicted to reduce the metabolic cost of neural information in Drosophila photoreceptors. Proc R Soc Lond B Biol Sci 270, Suppl. 1: S58-S61, 2003.
40. Niven JE, Vähäsöyrinki M, Kauranen M, Hardie RC, Juusola M, and Weckström M. The contribution of Shaker K(+) channels to the information capacity of Drosophila photoreceptors. Nature 421: 630-634, 2003.
41. Oberwinkler J and Stavenga DG. Calcium transients in the rhabdomeres of dark- and light-adapted fly photoreceptor cells. J Neurosci 20: 1701-1709, 2000.
42. Press WH, Flannery BP, Teukolsky SA, and Vetterling WT. Numerical Recipes in C. The Art of Scientific Computing. Cambridge, UK: Cambridge Univ. Press, 1990.
43. Pugh EN Jr, Nikonov S, and Lamb TD. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9: 410-418, 1999.
44. Reinagel P. How do visual neurons respond in the real world? Curr Opin Neurobiol 11: 437-442, 2001.
45. Reuss H, Mojet MH, Chyb S, and Hardie RC. In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron 19: 1249-1259, 1997.
46. Rieke F, Bodnar DA, and Bialek W. Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc R Soc Lond B Biol Sci 262: 259-265, 1995.
47. Rinberg D and Davidowitz H. A stimulus generating system for studying wind sensation in the American cockroach. J Neurosci Methods 121: 1-11, 2002.
48. Ruderman DL and Bialek W. Statistics of natural images: scaling in the woods. Phys Rev Lett 73: 814-817, 1994.
49. Salkoff L and Wyman R. Genetic modification of potassium channels in Drosophila Shaker mutants. Nature 293: 228-230, 1981.
50. Srinivasan MV, Laughlin SB, and Dubs A. Predictive coding: a fresh view of inhibition in the retina. Proc R Soc Lond B Biol Sci 216: 427-459, 1982.
51. Tolhurst DJ, Tadmor Y, and Chao T. Amplitude spectra of natural images. Ophthalmic Physiol Opt 12: 229-232, 1992.
52. van Hateren JH. Electrical coupling of neuro-ommatidial photoreceptor cells in the blowfly. J Comp Physiol A Sens Neural Behav Physiol 158: 795-811, 1986.
53. van Hateren JH. Processing of natural time series of intensities by the visual system of the blowfly. Vision Res 37: 3407-3416, 1997.
54. van Hateren JH and Snippe HP. Information theoretical evaluation of parametric models of gain control in blowfly photoreceptor cells. Vision Res 41: 1851-1865, 2001.
55. Vickers NJ, Christensen TA, Baker TC, and Hildebrand JG. Odour-plume dynamics influence the brain's olfactory code. Nature 410: 466-470, 2001.
56. Vinje WE and Gallant JL. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287: 1273-1276, 2000.
57. Vinje WE and Gallant JL. Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. J Neurosci 22: 2904-2915, 2002.
58. Weckström M, Hardie RC, and Laughlin SB. Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. J Physiol 440: 635-657, 1991.
59. Weckström M and Laughlin SB. Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci 18: 17-21, 1995.
60. Wolfram V, Niven JE, and Juusola M. Experience-dependent plasticity, gain control and information capacity in Drosophila photoreceptors. Proc 29th Göttingen Neurobiol Conf Abstr. 529, 2003.
61. Wong F, Knight BW, and Dodge FA. Dispersion of latencies in photoreceptors of Limulus and the adapting bump model. J Gen Physiol 76: 517-537, 1980.
62. Wu CF and Pak WL. Quantal basis of photoreceptor spectral sensitivity of Drosophila melanogaster. J Gen Physiol 66: 149-168, 1975.
63. Wu CF and Pak WL. Light-induced voltage noise in the photoreceptor of Drosophila melanogaster. J Gen Physiol 71: 249-268, 1978.
64. Yeandle S. Statistics and quantum bumps in arthropod photoreceptors. Fed Proc 44: 2947-2949, 1985.
65. Zettler F. Die Abhangigkeit des Übertragungsverhaltens von Frequenz und Adaptionszustand; gemessen am einzelnen Lichtrezeptor von Calliphora erythrocephala. Z Vergl Physiol 64: 432-449, 1969.