Direction-selective adaptation in fly visual motion-sensitive neurons is generated by an intrinsic conductance-based mechanism

Neuroscience

Volumn 146, Issue 2, 2007, Pages 573-583

  Kurtz, R ^a  

^a BIELEFELD UNIVERSITY   (Germany)

Author keywords

after hyperpolarization; blowfly; Ca2+ activated K+ channels; caged Ca2+; input resistance; visual system

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION;

ADAPTATION; AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; FLY; NERVE CONDUCTION; NERVE STIMULATION; NONHUMAN; OPTIC NERVE; PHOTOLYSIS; PRIORITY JOURNAL; ULTRAVIOLET RADIATION; VISION; VISUAL SYSTEM;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; CALCIUM; CALCIUM SIGNALING; DENDRITES; ELECTRIC IMPEDANCE; FEMALE; INSECTS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURONS; ORIENTATION; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTOLYSIS;

EID: 34247246811     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.01.058     Document Type: Article

References (61)

1. Anderson J.S., Carandini M., and Ferster D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84 (2000) 909-926
2. Benda J., Longtin A., and Maler L. Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25 (2005) 2312-2321
3. 2+. Trends Neurosci 28 (2005) 422-428
4. Borst A., and Egelhaaf M. In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc Natl Acad Sci U S A 89 (1992) 4139-4143
5. Borst A., Flanagin V.L., and Sompolinsky H. Adaptation without parameter change: Dynamic gain control in motion detection. Proc Natl Acad Sci U S A 102 (2005) 6172-6176
6. Borst A., and Haag J. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: I. Passive membrane properties. J Comput Neurosci 3 (1996) 313-336
7. Borst A., and Haag J. Neural networks in the cockpit of the fly. J Comp Physiol [A] 188 (2002) 419-437
8. Brenner N., Bialek W., and de Ruyter van Steveninck R.R. Adaptive rescaling maximizes information transmission. Neuron 26 (2000) 695-702
9. Brotz T.M., and Borst A. Cholinergic and GABAergic receptors on fly tangential cells and their role in visual motion detection. J Neurophysiol 76 (1996) 1786-1799
10. Carandini M. Visual cortex: Fatigue and adaptation. Curr Biol 10 (2000) R605-R607
11. Carandini M., and Ferster D. A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276 (1997) 949-952
12. Chung S., Li X., and Nelson S.B. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34 (2002) 437-446
13. Clifford C.W., and Ibbotson M.R. Fundamental mechanisms of visual motion detection: models, cells and functions. Prog Neurobiol 68 (2002) 409-437
14. Crowder N.A., Price N.S.C., Hietanen M.A., Dreher B., Clifford C.W.G., and Ibbotson M.R. Relationship between contrast adaptation and orientation tuning in V1 and V2 of cat visual cortex. J Neurophysiol 95 (2006) 271-283
15. Dragoi V., Sharma J., Miller E.K., and Sur M. Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5 (2002) 883-891
16. Dragoi V., Sharma J., and Sur M. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28 (2000) 287-298
17. Dürr V., and Egelhaaf M. In vivo calcium accumulation in presynaptic and postsynaptic dendrites of visual interneurons. J Neurophysiol 82 (1999) 3327-3338
18. Eckert H. The horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J Comp Physiol [A] 143 (1981) 511-526
19. Eckert H., and Dvorak D.R. The centrifugal horizontal cells in the lobula plate of the blowfly, Phaenicia sericata. J Insect Physiol 29 (1983) 547-560
20. Egelhaaf M., and Borst A. Transient and steady-state response properties of movement detectors. J Opt Soc Am A 6 (1989) 116-127
21. Egelhaaf M., and Borst A. Calcium accumulation in visual interneurons of the fly: stimulus dependence and relationship to membrane potential. J Neurophysiol 73 (1995) 2540-2552
22. Egelhaaf M., Grewe J., Karmeier K., Kern R., Kurtz R., and Warzecha A.K. Novel approaches to visual information processing in insects: case studies on neuronal computations in the blowfly. In: Christensen T.A. (Ed). Methods in insect sensory neuroscience (2005), CRC Press, Boca Raton 185-212
23. Egelhaaf M., Kern R., Krapp H.G., Kretzberg J., Kurtz R., and Warzecha A.-K. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends Neurosci 25 (2002) 96-102
24. Fain G.L., Matthews H.R., Cornwall M.C., and Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev 81 (2001) 117-151
25. Fettiplace R., and Ricci A.J. Adaptation in auditory hair cells. Curr Opin Neurobiol 13 (2003) 446-451
26. Götz K.G., and Wenking H. Visual control of locomotion in walking fruitfly Drosophila. J Comp Physiol 85 (1973) 235-266
27. Gurney A.M., Tsien R.Y., and Lester H.A. Activation of a potassium current by rapid photochemically generated step increases of intracellular calcium in rat sympathetic neurons. Proc Natl Acad Sci U S A 84 (1987) 3496-3500
28. Haag J., and Borst A. Dendro-dendritic interactions between motion-sensitive large-field neurons in the fly. J Neurosci 22 (2002) 3227-3233
29. Haag J., Theunissen F., and Borst A. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: II. Active membrane properties. J Comput Neurosci 4 (1997) 349-369
30. Harris R.A., O'Carroll D.C., and Laughlin S.B. Contrast gain reduction in fly motion adaptation. Neuron 28 (2000) 595-606
31. Hausen K. Motion sensitive interneurons in the optomotor system of the fly: I. The horizontal cells: structure and signals. Biol Cybern 45 (1982) 143-156
32. Hengstenberg R. Spike responses of 'non-spiking' visual interneurone. Nature 270 (1977) 338-340
33. Hengstenberg R. Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J Comp Physiol [A] 149 (1982) 179-193
34. Huk A.C., Rees D., and Heeger D.J. Neuronal basis of the motion aftereffect reconsidered. Neuron 32 (2001) 161-172
35. Ibbotson M.R., Clifford C.W., and Mark R.F. Adaptation to visual motion in directional neurons of the nucleus of the optic tract. J Neurophysiol 79 (1998) 1481-1493
36. Kirschfeld K., and Franceschini N. Evidence for a sensitising pigment in fly photoreceptors. Nature 269 (1977) 386-390
37. Kohn A., and Movshon J.A. Adaptation changes the direction tuning of macaque MT neurons. Nat Neurosci 7 (2004) 764-772
38. Krekelberg B., Boynton G.M., and van Wezel R.J. Adaptation: from single cells to BOLD signals. Trends Neurosci 29 (2006) 250-256
39. Kurahashi T., and Menini A. Mechanism of odorant adaptation in the olfactory receptor cell. Nature 385 (1997) 725-729
40. 2+. J Neurophysiol 92 (2004) 458-467
41. Kurtz R., Dürr V., and Egelhaaf M. Dendritic calcium accumulation associated with direction-selective adaptation in visual motion-sensitive neurons in vivo. J Neurophysiol 84 (2000) 1914-1923
42. Kurtz R., Warzecha A.K., and Egelhaaf M. Transfer of visual motion information via graded synapses operates linearly in the natural activity range. J Neurosci 21 (2001) 6957-6966
43. Lancaster B., Nicoll R.A., and Perkel D.J. Calcium activates two types of potassium channels in rat hippocampal neurons in culture. J Neurosci 11 (1991) 23-30
44. + current in rat hippocampal neurones. J Physiol 475 (1994) 229-239
45. Maddess T., and Laughlin S.B. Adaptation of the motion-sensitive neuron H1 is generated locally and governed by contrast frequency. Proc R Soc Lond B Biol Sci 228 (1985) 251-275
46. Manookin M.B., and Demb J.B. Presynaptic mechanisms for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50 (2006) 453-464
47. Neri P., and Laughlin S.B. Global versus local adaptation in fly motion-sensitive neurons. Proc Biol Sci 272 (2005) 2243-2249
48. Oertner T.G., Brotz T.M., and Borst A. Mechanisms of dendritic calcium signaling in fly neurons. J Neurophysiol 85 (2001) 439-447
49. Osmanovic S.S., and Shefner S.A. Calcium-activated hyperpolarizations in rat locus coeruleus neurons in vitro. J Physiol 469 (1993) 89-109
50. 2+]i reveals slow kinetics of potassium channels underlying the afterhyperpolarization in hippocampal pyramidal neurons. J Neurosci 19 (1999) 3657-3664
51. Sanchez-Vives M.V., Nowak L.G., and McCormick D.A. Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 20 (2000) 4286-4299
52. Sanchez-Vives M.V., Nowak L.G., and McCormick D.A. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20 (2000) 4267-4285
53. Schwindt P.C., Spain W.J., and Crill W.E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol 61 (1989) 233-244
54. Schwindt P.C., Spain W.J., and Crill W.E. Effects of intracellular calcium chelation on voltage-dependent and calcium-dependent currents in cat neocortical neurons. Neuroscience 47 (1992) 571-578
55. Sengpiel F., and Bonhoeffer T. Orientation specificity of contrast adaptation in visual cortical pinwheel centres and iso-orientation domains. Eur J Neurosci 15 (2002) 876-886
56. Single S., and Borst A. Dendritic integration and its role in computing image velocity. Science 281 (1998) 1848-1850
57. Single S., and Borst A. Different mechanisms of calcium entry within different dendritic compartments. J Neurophysiol 87 (2002) 1616-1624
58. Single S., Haag J., and Borst A. Dendritic computation of direction selectivity and gain control in visual interneurons. J Neurosci 17 (1997) 6023-6030
59. Srinivasan M.V., and Dvorak D.R. The waterfall illusion in an insect visual system. Vision Res 19 (1979) 1435-1437
60. Tolias A.S., Smirnakis S.M., Augath M.A., Trinath T., and Logothetis N.K. Motion processing in the macaque: revisited with functional magnetic resonance imaging. J Neurosci 21 (2001) 8594-8601
61. + channels. Nat Neurosci 3 (2000) 566-571