Motion adaptation leads to parsimonious encoding of natural optic flow by blowfly motion vision system

Journal of Neurophysiology

Volumn 94, Issue 3, 2005, Pages 1761-1769

  Heitwerth, J ^a   Kern, R ^a   Van Hateren, J H ^b   Egelhaaf, M ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ARTICLE; FEMALE; FLY; MOTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; VELOCITY; VISION; VISUAL NERVOUS SYSTEM; VISUAL STIMULATION;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; COMPUTER SIMULATION; DIPTERA; FEMALE; LINEAR MODELS; MODELS, NEUROLOGICAL; MOTION; NEURONS; PHOTIC STIMULATION; REACTION TIME; TIME FACTORS; VISUAL PATHWAYS;

EID: 23944508493     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00308.2005     Document Type: Article

References (50)

1. Attwell D and Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21: 1133-1145, 2001.
2. Azouz R and Gray CM. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37: 513-523, 2003.
3. Barberini CL, Horwitz GD, and Newsome WT. A comparison of spiking statistics in motion sensing neurones of flies and monkeys. In: Motion Vision-Computational, Neural, and Ecological Constraints, edited by Zanker JM and Zeil J. New York: Springer Verlag, 2001.
4. Barlow HB and Hill RM. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139: 412-414, 1963.
5. Bendat JS and Piersol AG. Random Data: Analysis and Measurement Procedures. New York: Wiley-Interscience, 2000.
6. Borst A and Egelhaaf M. Temporal modulation of luminance adapts time constant of fly movement detector. Biol Cybern 56: 209-215, 1987.
7. Borst A, Flanagin VL, and Sompolinsky H. Adaptation without parameter change: dynamic gain control in motion detection. Proc Natl Acad Sci USA 102: 6172-6176, 2005.
8. Borst A and Haag J. Effects of mean firing on neural information rate. J Comput Neurosci 10: 213-221, 2001.
9. Borst A, Reisenman C, and Haag J. Adaptation of response transients in fly motion vision. II: Model studies. Vision Res 43: 1311-1324, 2003.
10. Brenner N, Strong SP, Koberle R, Bialek W, and de Ruyter van Steveninck R. Synergy in a neural code. Neural Comput 12: 1531-1552, 2000.
11. Clifford CW, Ibbotson MR, and Langley K. An adaptive Reichardt detector model of motion adaptation in insects and mammals. Vis Neurosci 14: 741-749, 1997.
12. de Ruyter van Steveninck RR, Lewen GD, Strong SP, Koberle R, and Bialek W. Reproducibility and variability in neural spike trains. Science 275: 1805-1808, 1997.
13. de Ruyter van Steveninck RR, Zaagman WH, and Mastebroek HAK. Adaptation of transient responses of a movement-sensitive neuron in the visual system of the blowfly Calliphora erythrocephala. Biol Cybern 54: 223-236, 1986.
14. Dror RO, O'Carroll DC, and Laughlin SB. Accuracy of velocity estimation by Reichardt correlators. J Opt Soc Am A Opt Image Sci Vis 18: 241-252, 2001.
15. Dürr V and Egelhaaf M. In vivo calcium accumulation in presynaptic and postsynaptic dendrites of visual interneurons. J Neurophysiol 82: 3327-3338, 1999.
16. Eckert H. Functional properties of the H1 neuron in the third optical ganglion of the blowfly, Phaenecia. J Comp Physiol A Sens Neural Behav Physiol 29-39, 1980.
17. Fairhall AL, Lewen GD, Bialek W, and de Ruyter van Steveninck RR. Efficiency and ambiguity in an adaptive neural code. Nature 412: 787-792, 2001.
18. Giaschi D, Douglas R, Marlin S, and Cynader M. The time course of direction-selective adaptation in simple and complex cells in cat striate cortex. J Neurophysiol 70: 2024-2034, 1993.
19. Harris RA and O'Carroll DC. Afterimages in fly motion vision. Vision Res 42: 1701-1714, 2002.
20. Harris RA, O'Carroll DC, and Laughlin SB. Adaptation and the temporal delay filter of fly motion detectors. Vision Res 39: 2603-2613, 1999.
21. Harris RA, O'Carroll DC, and Laughlin SB. Contrast gain reduction in fly motion adaptation. Neuron 28: 595-606, 2000.
22. Hausen K. Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneurone im dritten optischen Nueropil der Schmeißfliege Calliphora erythrocephala (Dissertation). Tübingen, Germany: Universität Tübingen, 1976.
23. Hausen K and Egelhaaf M. Neural mechanisms of visual course control in insects. In: Facets of Vision, edited by Stavenga D and Hardie RC. New York: Springer-Verlag, 1989, p. 391-424.
24. Ibbotson MR and Mark RF. Impulse responses distinguish two classes of directional motion-sensitive neurons in the nucleus of the optic tract. J Neurophysiol 75: 996-1007, 1996.
25. Kern R, van Hateren JH, Michaelis C, Lindemann JP, and Egelhaaf M. Function of a fly motion-sensitive neuron matches eye movements during free flight. PLoS Biol 3: e171, 2005.
26. Kohn A and Movshon JA. Neuronal adaptation to visual motion in area MT of the macaque. Neuron 39: 681-691, 2003.
27. Kohn A and Movshon JA. Adaptation changes the direction tuning of macaque MT neurons. Nat Neurosci 7: 764-772, 2004.
28. 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: 1914-1923, 2000.
29. Lewen GD, Bialek W, and de Ruyter van Steveninck RR. Neural coding of naturalistic motion stimuli. Network 12: 317-329, 2001.
30. Lindemann JP, Kern R, Michaelis C, Meyer P, van Hateren JH, and Egelhaaf M. FliMax, a novel stimulus device for panoramic and highspeed presentation of behaviourally generated optic flow. Vision Res 43: 779-791, 2003.
31. Lindemann JP, Kern R, van Hateren JH, Ritter H, and Egelhaaf M. On the computations analysing natural optic flow: quantitative model analysis of the blowfly motion vision pathway. J Neurosci In press.
32. Maddess T and Laughlin SB. Adaptation of the motion-sensitive neuron H1 is generated locally and governed by contrast frequency. Proc R Soc Lond B Biol Sci 225: 251-275, 1985.
33. Marlin S, Douglas R, and Cynader M. Position-specific adaptation in complex cell receptive fields of the cat striate cortex. J Neurophysiol 69: 2209-2221, 1993.
34. Marlin SG, Douglas RM, and Cynader MS. Position-specific adaptation in simple cell receptive fields of the cat striate cortex. J Neurophysiol 66: 1769-1784, 1991.
35. Panzeri S, Petersen RS, Schultz SR, Lebedev M, and Diamond ME. The role of spike timing in the coding of stimulus location in rat somatosensory cortex. Neuron 29: 769-777, 2001.
36. Reisenman C, Haag J, and Borst A. Adaptation of response transients in fly motion vision. I: Experiments. Vision Res 43: 1291-1307, 2003.
37. Schilstra C and van Hateren JH. Stabilizing gaze in flying blowflies. Nature 395: 654, 1998.
38. Schilstra C and van Hateren JH. Blowfly flight and optic flow. 1. Thorax kinematics and flight dynamics. J Exp Biol 202: 1481-1490, 1999.
39. Schneidman E, Brenner N, Tishby N, de Ruyter van Steveninck R, and Bialek W. Universality and individuality in a neural code. In: Advances in Neural Information Processing, edited by Leem TKDTTV. Cambridge, MA: MIT Press, 2001, vol. 13, p. 151-165.
40. Srinivasan MV and Dvorak DR. The waterfall illusion in an insect visual system. Vision Res 19: 1435-1437, 1979.
41. Stavenga DG, Schwering PBW, and Tinbergen J. A three-compartment model describing temperature changes in tethered flying blowflies. J Exp Biol 185: 326-333, 1993.
42. Tolhurst DJ, Movshon JA, and Dean AF. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23: 775-785, 1983.
43. van Hateren JH, Kern R, Schwerdtfeger G, and Egelhaaf M. Function and coding in the blowfly H1 neuron during naturalistic optic flow. J Neurosci 25: 4343-4352, 2005.
44. van Hateren JH, Ruttiger L, Sun H, and Lee BB. Processing of natural temporal stimuli by macaque retinal ganglion cells. J Neurosci 22: 9945-9960, 2002.
45. van Hateren JH and Schilstra C. Blowfly flight and optic flow. II. Head movements during flight. J Exp Biol 202: 1491-1500, 1999.
46. 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.
47. Vogels R, Spileers W, and Orban GA. The response variability of striate cortical neurons in the behaving monkey. Exp Brain Res 77: 432-436, 1989.
48. Warzecha AK and Egelhaaf M. Variability in spike trains during constant and dynamic stimulation. Science 283: 1927-1930, 1999.
49. Warzecha AK, Kretzberg J, and Egelhaaf M. Reliability of a fly motion-sensitive neuron depends on stimulus parameters. J Neurosci 20: 8886-8896, 2000.
50. Zaagman WH, Mastebroek HAK, and de Ruyter van Steveninck R. Adaptive strategies in fly vision: on their image-processing qualities. IEEE Trans Syst Man Cybern 5: 900-906, 1983.