Implications of functionally different synaptic inputs for neuronal gain and computational properties of fly visual interneurons

Journal of Neurophysiology

Volumn 96, Issue 4, 2006, Pages 1838-1847

  Grewe, Jan ^a,b   Matos, Nélia ^a   Egelhaaf, Martin ^a   Warzecha, Anne Kathrin ^a,b  

^a BIELEFELD UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FLY; IN VIVO STUDY; INTERNEURON; MEMBRANE POTENTIAL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RECORDING; SENSORY STIMULATION; SYNAPTIC MEMBRANE; VISUAL STIMULATION;

ANIMALS; BEHAVIOR, ANIMAL; DIPTERA; ELECTROPHYSIOLOGY; FEMALE; GANGLIA, INVERTEBRATE; INTERNEURONS; MOVEMENT; NEURONS, AFFERENT; SYNAPSES; VISUAL PERCEPTION;

EID: 33749533071     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00170.2006     Document Type: Article

References (54)

1. Anderson JS, Lampl I, Gillespie DC, and Ferster D. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290: 1968-1972, 2000.
2. Azouz R and Gray CM. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209-2223, 1999.
3. Berman NJ, Douglas RJ, and Martin KA. GABA-mediated inhibition in the neural networks of visual cortex. Prog Brain Res 90: 443-476, 1992.
4. Bialek W, Rieke F, de Ruyter van Steveninck RR, and Warland D. Reading a neural code. Science 252: 1854-1857, 1991.
5. Borst A, Egelhaaf M, and Haag J. Mechanisms of dendritic integration underlying gain control in fly motion-sensitive interneurons. J Comput Neurosci 2: 5-18, 1995.
6. Borst A and Haag J. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells. I. Passive membrane properties. J Comput Neurosci 3: 313-336, 1996.
7. Borst A and Haag J. Neural networks in the cockpit of the fly. J Comp Physiol A Sens Neural Behav Physiol 188: 419-437, 2002.
8. Brenner N, Strong SP, Koberle R, Bialek W, and de Ruyter van Steveninck RR. Synergy in a neural code. Neural Comput 12: 1531-1552, 2000.
9. Brotz TM, Gundelfinger ED, and Borst A. Cholinergic and GABAergic receptors on fly tangential cells and their role in visual motion detection. J Neurophysiol 76: 1786-1799, 1996.
10. Buchner E. Elementary movement detectors in an insect visual system. Biol Cybern 24: 85-101, 1976.
11. Carandini M and Heeger DJ. Summation and division by neurons in primate visual cortex. Science 264: 1333-1336, 1994.
12. Carandini M, Heeger DJ, and Movshon JA. Linearity and normalization in simple cells of the macaque primary visual cortex. J Neurosci 17: 8621-8644, 1997.
13. Chance FS, Abbott LF, and Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
14. Churan J and Ilg UJ. Flicker in the visual background impairs the ability to process a moving visual stimulus. Eur J Neurosci 16: 1151-1162, 2002.
15. Connors BW, Malenka RC, and Silva LR. Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol 406: 443-468, 1988.
16. Destexhe A, Rudolph M, and Paré D. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751, 2003.
17. Egelhaaf M and Borst A. Motion computation and visual orientation in flies. Comp Biochem Physiol 104A: 659-673, 1993.
18. Egelhaaf M, Grewe J, Karmeier K, Kern R, Kurtz R, and Warzecha A-K. Novel approaches to visual processing in insects: case studies on neuronal computations in the blowfly. In: Methods in Insect Sensory Neuroscience, edited by Christensen TA. Boca Raton, FL: CRC Press, 2005, p. 185-212.
19. Egelhaaf M, Kern R, Krapp HG, Kretzberg J, Kurtz R, and Warzecha A-K. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends Neurosci 25: 96-102, 2002.
20. Egelhaaf M and Warzecha A-K. Encoding of motion in real time by the fly visual system. Curr Opin Neurobiol 9: 454-460, 1999.
21. Fellous JM, Rudolph M, Destexhe A, and Sejnowski TJ. Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122: 811-829, 2003.
22. Franceschini N. Sampling of the visual environment by the compound eye of the fly: fundamentals and applications. In: Photoreceptor Optics, edited by Snyder AW and Menzel R. New York: Springer-Verlag, 1975, p. 98-125.
23. Gilbert C, Gronenberg W, and Strausfeld NJ. Oculomotor control in calliphorid flies: head movements during activation and inhibitions of neck motor neurons corroborate neuroanatomical predictions. J Comp Neurol 361: 285-297, 1995.
24. Gronenberg W, Milde JJ, and Strausfeld NJ. Oculomotor control in calliphorid flies: organization of descending neurons to neck motor neurons responding to visual stimuli. J Comp Neurol 361: 267-284, 1995.
25. Haag J and Borst A. Active membrane properties and signal encoding in graded potential neurons. J Neurosci 18: 7972-7986, 1998.
26. Hausen K. Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala. Z Naturforsch 31c: 629-633, 1976.
27. Hausen K. Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol Cybern 45: 143-156, 1982a.
28. Hausen K. Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive field organization and response characteristics. Biol Cybern 46: 67-79, 1982b.
29. Hausen K. The lobula-complex of the fly: structure, function and significance in visual behaviour. In: Photoreception and Vision in Invertebrates, edited by Ali MA. New York: Plenum Press, 1984, p. 523-559.
30. Heitwerth J, Kern R, van Hateren JH, and Egelhaaf M. Motion adaptation leads to parsimonious encoding of natural optic flow by blowfly motion vision system. J Neurophysiol 94: 1761-1769, 2005.
31. Hengstenberg R. Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J Comp Physiol 149: 179-193, 1982.
32. Holt GR and Koch C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9: 1001-1013, 1997.
33. Karmeier K, Krapp HG, and Egelhaaf M. Population coding of self-motion: applying Bayesian analysis to a population of visual interneurons in the fly. J Neurophysiol 94: 2182-2194, 2005.
34. Karmeier K, van Hateren JH, Kern R, and Egelhaaf M. Encoding of naturalistic optic flow by a population of blowfly motion sensitive neurons. J Neurophysiol 96: 1602-1614, 2006.
35. 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.
36. Koch C, Poggio T, and Torre V. Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci USA 80: 2799-2802, 1983.
37. Krapp HG, Hengstenberg B, and Hengstenberg R. Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J Neurophysiol 79: 1902-1917, 1998.
38. Krapp HG, Hengstenberg R, and Egelhaaf M. Binocular contributions to optic flow processing in the fly visual system. J Neurophysiol 85: 724-734, 2001.
39. Kretzberg J, Egelhaaf M, and Warzecha AK. Membrane potential fluctuations determine the precision of spike timing and synchronous activity: a model study. J Comput Neurosci 10: 79-97, 2001.
40. Milde JJ, Gronenberg W, and Strausfeld NJ. Oculomotor control in calliphorid flies: organization of descending neurons to neck motor neurons responding to visual stimuli. J Comp Neurol 361: 267-284, 1995.
41. Mitchell SJ and Silver RA. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38: 433-445, 2003.
42. Prescott SA and De Koninck Y. Gain control of firing rate by shunting inhibition: roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci USA 100: 2076-2081, 2003.
43. Prinz AA, Abbott LF, and Marder E. The dynamic clamp comes of age. Trends Neurosci 27: 218-224, 2004.
44. Reichardt W, Poggio T, and Hausen K. Figure-ground discrimination by relative movement in the visual system of the fly. Part II. Towards the neural circuitry. Biol Cybern Suppl 46: 1-30, 1983.
45. Schuling FH, Mastebroek HAK, Bult R, and Lenting BPM. Properties of elementary movement detectors in the fly Calliphora erythrocephala. J Comp Physiol A Sens Neural Behav Physiol 165: 179-192, 1989.
46. Sherman SM and Guillery RW. On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators." Proc Natl Acad Sci USA 95: 7121-7126, 1998.
47. Single S, Haag J, and Borst A. Dendritic computation of direction selectivity and gain control in visual interneurons. J Neurosci 17: 6023-6030, 1997.
48. Strausfeld NJ, Seyan HS, and Milde JJ. The neck motor system of the fly Calliphora erythrocephala. I. Muscles and motor neurons. J Comp Physiol A Sens Neural Behav Physiol 160: 205-224, 1987.
49. van Hateren JH, Kern R, Schwertfeger G, and Egelhaaf M. Function and coding in the blowfly H1 neuron during naturalistic optic flow. J Neurosci 25: 4343-4352, 2005.
50. 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.
51. Warzecha AK, Egelhaaf M, and Borst A. Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques. J Neurophysiol 69: 329-339, 1993.
52. Warzecha AK, Kretzberg J, and Egelhaaf M. Temporal precision of the encoding of motion information by visual interneurons. Curr Biol 8: 359-368, 1998.
53. Warzecha AK, Kretzberg J, and Egelhaaf M. Reliability of a fly motion-sensitive neuron depends on stimulus parameters. J Neurosci 20: 8886-8896, 2000.
54. Wiesenfeld K and Moss F. Stochastic resonance and the benefits of noise: from ice ages to crayfish and squids. Nature 373: 33-36, 1995.