Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway

Journal of Experimental Biology

Volumn 213, Issue 15, 2010, Pages 2629-2639

  Simmons, Peter J ^a   De Ruyter Van Steveninck, Rob R ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Coding; Flight; Information; Locust; Ocellus; Precision; Spike

Indexed keywords

ACTION POTENTIAL; ANIMAL; ARTICLE; BRAIN; CYTOLOGY; EFFERENT NERVE; GRASSHOPPER; LIGHT; MOVEMENT (PHYSIOLOGY); NERVE CELL; NERVE FIBER; PHOTOSTIMULATION; PHYSIOLOGY; RADIATION EXPOSURE; SENSATION; SYNAPTIC POTENTIAL; TIME; CAELIFERA; RADIATION RESPONSE;

ACTION POTENTIALS; ANIMALS; AXONS; BRAIN; EFFERENT PATHWAYS; GRASSHOPPERS; LIGHT; MOVEMENT; NEURONS; PHOTIC STIMULATION; SENSATION; SYNAPTIC POTENTIALS; TIME FACTORS;

HEXAPODA;

EID: 77954853756     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.043547     Document Type: Article

References (73)

1. Adrian, E. D. and Zotterman, Y. (1926). The impulses produced by sensory nerve endings: Part II: the response of a single end organ. J. Physiol. 61, 151-171.
2. Ammermüller, J. and Zettler, F. (1986). Time-dependent and voltage-dependent currents in locust ocellar L-neurons. J. Comp. Physiol. A 159, 363-376.
3. Bacon, J. and Möhl, B. (1979). Activity of an identified wind interneurone in a flying locust. Nature 278, 638-640.
4. Bacon, J. and Möhl, B. (1983). The tritocerebral commissure giant (TCG) windsensitive interneurone in the locust-I. Its activity in straight flight. J. Comp. Physiol. A 150, 439-452.
5. Bair, W. and Koch, C. T. (1996). Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 8, 1185-1202.
6. Berry, R., Stange, G., Oldberg, R. and van Kleef, J. (2006). The mapping of visual space by identified large second-order neurons in the dragonfly median ocellus J. Comp. Physiol. A. 192, 1105-1123.
7. Billimoria, C. P., DiCaprio, R. A., Birmingham, J. T., Abbott, L. F. and Marder, E. (2006). Neuromodulation of spike-timing precision in sensory neurons. J. Neurosci. 26, 5910-5919.
8. Borst, A. and Theunissen, F. E. (1999). Information theory and neural coding. Nat. Neurosci. 2, 947-957.
9. Brenner, N., Bialek, W. and de Ruyter van Steveninck, R. R. (2000). Adaptive rescaling maximizes information transmission. Neuron 26, 695-702.
10. Carr, C. E. (1993). Processing of temporal information in the brain. Annu. Rev. Neurosci. 16, 223-243.
11. Carr, C. E. and Konishi, M. (1990). A circuit for detection of interaural time differences in the brainstem of the barn owl. J. Neurosci. 10, 3227-3246.
12. Carr, C. E., Rose, G. and Heiligenberg, W. (1986). A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J. Neurosci. 6, 107-119.
13. Cassenaer, S. and Laurent, G. (2007). Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709-713.
14. Christianson, G. B. and Peña, J. L. (2006). Noise reduction of coincidence detector output by the inferior colliculus of the barn owl. J. Neurosci. 26, 5948-5954.
15. Collett, T. S. and Land, M. F. (1985). Visual control of flight behaviour in the hoverfly Syritta pipiens. L. J. Comp. Physiol. 99, 1-66.
16. de Ruyter van Steveninck, R. R. and Laughlin, S. B. (1996). The rate of information transfer at graded-potential synapses. Nature 379, 642-645.
17. de Ruyter van Steveninck, R. R., Lewen, G. D., Strong, S. P., Koberle, R. and Bialek, W. (1997). Reproducibility and variability in neural spike trains. Science 275, 1805-1808.
18. Dhingra, N. K. and Smith, R. G. (2004). Spike generator limits efficiency of information transfer in a retinal ganglion cell. J. Neurosci. 24, 2914-2922.
19. Fairhall, A. L., Lewen, G. D., Bialek, W. and de Ruyter van Steveninck, R. R. (2001). Efficiency and ambiguity in an adaptive neural code. Nature 412, 787-792.
20. Fischer, B. J. and Konishi, M. (2008). Variability reduction in interaural time difference tuning in the barn owl. J. Neurophysiol. 100, 708-715.
21. Griss, C. and Rowell, C. H. F. (1986). Three descending interneurons reporting deviation from course in the locust. I. Anatomy. J. Comp. Physiol. A 158, 765-774.
22. Haag, J. and Borst, A. (1997). Encoding of visual motion information and reliability in spiking and graded potential neurons. J. Neurosci. 17, 4809-4819.
23. Haag, J. and Borst, A. (1998). Active membrane properties and signal encoding in graded potential neurons. J. Neurosci. 18, 7972-7986.
24. Haag, J., Wertz, A. and Borst, A. (2007). Integration of lobula plate output signals by DNOVS1, an identified premotor descending neuron. J. Neurosci. 27, 1992-2000.
25. Hensler, K. (1992). Neuronal co-processing of course deviation and head movements in locusts. I. Descending movement detectors. J. Comp. Physiol. A 171, 257-271.
26. Hensler, K. and Rowell, C. H. F. (1990). Control of optomotor responses by descending deviation detector neurones in intact flying locusts. J. Exp. Biol. 149, 191-205.
27. Judge, S. J. and Rind, F. C. (1997). The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories. J. Exp. Biol. 200, 2209-2216.
28. Juusola, M. and French, A. S. (1997). The efficiency of sensory information coding by mechanoreceptor neurons. Neuron 18, 959-968.
29. Kien, J. (1974). Sensory integration in the locust optomotor system, II. Direction selective neurons in the circumoesophageal connectives and the optic lobe. Vis. Res. 14, 1255-1268.
30. Levi, R. and Camhi, J. M. (2000). Population vector coding by the giant interneurons of the cockroach. J. Neurosci. 20, 3822-3829.
31. Lewen, G. D., Bialek, W. and de Ruyter van Steveninck, R. R. (2001). Neural coding of naturalistic motion stimuli. Network 12, 317-329.
32. Liebenthal, E., Uhlman, O. and Camhi, J. M. (1994). Critical parameters of the spike trains in a cell assembly: coding of turn direction by the giant interneurons of the cockroach. J. Comp. Physiol. A 174, 281-296.
33. Liu, R. C., Tzonev, S., Rebrik, S. and Miller, K. D. (2001). Variability and information in a neural code of the cat lateral geniculate nucleus. J. Neurophysiol. 86, 2789-2806.
34. Mason, A. C., Oshinsky, M. L. and Hoy, R. R. (2001). Hyperacute directional hearing in a microscale auditory system. Nature 410, 686-690.
35. Misizin, A. P. and Josephson, R. K. (1987). Mechanical power output of locust flight muscle. J. Comp. Physiol. A 160, 413-419.
36. Montemurro, M. A., Panzeri, S., Maravall, M., Alenda, A., Bale, M. R., Brambilla, M. and Petersen, R. S. (2007). Role of precise spike timing in coding of dynamic vibrissa stimuli in somatosensory thalamus J. Neurophysiol. 98, 1871-1882.
37. Nemenman, I., Lewen, G. D., Bialek, W. and de Ruyter van Steveninck, R. R. (2008). Neural coding of natural stimuli: information at sub-millisecond resolution. PLoS Comput. Biol. 4, e1000025.
38. Nirenberg, S., Carcieri, S. M., Jacobs, A. L. and Latham, P. E. (2001). Retinal ganglion cells act largely as independent encoders. Nature 411, 698-701.
39. Nolen, T. G. and Hoy, R. R. (1984). Initiation of behaviour by single neurons: the role of behavioural context. Science 226, 992-994.
40. Petersen, R. S., Panzeri, S. and Diamond, M. E. (2001). Population coding of stimulus location in rat somatosensory cortex. Neuron 32, 503-514.
41. Peron, S. and Gabbiani, F. (2009). Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat. Neurosci. 12, 318-326.
42. Pollak, G. D., Marsh, D., Bodenhamer, R. and Souther, A. (1977). Characteristics of phasic-on neurons in the inferior colliculus of unanaesthetised bats with observations relating to mechanisms of echo ranging. J. Neurophysiol. 40, 926-942.
43. Ramirez, J. M. and Pearson, K. G. (1991). Octopaminergic modulation of interneurons in the flight system of the locust. J. Neurophysiol. 166, 1522-1537.
44. Reinagel, P. and Reid, R. C. (2000). Temporal coding of visual information in the thalamus. J. Neurosci. 20, 5392-5400.
45. Rieke, F., Warland, D., de Ruyter van Steveninck, R. R. and Bialek, W. (1997). Spikes: exploring the neural code. Cambridge, MA: MIT Press.
46. Rind, F. C. (1983). A directionally sensitive motion detecting neurone in the brain of a moth. J. Exp. Biol. 102, 253-271.
47. Rind, F. C. (1990). A directionally selective motion-detecting neurone in the brain of the locust: physiological and morphological characterization. J. Exp. Biol. 149, 1-19.
48. Rind, F. C. and Simmons, P. J. (1992). Orthopteran DCMD neuron - a reevaluation of responses to moving-objects. I. Selective responses to approaching objects. J. Neurophysiol. 68, 1654-1666.
49. Rind, F. C., Santer, R. D. and Wright, G. A. (2008). Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust. J. Neurophysiol. 100, 670-680.
50. Rokem, A., Watzl, S., Gollisch, T., Stemmler, M., Herz, A. V. M. and Samengo, I. (2006). Spike-timing precision underlies the coding efficiency of auditory receptor neurons. J. Neurophysiol. 95, 2541-2552.
51. Rose, G. and Heiligenberg, W. (1985). Temporal hyperacuity in the electric sense of fish. Nature 318, 178-180.
52. Rowell, C. H. F. and Pearson, K. G. (1983). Ocellar input to the flight motor system of the locust-structure and function. J. Exp. Biol. 103, 265-288.
53. Rowell, C. H. F. and Reichert, H. (1986). Three descending interneurons reporting deviation from course in the locust. II. Physiology. J. Comp. Physiol. A 158, 775-794.
54. Santer, R. D., Rind, F. C., Stafford, R. and Simmons, P. J. (2006). The role of an identified looming-sensitive neuron in triggering a flying locust's escape. J. Neurophysiol. 95, 3391-3400.
55. Shannon, C. E. and Weaver, W. (1949). The Mathematical Theory of Information. Urbana: University of Illinois Press.
56. Simmons, P. J. (1980). A locust wind and ocellar brain neurone. J. Exp. Biol. 85, 281-294.
57. Simmons, P. J. (1981 ). Synaptic transmission between second- and third-order neurones of a locust ocellus. J. Comp. Physiol. 145, 265-276.
58. Simmons, P. J. (1982). Transmission mediated with and without spikes at connections between large 2nd-order neurons of locust ocelli. J. Comp. Physiol. 147, 401-414.
59. Simmons, P. J. (1986). Interactions made by large 2nd-order neurons of the median ocellus of the locust. J. Comp. Physiol. A 159, 97-105.
60. Simmons, P. J. (1990). The effects of temperature on locust ocellar L-neurons and their interconnections. J. Comp. Physiol. A 166, 575-583.
61. Simmons, P. J. (1993). Adaptation and responses to changes in illumination by 2ndorder and 3rd-order neurons of locust ocelli. J. Comp. Physiol. A 173, 635-648.
62. Simmons, P. J. (1995). The transfer of signals from photoreceptor cells to large 2nd-order neurons in the ocellar visual-system of the locust Locusta migratoria. J. Exp. Biol. 198, 537-549.
63. Simmons, P. J. (2002). Presynaptic depolarization rate controls transmission at an invertebrate synapse. Neuron 35, 749-758.
64. Simmons, P. J. and de Ruyter van Steveninck, R. R. (2005). Reliability of signal transfer at a tonically transmitting, graded potential synapse of the locust ocellar pathway. J. Neurosci. 25, 7529-7537.
65. Strong, S. P., Koberle, R., de Ruyter van Steveninck, R. R. and Bialek, W. (1998). Entropy and information in neural spike trains. Phys. Rev. Lett. 80, 197-200.
66. Taylor, G. K. and Zbikowski, R. (2005). Nonlinear time-periodic models of the longitudinal flight dynamics of desert locusts Schistocerca gregaria. J. R. Soc. Interface 2, 197-221.
67. van Rullen, R., Guyonneau, R. and Thorpe, S. J. (2005). Spike times make sense. Trends Neurosci. 28, 1-4.
68. Vogel, A., Hennig, R. M. and Ronacher, B. (2005). Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J. Neurophysiol. 93, 3548-3559.
69. Warzecha, A. K., Kretzberg, J. and Egelhaaf, M. (1998). Temporal precision of the encoding of motion information by visual interneurons. Curr. Biol. 26, 359-368.
70. Weis-Fogh, T. (1956). Biology and physics of locust flight. II. Flight performance of the desert locust (Schistocerca gregaria). Philos. Trans. R. Soc. B. Biol. Sci. 239, 459-510.
71. Wertz, A., Borst, A. and Haag, J. (2008). Nonlinear integration of binocular optic flow by DNOVS2, a descending neuron of the fly. J. Neurosci. 28, 3131-3140.
72. Wilson, M. (1978a). The functional organisation of locust ocelli. J. Comp. Physiol. 124, 297-316.
73. Wilson, M. (1978c). The origin and properties of discrete hyperpolarising potentials in the second order cells of locust ocellus. J. Comp. Physiol. 128, 347-358.