Multiplexing of Motor Information in the Discharge of a Collision Detecting Neuron during Escape Behaviors

Neuron

Volumn 69, Issue 1, 2011, Pages 147-158

  Fotowat, Haleh ^a,e   Harrison, Reid R ^b,c,f   Gabbiani, Fabrizio ^a,d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Department of Electrical and Computer Engineering   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d Rice University   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f Intan Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; DESCENDING CONTRALATERAL MOVEMENT DETECTOR; ESCAPE BEHAVIOR; FEMALE; JUMPING; LEG MUSCLE; LOCUST; MOTONEURON; MUSCLE CONTRACTION; NERVE CELL; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; TELEMETRY;

ANIMALS; ELECTROPHYSIOLOGY; ESCAPE REACTION; FEMALE; GRASSHOPPERS; LASER THERAPY; MOTION PERCEPTION; MOTOR ACTIVITY; MOTOR NEURONS; MOVEMENT; PHOTIC STIMULATION; REACTION TIME; TELEMETRY;

EID: 78649318893     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.12.007     Document Type: Article

References (65)

1. Burrows M. The Neurobiology of an insect brain 1996, Oxford University Press, Oxford.
2. Burrows M., Pflüger H. Positive feedback loops from proprioceptors involved in leg movements of the locust. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1988, 163:425-440.
3. Burrows M., Rowell C.F. Connections between descending visual interneurons and metathoracic motoneurons in the locust. J. Comp. Physiol. 1973, 85:221-234.
4. Camhi J.M., Levy A. The code for stimulus direction in a cell assembly in the cockroach. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1989, 165:83-97.
5. Cohen M.R., Newsome W.T. Estimates of the contribution of single neurons to perception depend on timescale and noise correlation. J. Neurosci. 2009, 29:6635-6648.
6. Cook E.P., Maunsell J.H.R. Dynamics of neuronal responses in macaque mt and vip during motion detection. Nat. Neurosci. 2002, 5:985-994.
7. De Lafuente V., Romo R. Neuronal correlates of subjective sensory experience. Nat. Neurosci. 2005, 8:1698-1703.
8. Edwards D.H., Heitler W.J., Krasne F.B. Fifty years of a command neuron: The neurobiology of escape behavior in the crayfish. Trends Neurosci. 1999, 22:153-161.
9. Farrow K., Haag J., Borst A. Input organization of multifunctional motion-sensitive neurons in the blowfly. J. Neurosci. 2003, 23:9805-9811.
10. Fotowat H., Gabbiani F. Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior. J. Neurosci. 2007, 27:10047-10059.
11. Fotowat H., Fayyazuddin A., Bellen H.J., Gabbiani F. A novel neuronal pathway for visually guided escape in drosophila melanogaster. J. Neurophysiol. 2009, 102:875-885.
12. Friedrich R.W., Habermann C.J., Laurent G. Multiplexing using synchrony in the zebrafish olfactory bulb. Nat. Neurosci. 2004, 7:862-871.
13. Gabbiani F., Krapp H.G., Laurent G. Computation of object approach by a wide-field, motion-sensitive neuron. J. Neurosci. 1999, 19:1122-1141.
14. Gabbiani F., Mo C., Laurent G. Invariance of angular threshold computation in a wide-field looming-sensitive neuron. J. Neurosci. 2001, 21:314-329.
15. Gabbiani F., Krapp H.G., Koch C., Laurent G. Multiplicative computation in a visual neuron sensitive to looming. Nature 2002, 420:320-324.
16. Gabbiani F., Cohen I., Laurent G. Time-dependent activation of feed-forward inhibition in a looming-sensitive neuron. J. Neurophysiol. 2005, 94:2150-2161.
17. Gray J.R., Blincow E., Robertson R.M. A pair of motion-sensitive neurons in the locust encode approaches of a looming object. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2010, 10.1007/s00359-010-0576-7.
18. Graziano M.S., Andersen R., Snowden R. Tuning of mst neurons to spiral motions. J. Neurosci. 1994, 14:54-67.
19. Gu Y., Angelaki D.E., Deangelis G.C. Neural correlates of multisensory cue integration in macaque MSTd. Nat. Neurosci. 2008, 11:1201-1210.
20. Gynther I.C., Pearson K.G. An evaluation of the role of identified interneurons in triggering kicks and jumps in the locust. J. Neurophysiol. 1989, 61:45-57.
21. Hatsopoulos N., Gabbiani F., Laurent G. Elementary computation of object approach by wide-field visual neuron. Science 1995, 270:1000-1003.
22. Heitler W.J. Quasi-reversible photo-axotomy used to investigate the role of extensor muscle tension in controlling the kick motor programme of grasshoppers. Eur. J. Neurosci. 1995, 7:981-992.
23. Hoyle G. Distributions of nerve and muscle fibre types in locust jumping muscle. J. Exp. Biol. 1978, 73:205-233.
24. Ishikane H., Gangi M., Honda S., Tachibana M. Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nat. Neurosci. 2005, 8:1087-1095.
25. Jacobs G.A., Miller J.P. Functional properties of individual neuronal branches isolated in situ by laser photoinactivation. Science 1985, 228:344-346.
26. Jellema T., Heitler W.J. Central and peripheral control of the trigger mechanism for kicking and jumping in the locust. J. Comp. Neurol. 1999, 404:212-220.
27. Judge S., Rind F.C. The locust dcmd, a movement-detecting neurone tightly tuned to collision trajectories. J. Exp. Biol. 1997, 200:2209-2216.
28. Killmann F., Schurmann F. Both electrical and chemical transmission between the 'lobula giant movement detector' and the 'descending contralateral movement detector' neurons of locusts are supported by electron microscopy. J. Neurocytol. 1985, 14:637-652.
29. Korn H., Faber D.S. The mauthner cell half a century later: A neurobiological model for decision-making? Neuron 2005, 47:13-28.
30. Kristan W.B., Shaw B.K. Population coding and behavioral choice. Curr. Opin. Neurobiol. 1997, 7:826-831.
31. Lewis J.E., Kristan W.B. A neuronal network for computing population vectors in the leech. Nature 1998, 391:76-79.
32. Lima S.Q., Miesenböck G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 2005, 121:141-152.
33. Liu K.S., Fetcho J.R. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 1999, 23:325-335.
34. Marsat G., Pollack G.S. A behavioral role for feature detection by sensory bursts. J. Neurosci. 2006, 26:10542-10547.
35. Meister M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 1996, 93:609-614.
36. Miller J.P., Selverston A. Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 1979, 206:702-704.
37. Mountcastle V.B., Lynch J.C., Georgopoulos A., Sakata H., Acuna C. Posterior parietal association cortex of the monkey: Command functions for operations within extrapersonal space. J. Neurophysiol. 1975, 38:871-908.
38. Nakagawa H., Hongjian K. Collision-sensitive neurons in the optic tectum of the bullfrog, Rana catesbeiana. J. Neurophysiol. 2010, 104:2487-2499.
39. Newsome W.T., Wurtz R.H., Komatsu H. Relation of cortical areas MT and MST to pursuit eye movements. ii. differentiation of retinal from extraretinal inputs. J. Neurophysiol. 1988, 60:604-620.
40. Nienborg H., Cumming B.G. Decision-related activity in sensory neurons reflects more than a neuron's causal effect. Nature 2009, 459:89-92.
41. O'Shea M., Rowell C., Williams J. The anatomy of a locust visual interneurone; the descending contralateral movement detector. J. Exp. Biol. 1974, 60:1-12.
42. Oliva D., Medan V., Tomsic D. Escape behavior and neuronal responses to looming stimuli in the crab chasmagnathus granulatus (decapoda: Grapsidae). J. Exp. Biol. 2007, 210:865-880.
43. Panzeri S., Brunel N., Logothetis N.K., Kayser C. Sensory neural codes using multiplexed temporal scales. Trends Neurosci. 2010, 33:111-120.
44. Pearson K., Robertson R. Interneurons coactivating hindleg flexor and extensor motoneurons in the locust. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1981, 144:391-410.
45. Pearson K.G., Heitler W.J., Steeves J.D. Triggering of locust jump by multimodal inhibitory interneurons. J. Neurophysiol. 1980, 43:257-278.
46. Peron S., Gabbiani F. Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat. Neurosci. 2009, 12:318-326.
47. Preuss T., Osei-Bonsu P.E., Weiss S.A., Wang C., Faber D.S. Neural representation of object approach in a decision-making motor circuit. J. Neurosci. 2006, 26:3454-3464.
48. Rind F.C. A chemical synapse between two motion detecting neurones in the locust brain. J. Exp. Biol. 1984, 110:143-167.
49. Rind F.C., Simmons P. Orthopteran dcmd neuron: A reevaluation of responses to moving objects. I. selective responses to approaching objects. J. Neurophysiol. 1992, 68:1654-1666.
50. Rogers S.M., Krapp H.G., Burrows M., Matheson T. Compensatory plasticity at an identified synapse tunes a visuomotor pathway. J. Neurosci. 2007, 27:4621-4633.
51. Roitman J.D., Shadlen M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 2002, 22:9475-9489.
52. Rowell C. The orthopteran descending movement detector (dmd) neurones: A characterisation and review. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1971, 73:167-194.
53. Rowell C. Variable responsiveness of a visual interneurone in the free-moving locust, and its relation to behaviour and arousal. J. Exp. Biol. 1971, 55:727-747.
54. Santer R.D., Yamawaki Y., Rind F.C., Simmons P.J. Motor activity and trajectory control during escape jumping in the locust Locusta migratoria. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2005, 191:965-975.
55. Santer R.D., Rind F.C., Stafford R., Simmons P. Role of an identified looming-sensitive neuron in triggering a flying locust's escape. J. Neurophysiol. 2006, 95:3391-3400.
56. Santer R.D., Yamawaki Y., Rind F.C., Simmons P.J. Preparing for escape: An examination of the role of the dcmd neuron in locust escape jumps. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2008, 194:69-77.
57. Schlotterer G.R. Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli. Can. J. Zool. 1977, 55:1372-1376.
58. Simmons P. Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust. J. Exp. Biol. 1980, 86:87-97.
59. Sun H., Frost B. Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat. Neurosci. 1998, 1:296-303.
60. Trimarchi J.R., Schneiderman A.M. Giant fiber activation of an intrinsic muscle in the mesothoracic leg of drosophila melanogaster. J. Exp. Biol. 1993, 177:149-167.
61. van Hateren J.H., Kern R., Schwerdtfeger G., Egelhaaf M. Function and coding in the blowfly H1 neuron during naturalistic optic flow. J. Neurosci. 2005, 25:4343-4352.
62. Wang Y., Frost B.J. Time to collision is signaled by neurons in the nucleus rotundus of pigeons. Nature 1992, 356:236-238.
63. Warzecha A.K., Egelhaaf M., 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. 1993, 69:329-339.
64. Wicklein M., Strausfeld N.J. Organization and significance of neurons that detect change of visual depth in the hawk moth manduca sexta. J. Comp. Neurol. 2000, 424:356-376.
65. Yamamoto K., Nakata M., Nakagawa H. Input and output characteristics of collision avoidance behavior in the frog rana catesbeiana. Brain Behav. Evol. 2003, 62:201-211.