Predator versus Prey: Locust Looming-Detector Neuron and Behavioural Responses to Stimuli Representing Attacking Bird Predators

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Santer, Roger D ^a,b   Rind, F Claire ^c   Simmons, Peter J ^c  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIMERICK   (Ireland)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACRIDIDAE; ANIMAL BEHAVIOR; ANIMAL CELL; ARTHROPOD; ARTICLE; BIRD; BLACK KITE; CONTROLLED STUDY; DESCENDING CONTRALATERAL MOVEMENT DETECTOR NEURON; ESCAPE BEHAVIOR; NERVE CELL; NONHUMAN; PREDATOR; PREY; STARTLE REFLEX; STIMULUS RESPONSE;

ANIMALS; ARTHROPODS; AUSTRALIA; BEHAVIOR, ANIMAL; BIRDS; ESCAPE REACTION; FLIGHT, ANIMAL; GRASSHOPPERS; MOTION; MOTION PERCEPTION; NEURONS; PREDATORY BEHAVIOR; PROBABILITY; SOCIAL BEHAVIOR; THORAX; VIDEO RECORDING; VISION, OCULAR; WING;

ARTHROPODA; AVES; MILVUS; ORTHOPTERA;

EID: 84870266572     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050146     Document Type: Article

References (77)

1. Card GM, (2012) Escape behaviors in insects. Curr Opin Neurobiol 22: 180-186.
2. Dangles O, Ory N, Steinmann T, Christides J-P, Casas J, (2006) Spider's attack versus cricket's escape: velocity modes determine success. Anim Behav 72: 603-610.
3. Casas J, Steinmann T, Dangles O, (2008) The aerodynamic signature of running spiders. PLoS One 3: e2116.
4. Dangles O, Casas J, Coolen I, (2006) Textbook cricket goes to the field: the ecological scene of the neuroethological play. J Exp Biol 209: 393-398.
5. Triblehorn JD, Yager DD, (2006) Wind generated by an attacking bat: anemometric measurements and detection by the praying mantis cercal system. J Exp Biol 209: 1430-1440.
6. Dupuy F, Casas J, Mody M, Lazzari C, (2011) Danger detection and escape behaviour in wood crickets. J Insect Physiol 57: 865-871.
7. Herberholz J, Sen MM, Edwards DH, (2004) Escape behaviour and escape circuit activation in juvenile crayfish during predator-prey interactions. J Exp Biol 207: 1855-1863.
8. Camhi JM, Tom W, Volman S, (1978) The escape behaviour of the cockroach Periplaneta americana II. detection of natural predators by air displacement. J Comp Physiol A 128: 203-212.
9. de Vries SEJ, Clandinin TR, (2012) Loom-sensitive neurons link computation to action in the Drosophila visual system. Curr Biol 22: 353-362.
10. Nakagawa H, Hongjian K, (2010) Collision-sensitive neurons in the optic tectum of the bullfrog, Rana catesbiana. J Neurophysiol 104: 2487-2499.
11. Oliva D, Medan V, Tomsic D, (2007) Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae). J Exp Biol 210: 865-880.
12. Sun H, Frost BJ, (1998) Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat Neurosci 1: 296-303.
13. Yamawaki Y, Toh Y, (2009) Responses of descending neurons to looming stimuli in the preaying mantis Tenodera aridifolia. J Comp Physiol A 195: 253-264.
14. Münch TA, da Silveira RA, Siegert S, Viney TJ, Awatramani GB, et al. (2009) Approach sensitivity in the retina processed by a multifunctional neural circuit. Nat Neurosci 12: 1308-1316.
15. Preuss T, Osei-Bonsu PE, Weiss SA, Wang C, Faber DS, (2006) Neural representation of object approach in a decision-making motor circuit. J Neurosci 26: 3454-3464.
16. Liu Y-J, Wang Q, Li B, (2011) Neuronal responses to looming objects in the superior colliculus of the cat. Brain Behav Evol 77: 193-205.
17. Rind FC, Simmons PJ, (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. selective responses to approaching objects. J Neurophysiol 68: 1654-1666.
18. Schlotterer GR, (1977) Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli. Can J Zool 55: 1372-1376.
19. O'Shea M, Rowell CHF, Williams JLD, (1974) The anatomy of a locust visual interneurone: the descending contralateral movement detector. J Exp Biol 60: 1-12.
20. Burrows M, Rowell CHF, (1973) Connections between descending visual interneurons and metathoracic motoneurons in the locust. J Comp Physiol A 85: 221-234.
21. Simmons PJ, (1980) Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust. J Exp Biol 86: 87-97.
22. O'Shea M, Williams JLD, (1974) The anatomy and output connections of a locust visual interneurone: the lobula giant movement detector (LGMD) neurone. J Comp Physiol A 91: 257-266.
23. Krapp HG, Gabbiani F, (2005) Spatial distribution of inputs and local receptive field properties of a wide-field looming sensitive neuron. J Neurophysiol 93: 2240-2253.
24. Gabbiani F, Krapp HG, Koch C, Laurent G, (2002) Multiplicative computation in a visual neuron sensitive to looming. Nature 420: 320-324.
25. Rind FC, Bramwell DI, (1996) Neural network based on the input organisation of an identified neuron signaling impending collision. J Neurophysiol 75: 967-984.
26. Rind FC, (1984) A chemical synapse between two motion detecting neurons in the locust brain. J Exp Biol 110: 143-167.
27. Judge SJ, Rind FC, (1997) The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories. J Exp Biol 200: 2209-2216.
28. Simmons PJ, Rind FC, (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. critical cues for detecting approaching objects. J Neurophysiol 68: 1667-1682.
29. Gabbiani F, Krapp HG, Hatsopoulos N, Mo CH, Koch C, et al. (2004) Multiplication and stimulus invariance in a looming-sensitive neuron. J Physiol Paris 98: 19-34.
30. Matheson T, Rogers SM, Krapp HG, (2004) Plasticity in the visual system is correlated with a change in lifestyle of solitarious and gregarious locusts. J Neurophysiol 91: 1-12.
31. Rind FC, Santer RD, Wright GA, (2008) Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust. J Neurophysiol 100: 670-680.
32. Simmons PJ, Rind FC, Santer RD, (2010) Escapes with and without preparation: the neuroethology of visual startle in locusts. J Insect Physiol 56: 876-883.
33. Fotowat H, Gabbiani F, (2011) Collision detection as a model for sensory-motor integration. Ann Rev Neurosci 34: 1-19.
34. Santer RD, Yamawaki Y, Rind FC, Simmons PJ, (2008) Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps. J Comp Physiol A 194: 69-77.
35. Fotowat H, Harrison RR, Gabbiani F, (2011) Multiplexing of motor information in the discharge of a collision detecting neuron during escape behaviors. Neuron 69: 147-158.
36. Fotowat H, Gabbiani F, (2007) Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior. J Neurosci 27: 10047-10059.
37. Santer RD, Simmons PJ, Rind FC, (2005) Gliding behaviour elicited by lateral looming stimuli in flying locusts. J Comp Physiol A 191: 61-73.
38. Santer RD, Rind FC, Stafford R, Simmons PJ, (2006) Role of an identified looming-sensitive neuron in triggering a flying locust's escape. J Neurophysiol 95: 3391-3400.
39. Robertson RM, Reye DN, (1992) Wing movements associated with collision-avoidance manoeuvres during flight in the locust Locusta migratoria. J Exp Biol 163: 231-258.
40. Robertson RM, Johnson AG, (1993) Collision avoidance of flying locusts: steering torques and behaviour. J Exp Biol 183: 35-60.
41. Ribak G, Rand D, Weihs D, Ayali A, (2012) Role of wing pronation in evasive steering of locusts. J Comp Physiol A 198: 541-555.
42. Rind FC, Santer RD, (2004) Collision avoidance and a looming sensitive neuron: size matters but biggest is not necessarily best. Proc R Soc B 271: S27-S29.
43. Stafford R, Santer RD, Rind FC, (2007) The role of behavioural ecology in the design of bio-inspired technology. Anim Behav 74: 1813-1819.
44. Greathead DJ, (1966) A brief survey of the effects of biotic factors on populations of the desert locust. J Appl Ecol 3: 239-250.
45. Nickerson B, (1958) Some observations of the carmine bee-eater Merops nubicus Gmelin in the French Sudan. Ibis 100: 454-457.
46. Smith KD, Popov GB, (1953) On birds attacking desert locust swarms in Eritrea. Entomologist 86: 3-7.
47. Sánchez-Zapata JA, Donázar JA, Delgado A, Forero MG, Ceballos O, et al. (2007) Desert locust outbreaks in the Sahel: resource competition, predation and ecological effects of pest control. J Appl Ecol 44: 323-329.
48. Joern A, (1992) Variable impact of avian predation on grasshopper assemblies in sandhills grassland. Oikos 64: 458-463.
49. Joern A, (1986) Experimental study of avian predation on coexisting grasshopper populations (Orthoptera: Acrididae) in sandhills grassland. Oikos 46: 243-249.
50. Curtis LK, Rowland P, (2008) Australian kites. Wildlife Australia Magazine Winter 2008: 41.
51. Ferguson-Lees J, Christie DA (2001) Raptors of the world. New York: Houghton Mifflin.
52. Gray JR, (2005) Habituated visual neurons in locusts remain sensitive to novel looming objects. J Exp Biol 208: 2515-2532.
53. Baker PS, Gewecke M, Cooter RJ, (1981) The natural flight of the migratory locust, Locusta migratoria L. III. wing-beat frequency, flight speed and attitude. J Comp Physiol A 141: 233-237.
54. Irschick DJ, (2003) Measuring performance in nature: Implications for studies of fitness within populations. Integr Comp Biol 43: 396-407.
55. Bruderer B, Boldt A, (2001) Flight characteristics of birds: I. Radar measurements of speeds. Ibis 143: 178-204.
56. Spaar R, (1997) Flight strategies of migrating raptors; a comparative study of interspecific variation in flight characteristics. Ibis 139: 523-535.
57. Chatterjee S, Templin RJ, Campbell KE Jr, (2007) The aerodynamics of Argentavis, the world's largest flying bird from the Miocene of Argentina. Proc Natl Acad Sci USA 104: 12398-12403.
58. Blake RW, Kolotylo R, de la Cueva H, (1990) Flight speeds of the barn swallow, Hirundo rustica. Can J Zool 68: 1-5.
59. Brigham RM, Fenton MB, Aldridge HDJN, (1998) Flight speeds of foraging common nighthawks (Chordeiles minor): Does the measurement technique matter? Am Midl Nat 139: 325-330.
60. Cramp S (1985) Handbook of the birds of Europe, the middle east, and north Africa. The birds of the western palearctic, vol. IV. terns to woodpeckers. Oxford: Oxford University Press.
61. Cramp S (1988) Handbook of the birds of Europe, the middle east and north Africa. The birds of the western palearctic, vol. V. tyrant flycatchers to thrushes. Oxford: Oxford University Press.
62. Gabbiani F, Mo C, Laurent G, (2001) Invariance of angular threshold computation in a wide-field looming-sensitive neuron. J Neurosci 21: 314-329.
63. McMillan GA, Gray JR, (2012) A looming-sensitive pathway responds to changes in the trajectory of object motion. J Neurophysiol 108: 1052-1068.
64. Rogers SM, Harston GWJ, Kilburn-Toppin F, Matheson T, Burrows M, et al. (2010) Spatiotemporal receptive field properties of a looming-sensitive neuron in solitarious and gregarious phases of the desert locust. J Neurophysiol 103: 779-792.
65. Sword GA, Lorch PD, Gwynne DT, (2005) Migratory bands give crickets protection. Nature 433: 703.
66. Yamamoto K, Nakata M, Nakagawa H, (2003) Input and output characteristics of collision avoidance behavior in the frog Rana catesbeiana. Brain Behav Evol 62: 201-211.
67. Yamawaki Y, (2011) Defence behaviours of the praying mantis Tenodera aridifolia in response to looming objects. J Insect Physiol 57: 1510-1517.
68. Gray JR, Lee JK, Robertson RM, (2001) Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts. J Comp Physiol A 187: 115-129.
69. Triblehorn JD, Ghose K, Bohn K, Moss CF, Yager DD, (2008) Free-flight encounters between praying mantids (Parasphendale agrionina) and bats (Eptesicus fuscus). J Exp Biol 211: 555-562.
70. Cooper WE, (2006) Risk factors and escape strategy in the grasshopper Dissosteira carolina. Behaviour 143: 1201-1218.
71. Kayser C, Körding KP, König P, (2004) Processing of complex stimuli and natural scenes in the visual cortex. Curr Opin Neurobiol 14: 1-6.
72. Reinagel P, (2001) How do visual neurons respond in the real world? Curr Opin Neurobiol 11: 437-442.
73. Rind FC, Simmons PJ, (1998) Local circuit for the computation of object approach by an identified visual neuron in the locust. J Comp Neurol 395: 405-415.
74. Straw AD, (2008) Vision egg: an open-source library for realtime stimulus generation. Front Neuroinform 2: 4.
75. Unwin DM (1980) Microclimate measurement for ecologists. London: Academic Press.
76. Middleton WEK (1952) Vision through the atmosphere. Toronto: University of Toronto Press.
77. Gabbiani F, Krapp HG, Laurent G, (1999) Computation of object approach by a wide-field motion-sensitive neuron. J Neurosci 19: 1122-1141.