Receptive field properties and intensity-response functions of polarization-sensitive neurons of the optic tubercle in gregarious and solitarious locusts

Journal of Neurophysiology

Volumn 108, Issue 6, 2012, Pages 1695-1710

  el Jundi, Basil ^a   Homberg, Uwe ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Desert locust; Insect brain; Orientation; Polarization vision; Visual system

Indexed keywords

ANTERIOR OPTIC TUBERCLE; ARTICLE; BRAIN; CELL POLARITY; CONTROLLED STUDY; DIURNAL ANIMAL; INSECT SWARM; LIGHT INTENSITY; LOCUST; MALE; MIGRATION; NERVE CELL; NERVE CELL NETWORK; NOCTURNAL SPECIES; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; SCHISTOCERCA GREGARIA; SIGNAL TRANSDUCTION; VISION;

ANIMALS; BRAIN; EVOKED POTENTIALS, VISUAL; GRASSHOPPERS; LIGHT; NERVE NET; NEURONS; OPTIC LOBE, NONMAMMALIAN; ORIENTATION; PHOTIC STIMULATION; PHOTOPERIOD; VISUAL PERCEPTION;

EID: 84866413846     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01023.2011     Document Type: Article

References (57)

1. Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ. Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323: 627-630, 2009.
2. Baker RR. The Evolutionary Ecology of Animal Migration. London: Hodder and Stoughton, 1978.
3. Batschelet E. Circular Statistics in Biology. New York: Academic, 1981.
4. Chiappe ME, Seelig JD, Reiser MB, Jayaraman V. Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol 20: 1470-1475, 2010.
5. Clements AN, May TE. Studies on locust neuromuscular physiology in relation to glutamic acid. J Exp Biol 60: 673-705, 1974.
6. Collett TS, Collett M. Path integration in insects. Curr Opin Neurobiol 10: 757-762, 2000.
7. Dacke M, Byrne MJ, Scholtz CH, Warrant EJ. Lunar orientation in a beetle. Proc R Soc Lond B 271: 361-365, 2004.
8. Dacke M, Nilsson DE, Scholtz CH, Byrne M, Warrant EJ. Animal behaviour: insect orientation to polarized moonlight. Nature 424: 33, 2003.
9. Dirsh VM. Morphometrical studies on phases of the desert locust (Schistocerca gregaria Forskål). Anti-Locust Bull 16: 1-34, 1953.
10. Eggers A, Gewecke M. The dorsal rim area of the compound eye and polarization vision in the desert locust (Schistocerca gregaria). In: Sensory Systems of Arthropods, edited by Wiese K, Gribakin FG, Popov AV, Renninger G. Basel: Birkhäuser, 1993, p. 101-109.
11. el Jundi B, Homberg U. Evidence for the possible existence of a second polarization-vision pathway in the locust brain. J Insect Physiol 56: 971-979, 2010.
12. el Jundi B, Huetteroth W, Kurylas AE, Schachtner J. Anisometric brain dimorphism revisited: Implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517: 210-225, 2009.
13. el Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U. The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3: 21, 2010.
14. el Jundi B, Pfeiffer K, Homberg U. A distinct layer of the medulla integrates sky compass signals in the locust brain. PLoS One 6: e27855, 2011.
15. Elvegård E, Sjöstedt G. The calculation of illumination from sun and sky. Illum Engin 35: 333-342, 1940.
16. Frost BJ, Mouritsen H. The neural mechanisms of long distance animal navigation. Curr Opin Neurobiol 16: 481-488, 2006.
17. Giurfa M, Capaldi EA. Vectors, routes and maps: new discoveries about navigation in insects. Trends Neurosci 51: 237-242, 1999.
18. Heinze S, Homberg U. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315: 995-997, 2007.
19. Heinze S, Homberg U. Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511: 454-478, 2008.
20. Heinze S, Gotthardt S, Homberg U. Transformation of polarized light information in the central complex of the locust. J Neurosci 29: 11783- 11793, 2009.
21. Homberg U. Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J Comp Physiol A 175: 597-610, 1994.
22. Homberg U. In search of the sky compass in the insect brain. Naturwissenschaften 91: 199-208, 2004.
23. Homberg U, Paech A. Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30: 271-280, 2002.
24. Homberg U, Hofer S, Pfeiffer K, Gebhardt S. Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462: 415-430, 2003.
25. Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B. Central neural coding of sky polarization in insects. Phil Trans R Soc B 366: 680-687, 2011.
26. Johnsen S, Kelber A, Warrant E, Sweeney AM, Widder EA, Lee RL Jr, Hernández-Andrés J. Crepuscular and nocturnal illumination and its effects on color perception by nocturnal hawkmoth Deilephila elpenor. J Exp Biol 209: 789-800, 2006.
27. Kennedy JS. The migration of the desert locust (Schistocerca gregaria Forsk). I. The behaviour of swarms. II. A theory of long-range migrations. Phil Trans R Soc B 235: 163-290, 1951.
28. Kinoshita M, Pfeiffer K, Homberg U. Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210: 1350-1361, 2007.
29. Labhart T, Meyer EP. Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47: 368-379, 1999.
30. Labhart T. Polarization-opponent interneurons in the insect visual system. Nature 331: 435-437, 1988.
31. Labhart T. How polarization-sensitive interneurones of crickets perform at low degrees of polarization. J Exp Biol 199: 1467-1475, 1996.
32. Labhart T, Petzold J. Processing of polarized light information in the visual system of crickets. In: Sensory Systems of Arthropods, edited by Wiese K, Gribakin FG, Popov AV, Renninger G. Basel: Birkhäuser, 1993, p. 158-169.
33. Labhart T, Petzold J, Helbling H. Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J Exp Biol 204: 2423-2430, 2001.
34. Maimon G, Straw AD, Dickinson MH. Active flight increases the gain of visual motion processing in Drosophila. Nat Neurosci 13: 393-399, 2010.
35. Mappes M, Homberg U. Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190: 61-68, 2004.
36. Müller M, Homberg U, Kühn A. Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288: 159-176, 1997.
37. Naka KI, Rushton WAH. S-Potentials from colour units in the retina of fish (Cyprinidae). J Physiol 185: 536-555, 1966.
38. Ott SR, Rogers SM. Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase. Proc R Soc Lond B 277: 3087-3096, 2010.
39. Petzold J. Polarisationsempfindliche Neuronen im Sehsystem der Feldgrille Gryllus campestris: Elektrophysiologie, Anatomie und Modellrechnungen (PhD thesis). Zürich: Univ. of Zurich, 2001.
40. Pfeiffer K, Homberg U. Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17: 960-965, 2007.
41. Pfeiffer K, Kinoshita M, Homberg U. Polarization-sensitive and lightsensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94: 3903-3915, 2005.
42. Pfeiffer K, Negrello M, Homberg U. Conditional perception under stimulus ambiguity: polarization- and azimuth-sensitive neurons in the locust brain are inhibited by low degrees of polarization. J Neurophysiol 105: 28-35, 2011.
43. Roessingh P, Simpson SJ, James S. Analysis of phase-related changes in behaviour of desert locust nymphs. Proc R Soc Lond B 252: 43-49, 1993.
44. Roffey J. Observations on night flight in the desert locust (Schistocerca gregaria Forskål). Anti-Locust Bull 39: 1-32, 1963.
45. Rogers SM, Harston GWJ, Kilburn-Toppin F, Matheson T, Burrows M, Gabbiani F, Krapp HG. Spatiotemporal receptive field properties of a looming-sensitive neuron in solitarious and gregarious phases of the desert locust. J Neurophysiol 103: 779-792, 2010.
46. Rosner R, Egelhaaf M, Warzecha AK. Behavioural state affects motionsensitive neurones in the fly visual system. J Exp Biol 213: 331-338, 2010.
47. Schmitt S, Evers JF, Duch C, Scholz M, Obermayer K. New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks. Neuroimage 23:1283-1298, 2004.
48. Simpson S, McCaffery A, Hägele BF. A behavioural analysis of phase change in the desert locust. Biol Rev 74: 461-480, 1999.
49. Stower WJ, Davies DE, Jones IB. Morphometric studies of the desert locust Schistocerca gregaria (Forsk.). J Anim Ecol 29: 309-339, 1960.
50. Träger U, Wagner R, Bausenwein B, Homberg U. A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506: 288-300, 2008.
51. Uvarov B. Grasshoppers and Locusts. A Handbook of General Acridology. Cambridge: Cambridge Univ. Press, 1966.
52. Vitzthum H, Müller M, Homberg U. Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22: 1114-1125, 2002.
53. Waloff Z. Field studies on solitary and transiens desert locusts in the Red Sea area. Anti-Locust Bull 40: 1-91, 1963.
54. Warrant EJ. Vision in the dimmest habitats on Earth. J Comp Physiol A 190: 765-789, 2004.
55. Warrant EJ, Dacke M. Vision and visual navigation in nocturnal insects. Annu Rev Entomol 56: 239-254, 2011.
56. Wehner R. Astronavigation in insects. Annu Rev Entomol 29: 277-298, 1984.
57. Wehner R, Labhart T. Polarization vision. In: Invertebrate Vision, edited by Warrant E, Nilsson DE. Cambridge: Cambridge Univ. Press, 2006, p. 291-348.