Evidence for instantaneous e-vector detection in the honeybee using an associative learning paradigm

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1728, 2012, Pages 535-542

  Sakura, Midori ^a   Okada, Ryuichi ^b   Aonuma, Hitoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b TOKUSHIMA BUNRI UNIVERSITY   (Japan)

Author keywords

Dorsal rim area; Insect; Navigation; Polarization vision; Proboscis extension reflex

Indexed keywords

ALGORITHM; DETECTION METHOD; FLIGHT; FORAGING BEHAVIOR; HONEYBEE; HYPOTHESIS TESTING; LEARNING; ORIENTATION BEHAVIOR; POLARIZATION; ULTRAVIOLET RADIATION;

EID: 84055212389     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0929     Document Type: Article

References (55)

1. Lohmann, K. J. & Lohmann, C. M. F. 1996 Orientation and open-sea navigation in sea turtles. J. Exp. Biol. 199,73-81.
2. Walcott, C. 1996 Pigeon homing: observations, experiments and confusions. J. Exp. Biol. 199, 21-27.
3. Reppert, S. M., Gegear, R. J. & Merlin, C. 2010 Navigational mechanism of migrating monarch butterflies. Trends Neurosci. 33, 399-406.(doi:10.1016/j.tins.2010.04.004)
4. Menzel, R., De Marco, R. & Gregger, U. 2006 Spatial memory, navigation and dance behaviour in Apis mellifera. J. Comp. Physiol. A 192, 889-903.(doi:10.1007/s00359-006-0136-3)
5. Wehner, R. & Wehner, S. 1990 Insect navigation: use of maps or Ariadne's thread? Ethol. Ecol. Evol. 2, 27-48.(doi:10.1080/08927014.1990.9525492)
6. Frost, B. J. & Mouritsen, H. 2006 The neural mechanisms of long distance animal navigation. Curr. Opin. Neurobiol. 16, 481-488.(doi:10.1016/j.conb.2006.06.005)
7. Taube, J. S. 1998 Head direction cells and the neurophysiological basis for a sense of direction. Prog. Neurobiol. 55, 225-256.(doi:10.1016/S0301-0082(98)00004-5)
8. Sharp, P. E., Blair, H. T. & Cho, J. 2001 The anatomical and computational basis of the rat head direction cell signal. Trends Neurosci. 24, 289-294.(doi:10.1016/S0166-2236(00)01797-5)
9. Harvey, C. D., Collman, F., Dombeck, K. & Tank, D. W. 2009 Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-949.(doi:10.1038/nature08499)
10. Chittka, L. & Niven, J. 2009 Are bigger brains better? Curr. Biol. 19, R995-R1008.(doi:10.1016/j.cub.2009.08.023)
11. Rossel, S. & Wehner, R. 1987 The bee's e-vector compass. In Neurobiology and behavior of honeybees (eds R. Menzel & A. Mercer), pp. 76-93. Berlin, Germany: Springer.
12. Wehner, R. 1994 The polarization-vision project: championing organismic biology. In Neural basis of behavioural adaptation (eds K. Schildberger & N. Elsner), pp. 103-143. Stuttgart, Germany: Fischer-Verlag.
13. Wehner, R. & Labhart, T. 2006 Polarisation vision. In Invertebrate vision (eds E. Warrant & D. E. Nilsson), pp. 291-348. Cambridge, UK: Cambridge University Press.
14. Collett, T. S. & Collett, M. 2000 Path integration in insects. Curr. Opin. Neurobiol. 10, 757-762.(doi:10. 1016/S0959-4388(00)00150-1)
15. Wehner, R. 2003 Desert ant navigation: how miniature brains solve complex tasks. J. Comp. Physiol. A 189, 579-588.(doi:10.1007/s00359-003-0431-1)
16. Strutt, J. 1871 On the light from the sky, its polarization and colour. Phil. Mag. 41, 107-120.
17. Sherman, G. & Visscher, P. K. 2002 Honeybee colonies achieve fitness through dancing. Nature 419, 920-922.(doi:10.1038/nature01127)
18. Labhart, T. & Meyer, E. P. 1999 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.(doi:10.1002/(SICI)1097-0029(1999 1215)47:6,368::AID-JEMT2.3.0.CO;2-Q)
19. Meyer, E. P. & Labhart, T. 1981 Pore canals in the cornea of a functionally specialized area of the honey bee's compound eye. Cell Tissue Res. 216, 491-501.(doi:10.1007/BF00238646)
20. Schinz, R. 1975 Structure specialization in the dorsal retina of the bee, Apis mellifera. Cell Tissue Res. 162, 23-34.(doi:10.1007/BF00223259)
21. Wehner, R., Bernard, G. D. & Geiger, E. 1975 Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J. Comp. Physiol. 104, 225-245.(doi:10.1007/BF01379050)
22. Rossel, S. & Wehner, R. 1986 Polarization vision in bees. Nature 323, 128-131.(doi:10.1038/323128a0)
23. Labhart, T. 1980 Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: polarizational and angular sensitivity. J. Comp. Physiol. A 141, 19-30.(doi:10.1007/BF00611874)
24. Wehner, R. & Strasser, S. 1985 The POL area of the honey bee's eye: behavioural evidence. Physiol. Entomol. 10, 337-349.(doi:10.1111/j.1365-3032.1985.tb00055.x)
25. von Helversen, O. & Edrich, W. 1974 Der polarisationsempfänger im Bienenauge: ein Ultraviolettrezeptor. J. Comp. Physiol. 94, 33-47.(doi:10.1007/BF00610156)
26. Labhart, T. 1988 Polarization-opponent interneurons in the insect visual system. Nature 331, 435-437.(doi:10.1038/331435a0)
27. Labhart, T., Petzold, J. & Helbling, H. 2001 Spatial integration in polarization-sensitive interneurons of crickets: a survey of evidence, mechanisms and benefits. J. Exp. Biol. 204, 2423-2430.
28. Petzold, J. 2001 Polarisationsempfindliche Neuronen im Sehsystem der Feldgrill, Gryllus campestris: Elektrophysiologie, Anatomie und Modellrechnungen. PhD thesis, University of Zurich, Zurich, Germany.
29. Heinze, S. & Homberg, U. 2007 Maplike representation of celestial e-vector orientations in the brain of an insect. Science 315, 995-997.(doi:10.1126/science.1135531)
30. Heinze, S., Gotthardt, S. & Homberg, U. 2009 Transformation of polarized light information in the central complex of the locust. J. Neurosci. 29, 11 783-11 793.(doi:10.1523/JNEUROSCI.1870-09.2009)
31. Vitzthum, H., Müller, M. & Homberg, U. 2002 Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J. Neurosci. 22, 1114-1125.
32. Sakura, M., Lambrinos, D. & Labhart, T. 2008 Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J. Neurophysiol. 99, 667-682.(doi:10.1152/jn.00784.2007)
33. Labhart, T. & Meyer, E. P. 2002 Neural mechanisms in insect navigation: polarization compass and odometer. Curr. Opin. Neurobiol. 12, 707-714.(doi:10.1016/S0959-4388(02)00384-7)
34. Rossel, S. 1993 Navigation by bees using polarized skylight. Comp. Biochem. Physiol. 104A, 695-708.(doi:10.1016/0300-9629(93)90146-U)
35. Edrich, W. & von Helversen, O. 1987 Polarized light orientation in honey bees: is time a component in sampling? Biol. Cybern. 56, 89-96.(doi:10.1007/BF00317983)
36. Bitterman, M. E., Menzel, R., Fietz, A. & Schäfer, S. 1983 Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97, 107-119.(doi:10.1037/0735-7036.97.2.107)
37. Hori, S., Takeuchi, H., Arikawa, K., Kinoshita, M., Ichikawa, N., Sasaki, M. & Kubo, T. 2006 Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J. Comp. Physiol. A 192, 691-700.(doi:10.1007/s00359-005-0091-4)
38. Hori, S., Takeuchi, H. & Kubo, T. 2007 Associative learning and discrimination of motion cues in the harnessed honeybee Apis mellifera L. J. Comp. Physiol. A 193, 825-833.(doi:10.1007/s00359-007-0234-x)
39. Menzel, R. 2001 Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53-62.(doi:10.1101/lm.38801)
40. Okada, R., Rybak, J., Manz, G. & Menzel, R. 2007 Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J. Neurosci. 27, 11 736-11 747.(doi:10.1523/JNEUR OSCI.2216-07.2007)
41. Rossel, S. & Wehner, R. 1984 Celestial orientation in bees: the use of spectral cues. J. Comp. Physiol. A 155, 605-613.(doi:10.1007/BF00610846)
42. Menzel, R. & Blakers, M. 1976 Colour receptors in the bee eye: morphology and spectral sensitivity. J. Comp. Physiol. 108, 11-33.(doi:10.1007/BF00625437)
43. Menzel, R. & Giurfa, M. 2001 Cognitive architecture of a mini-brain: the honeybee. Trends Cogn. Sci. 5, 62-71.(doi:10.1016/S1364-6613(00)01601-6)
44. Esch, H. E., Shang, S., Srinivasan, M. V. & Tautz, J. 2001 Honeybee dances communicate distances measured by optic flow. Nature 411, 581-583.(doi:10.1038/35079072)
45. Menzel, R., Manz, G., Menxel, R. & Greggers, U. 2001 Massed and spaced learning in honeybees: the role of CS, US, the intertribal interval, and the test interval. Learn. Mem. 8, 198-208.(doi:10.1101/lm.40001)
46. Sandoz, J. C. & Pham-Delegue, M. H. 2004 Spontaneous recovery after extinction of the conditioned proboscis extension response in the honeybee. Learn. Mem. 11, 586-597.(doi:10.1101/lm.81504)
47. Menzel, R. et al. 2005 Honey bees navigate according to a map-like spatial memory. Proc. Natl Acad. Sci. USA 102, 3040-3045.(doi:10.1073/pnas.0408550102)
48. Menzel, R. 1999 Memory dynamics in the honeybee. J. Comp. Physiol. A 185, 323-340.(doi:10.1007/s003590050392)
49. Gould, J. L. & Gould, C. G. 1988 The honey bee. New York, NY: Scientific American Library.
50. Scheiner, R., Barner, M. & Erber, J. 2003 Variation in water and sucrose responsiveness during the foraging season affects proboscis extension learning in honey bees. Apidologie 34, 67-72.(doi:10.1051/apido:2002050)
51. Kirschfeld, K. 1972 Die notwendige Anzahl von Rezeptoren zur Bestimmung der Richtung des elektrischen Vektors linear polarisierten Lichtes. Z. Naturforsch. 27, 578-579.
52. Bernard, G. D. & Wehner, R. 1977 Functional similarities between polarization vision and color vision. Vis. Res. 17, 1019-1028.(doi:10.1016/0042-6989(77)90005-0)
53. Lambrinos, D., Mö ller, R., Labhart, T., Pfeifer, R. & Wehner, R. 2000 A mobile robot employing insect strategies for navigation. Robot. Auton. Syst. 30, 39-64.(doi:10.1016/S0921-8890(99)00064-0)
54. Mappes, M. & Homberg, U. 2004 Behavioral analysis of polarization vision in tethered flying locusts. J. Comp. Physiol. A 190, 61-68.(doi:10.1007/s00359-003-0473-4)
55. Neuser, K., Triphan, T., Mronz, M., Poeck, B. & Strauss, R. 2008 Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244-1248.