Neural mechanisms in insect navigation: Polarization compass and odometer

Current Opinion in Neurobiology

Volumn 12, Issue 6, 2002, Pages 707-714

  Labhart, Thomas ^a   Meyer, Eric P ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANT; BRAIN; CONTROLLED STUDY; FLIGHT; FLYING; HONEYBEE; INSECT; LOCUST; NERVE CELL; NONHUMAN; OPTIC LOBE; PHOTORECEPTOR; POLARIZATION; PRIORITY JOURNAL; PROPRIOCEPTION; RETINA; REVIEW; SENSE ORGAN; SENSORY SYSTEM; SMELLING; SPATIAL ORIENTATION; THEORETICAL MODEL; TRAVEL;

EID: 0036902998     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(02)00384-7     Document Type: Review

References (63)

1. Wehner R. Arthropods. Papi F. Animal Homing. 1992;45-144 Chapman & Hall, London.
2. von Frisch K. The Dance Language and Orientation of Bees. 1993;Harvard University Press, Cambridge.
3. Wehner R. Navigation in context: grand theories and basic means. J Avian Biol. 29:1998;370-386.
4. Collett M., Collett T.S. How do insects use path integration for their navigation? Biol Cybern. 83:2000;245-259.
5. Collett T.S., Collett M. Path integration in insects. Curr Opin Neurobiol. 10:2000;757-762.
6. Wehner R., Gallizzi K., Frei C., Vesely M. Calibration processes in desert ant navigation: vector courses and systematic search. J Comp Physiol [A]. 188:2002;683-693.
7. Dyer F.C., Dickinson J.A. Development of sun compensation by honeybees: how partially experienced bees estimate the sun's course. Proc Natl Acad Sci USA. 91:1994;4471-4474.
8. Wehner R. The ant's celestial compass system: spectral and polarization channels. Lehrer M. Orientation and Communication in Arthropods. 1997;145-185 Birkhäuser Verlag, Basel.
9. Israelachvili J.N., Wilson M. Absorption characteristics of oriented photopigments in microvilli. Biol Cybern. 21:1976;9-15.
10. Goldsmith T.H., Wehner R. Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol. 70:1977;453-490.
11. Hardie R.C. Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J Comp Physiol [A]. 154:1984;157-165.
12. Wehner R., Bernard G.D., Geiger E. Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J Comp Physiol. 104:1975;225-245.
13. Nilsson D., Labhart T., Meyer E.P. Photoreceptor design and optical properties affecting polarization sensitivity in ants and crickets. J Comp Physiol [A]. 161:1987;645-658.
14. Labhart T., Meyer E.P. Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech. 47:1999;368-379. This survey of ommatidial specializations in the DRA demonstrates that the detection of polarized skylight is a common visual function in insects. Although the DRA ommatidia are functionally similar in different insect groups, differences in ommatidial fine structure indicate that the polarization compass arose polyphyletically.
15. Dacke M., Nordström P., Scholtz C.H., Warrant E.J. A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum. J Comp Physiol [A]. 188:2002;211-216.
16. Homberg U., Paech A. Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev. 30:2002;271-280.
17. Labhart T., Hodel B., Valenzuela I. The physiology of the cricket's compound eye with particular reference to the anatomically specialized dorsal rim area. J Comp Physiol [A]. 155:1984;289-296.
18. Labhart T. The electrophysiology of photoreceptors in different eye regions of the desert ant, Cataglyphis bicolor. J Comp Physiol [A]. 158:1986;1-7.
19. Labhart T. Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: polarizational and angular sensitivity. J Comp Physiol. 141:1980;19-30.
20. Wehner R., Bernard G.D. Photoreceptor twist: a solution to the false-color problem. Proc Natl Acad Sci USA. 90:1993;4132-4135.
21. Dacke M., Nilsson D.-E., Warrant E.J., Blest A.D., Land M.F., O'Carroll D.C. Built-in polarizers form part of a compass organ in spiders. Nature. 401:1999;470-473. This is the first time that a polarizing optical element was found in an eye. The secondary, postero-median eyes of the spider Drassodes are highly specialized polarization-detecting organs missing imaging optics and sporting a polarizing tapetum.
22. Dacke M., Doan T.A., O'Carroll D.C. Polarized light detection in spiders. J Exp Biol. 204:2001;2481-2490. This paper surveys the polarization detecting organs of spiders. The lycosid type of polarization detector, a specialized ventral area of the principal, antero-median eyes, is functionally analogous to the DRA of insects and is present in several spider families. Secondary eyes with polarizing tapeta were found in many spiders, although their significance for polarization vision is clear for Drassodes only.
23. Rossel S. Navigation by bees using polarized light. Comp Biochem Physiol [A]. 104:1993;695-708.
24. Petzold J: Polarisationsempfindliche Neuronen im Sehsystem der Feldgrille, Gryllus campestris: Elektrophysiologie, Anatomie und Modellrechnungen. PhD thesis, University of Zürich, 2001. [Translation of the title: Polarization sensitive neurons in optical systems of crickets: electrophysiology, anatomy and model calculations].
25. Labhart T., Petzold J. Processing of polarized light information in the visual system of crickets. Wiese K., Gribakin F.G., Popov A.V., Renninger G. Sensory Systems of Arthropods. 1993;158-168 Birkhäuser Verlag, Basel.
26. Labhart T. Polarization-opponent interneurons in the insect visual system. Nature. 331:1988;435-437.
27. Labhart T. How polarization-sensitive interneurones of crickets perform at low degrees of polarization. J Exp Biol. 199:1996;1467-1475.
28. Blum M., Labhart T. Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J Comp Physiol [A]. 186:2000;119-128.
29. Labhart T., Petzold J., Helbling H. Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J Exp Biol. 204:2001;2423-2430. On the basis of histological and electrophysiological data, the paper explains the optical and neural mechanisms leading to spatial integration in POL-neurons and discusses reasons why the cricket polarization vision system has abandoned spatial resolution.
30. Labhart T. How polarization-sensitive interneurones of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neurone. J Exp Biol. 202:1999;757-770.
31. Herzmann D., Labhart T. Spectral sensitivity and absolute threshold of polarization vision in crickets: a behavioral study. J Comp Physiol [A]. 165:1989;315-319.
32. Gál J., Horváth G., Barta A., Wehner R. Polarization of the moonlit clear night sky measured by full-sky imaging polarimetry at full moon: comparison of the polarization of moonlit and sunlit skies. J Geophys Res. 106:2001;22647-22653.
33. Gebhardt S., Homberg U. Columnar neurons of the central complex in the brain of the locust Schistocerca gregaria are sensitive to polarized light. Elsner N., Kreutzberg G.W. Proceedings of the 28th Göttingen Neurobiology Conference. 2001;520 Thieme, Stuttgart.
34. Vitzthum H., Müller M., Homberg U. Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci. 22:2002;1114-1125. The physiology and morphology of POL-neurons in the central brain of locusts were examined by intracellular recording and dye marking. This is the first time that data on neurons representing central processing of polarized skylight information became available.
35. Hofer S., Homberg U. Anatomical organization of the anterior optic tubercle in the brain of the locust Schistocerca gregaria. Elsner N., Kreutzberg G.W. Proceedings of the 28th Göttingen Neurobiology Conference. 2001;521 Thieme, Stuttgart, New York.
36. Pfeiffer K, Homberg U: Visual signal processing in neurons of the anterior optic tubercle of the locust, Schistocerca gregaria. Zoology 2002, 105(Suppl. V):45. [Translation of title: The necessary number of receptors for the determination of the direction of electrical vectors of linear polarized light].
37. Kirschfeld K. Die notwendige Anzahl von Rezeptoren zur Bestimmung der Richtung des elektrischen Vektors linear polarisierten Lichtes. Z Naturforsch. 27:1972;578-579. [Translation of the title:].
38. Bernard G.D., Wehner R. Functional similarities between polarization vision and color vision. Vision Res. 17:1977;1019-1028.
39. Lambrinos D., Maris M., Kobayashi H., Labhart T., Pfeifer R., Wehner R. An autonomous agent navigating with a polarized light compass. Adaptive Behav. 6:1997;131-161.
40. Lambrinos D., Möller R., Labhart T., Pfeifer R., Wehner R. A mobile robot employing insect strategies for navigation. Robot Auton Syst. 30:2000;39-64.
41. Taube J.S., Muller R.U., Ranck J.B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci. 10:1990;420-435.
42. Hartmann G., Wehner R. The ant's path integration system: a neural architecture. Biol Cybern. 73:1995;483-497.
43. Wehner R. Polarization vision - a uniform sensory capacity? J Exp Biol. 204:2001;2589-2596.
44. Labhart T, Lambrinos D: How does the insect nervous system code celestial e-vector orientation? A neural model for "compass neurons". International Conference on Invertebrate Vision, 7-12 August 2001, Bäckaskog Castle, Sweden, p 66.
45. Labhart T: Neuromimetic models of the polarization compass: using the synthetic approach. URL: http://www.zool.unizh.ch/neurobiology/labhart/tl_2.html.
46. Labhart T. Polarization-sensitive interneurons in the optic lobe of the desert ant Cataglyphis bicolor. Naturwiss. 87:2000;133-136.
47. Homberg U., Würden S. Movement-sensitive, polarization-sensitive and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol. 386:1997;329-346.
48. Loesel R., Homberg U. Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol. 439:2001;193-207.
49. Helfrich-Förster C., Stengl M., Homberg U. Organization of the circadian system in insects. Chronobiol Int. 15:1998;576-594.
50. Esch H.E., Burns J.E. Distance estimation by foraging honeybees. J Exp Biol. 199:1996;155-162.
51. Srinivasan M.V., Zhang S.W., Bidwell N.J. Visually mediated odometry in honeybees. J Exp Biol. 200:1997;2513-2522.
52. Srinivasan M.V., Zhang S., Altwein M., Tautz J. Honeybee navigation: nature and calibration of the "odometer" Science. 287:2000;851-853. In this cleverly designed behavioral study, forager bees visited a food source by either flying through an environment with relatively distant objects (outdoors) or near visual stimuli (narrow tunnel with textured walls), producing vastly different amounts of image motion on the eye per distance flown. Comparing the foragers' waggle dances for the two situations showed that the odometer is not calibrated in absolute distance units but in optic-flow units.
53. Esch H.E., Zhang S., Srinivasan M.V., Tautz J. Honeybee dances communicate distances measured by optic flow. Nature. 411:2001;581-583. This paper demonstrates that the bee's interpretation of waggle dance frequency strongly depends on the visual environment. At a given waggle duration, recruits directed to open terrain fly much further than through a tree-clustered area, that is, the dances provide no information about the visual structure of the foraging area.
54. Hausen K., Egelhaaf M. Neural mechanisms of visual course control in insects. Stavenga D.G., Hardie R.C. Facets of Vision. 1989;391-424 Springer, Berlin.
55. Srinivasan M.V., Poteser M., Kral K. Motion detection in insect orientation and navigation. Vision Res. 39:1999;2749-2766.
56. Ronacher B., Wehner R. Desert ants Cataglyphis fortis use self-induced optic flow to measure distances travelled. J Comp Physiol [A]. 177:1995;21-27.
57. Ronacher B., Gallizzi K., Wohlgemuth S., Wehner R. Lateral optic flow does not influence distance estimation in the desert ant Cataglyphis fortis. J Exp Biol. 203:2000;1113-1121.
58. Schäfer M., Wehner R. Loading does not affect measurement of walking distance in desert ants Cataglyphis fortis. Verh Dtsch Zool Ges. 86:1993;270.
59. Wohlgemuth S., Ronacher B., Wehner R. Distance estimation in the third dimension in desert ants. J Comp Physiol [A]. 188:2002;273-281. This paper extends the navigation studies with Cataglyphis to the third dimension. The ants were trained to walk in an array of uphill and downhill channels. When tested on flat terrain, the ants indicated homing distances corresponding to the ground distances travelled (compare Fig. 4). These and several carefully designed control experiments feed a thorough discussion on the nature of the ant's odometer.
60. Wohlgemuth S., Ronacher B., Wehner R. Ant odometry in the third dimension. Nature. 411:2001;795-798.
61. Wehner R., Wehner S. Insect navigation: use of maps or Ariadne's thread? Ethol Ecol Evol. 2:1990;27-48.
62. Markl H. Borstenfelder an den Gelenken als Schweresinnesorgane bei Ameisen und anderen Hymenopteren. Z Vergl Physiol. 45:1962;475-569. [Translation of the title: Areas of bristles on the joints as weight sensing organs in ants and other hymenoptera].
63. Rossel S., Wehner R. Polarization vision in bees. Nature. 323:1986;128-131.