Journal of Comparative Physiology A

, Volume 193, Issue 1, pp 43–50 | Cite as

Surgical lesion of the anterior optic tract abolishes polarotaxis in tethered flying locusts, Schistocerca gregaria

Original Paper

Abstract

Many insects can detect the polarization pattern of the blue sky and rely on polarization vision for sky compass orientation. In laboratory experiments, tethered flying locusts perform periodic changes in flight behavior under a slowly rotating polarizer even if one eye is painted black. Anatomical tracing studies and intracellular recordings have suggested that the polarization vision pathway in the locust brain involves the anterior optic tract and tubercle, the lateral accessory lobe, and the central complex of the brain. To investigate whether visual pathways through the anterior optic tract mediate polarotaxis in the desert locust, we transected the tract on one side and tested polarotaxis (1) with both eyes unoccluded and (2) with the eye of the intact hemisphere painted black. In the second group of animals, but not in the first group, polarotaxis was abolished. Sham operations did not impair polarotaxis. The experiments show that the anterior optic tract is an indispensable part of visual pathways mediating polarotaxis in the desert locust.

Keywords

Polarization vision Polarotaxis Visual system Compass navigation Schistocerca gregaria 

Abbreviations

AOT

Anterior optic tract

AOTu

Anterior optic tubercle

DRA

Dorsal rim area

FFT

Fast Fourier transform

LD

Light–dark

PAP

Peroxidase–antiperoxidase

POT

Posterior optic tract

POTu

Posterior optic tubercle

References

  1. Brunner D, Labhart T (1987) Behavioural evidence for polarization vision in crickets. Physiol Entomol 12:1–10Google Scholar
  2. Dacke M, Nordström P, Scholtz C (2003) Twilight orientation to polarised light in the crepuscular dung beetle Scarabaeus zambesianus. J Exp Biol 206:1535–1543PubMedCrossRefGoogle Scholar
  3. von Frisch K (1949) Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5:142–148CrossRefPubMedGoogle Scholar
  4. Gewecke M (1975) The influence of the air-current sense organs on the flight behaviour of Locusta migratoria. J Comp Physiol 103:79–95CrossRefGoogle Scholar
  5. Hausen K, Wehrhahn C (1983) Microsurgical lesion of horizontal cells changes optomotor yaw responses in the blowfly Calliphora erythrocephala. Proc R Soc Lond B 219:211–216CrossRefGoogle Scholar
  6. Heinze S, Homberg U (2005) A new set of tangential neurons of the protocerebral bridge in the desert locust Schistocerca gregaria is sensitive to polarized light. 98. Annual meeting of the DZG, Bayreuth, p 73. http://www.uni-bayreuth.de/dzg-gebin2005
  7. Hofer S, Dircksen H, Tollbäck P, Homberg U (2005) Novel insect orcokinins: characterization and neuronal distribution in the brains of selected dicondylian insects. J Comp Neurol 490:57–71PubMedCrossRefGoogle Scholar
  8. Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245–254PubMedCrossRefGoogle Scholar
  9. Homberg U (2004) In search of the sky compass in the insect brain. Naturwissenschaften 91:199–208PubMedCrossRefGoogle Scholar
  10. Homberg U, Heinze S (2006) A computational map of e-vector orientations in the central complex of the desert locust (Schistocerca gregaria). FENS Abstr 3:A129.9Google Scholar
  11. Homberg U, Würden S (1997) Movement-sensitive, polarization-sensitive, and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol 386:329–346PubMedCrossRefGoogle Scholar
  12. Homberg U, Hofer S, Pfeiffer K, Gebhardt S (2003a) Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462:415–430CrossRefGoogle Scholar
  13. Homberg U, Reischig T, Stengl M (2003b) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591CrossRefGoogle Scholar
  14. Labhart T, Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47:368–379PubMedCrossRefGoogle Scholar
  15. Labhart T, Meyer EP (2002) Neural mechanisms in insect navigation: polarization compass and odometer. Curr Opin Neurobiol 12:707–714PubMedCrossRefGoogle Scholar
  16. Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf R, Heisenberg M, Liu L (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–556PubMedCrossRefGoogle Scholar
  17. Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190:61–68CrossRefGoogle Scholar
  18. Pfeiffer K, Kinoshita M, Homberg U (2005) Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94:3903–3915PubMedCrossRefGoogle Scholar
  19. von Philipsborn A, Labhart T (1990) A behavioral study of polarization vision in the fly, Musca domestica. J Comp Physiol A 167:737–743CrossRefGoogle Scholar
  20. Preiss R, Gewecke M (1991) Compensation of visually simulated wind drift in the swarming flight of the desert locust (Schistocerca gregaria). J Exp Biol 157:461–481Google Scholar
  21. Rossel S, Wehner R (1986) Polarization vision in bees. Nature 323:128–131CrossRefGoogle Scholar
  22. Sakura M, Labhart T (2005) Polarization-sensitive neurons in the central complex of the cricket, Gryllus bimaculatus. Neuroforum (Suppl):154BGoogle Scholar
  23. Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, Yuan Q, Casselman A, Reppert SM (2005) Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46:457–467PubMedCrossRefGoogle Scholar
  24. Stalleicken J, Mukhida M, Labhart T, Wehner R, Frost B, Mouritsen M (2005) Do monarch butterflies use polarized skylight for migratory orientation? J Exp Biol 208:2399–2408PubMedCrossRefGoogle Scholar
  25. Sternberger LA (1979) Immunocytochemistry.Wiley, New YorkGoogle Scholar
  26. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638PubMedCrossRefGoogle Scholar
  27. Vitzthum H, Homberg U (1998) Immunocytochemical demonstration of locustatachykinin-related peptides in the central complex of the locust brain. J Comp Neurol 390:455–469PubMedCrossRefGoogle Scholar
  28. Vitzthum H, Müller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114–1125PubMedGoogle Scholar
  29. Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Biology, Animal PhysiologyPhilipps-University of MarburgMarburgGermany

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