Skip to main content
SpringerLink
Log in

In search of the sky compass in the insect brain

  • Review
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Like many vertebrate species, insects rely on a sun compass for spatial orientation and long- range navigation. In addition to the sun, however, insects can also use the polarization pattern of the sky as a reference for estimating navigational directions. Recent analysis of polarization vision pathways in the brain of orthopteroid insects sheds some light onto brain areas that might act as internal navigation centers. Here I review the significance, peripheral mechanisms, and central processing stages for polarization vision in insects with special reference to the locust Schistocerca gregaria. As in other insect species, polarization vision in locusts relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Stages in the brain involved in polarized light signaling include specific areas in the lamina, medulla and lobula of the optic lobe and, in the midbrain, the anterior optic tubercle, the lateral accessory lobe, and the central complex. Integration of polarized-light signals with information on solar position appears to start in the optic lobe. In the central complex, polarization-opponent interneurons form a network of interconnected neurons. The organization of the central complex, its connections to thoracic motor centers, and its involvement in the spatial control of locomotion strongly suggest that it serves as a spatial organizer within the insect brain, including the functions of compass orientation and path integration. Time compensation in compass orientation is possibly achieved through a neural pathway from the internal circadian clock in the accessory medulla to the protocerebral bridge of the central complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–D
Fig. 2
Fig. 3A–F
Fig. 4 A, B
Fig. 5

Similar content being viewed by others

References

  • Baker RR (1978) The evolutionary ecology of animal migration. Hodder and Stoughton, London

  • Baker PS, Gewecke M, Cooter RJ (1984) Flight orientation of swarming Locusta migratoria. Physiol Entomol 9:247–252

    Google Scholar 

  • Bingman VP, Able KP (2002) Maps in birds: representational mechanisms and neural bases. Curr Opin Neurobiol 12:745–750

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Labhart T (2000) 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 186:119–128

    Article  CAS  PubMed  Google Scholar 

  • Collett M, Collett TS (2000) How do insects use path integration for their navigation? Biol Cybern 83:245–259

    Article  CAS  PubMed  Google Scholar 

  • Collett TS, Collett M (2002) Memory use in insect visual navigation. Nat Rev Neurosci 3:542–552

    Article  CAS  PubMed  Google Scholar 

  • Eggers A, Gewecke M (1993) The dorsal rim area of the compound eye and polarization vision in the desert locust (Schistocerca gregaria). In: Wiese K, Gribakin FG, Popov AV, Renninger G (eds) Sensory systems of arthropods. Birkhäuser, Basel, pp 101–109

  • Eggers A, Weber T (1993) Behavioural evidence for polarization vision in locusts. In: Elsner N, Heisenberg M (eds) Gene–brain–behaviour. Thieme, Stuttgart, p 336

  • Esch HE, Burns JE (1996) Distance estimation by foraging honeybees. J Exp Biol 199:155–162

    PubMed  Google Scholar 

  • Farrow RA (1990) Flight and migration in acridoids. In Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, pp 227–314

  • Frisch K von (1967) The dance language and orientation of bees. Harvard University Press, Cambridge, Mass.

  • Ghaffar H, Larsen JR, Booth GM, Perkes R (1984) General morphology of the brain of the blind cave beetle, Neaphaenops tellkampfii Erichson (Coleoptera: Carabidae). Int J Insect Morphol Embryol 13:357–371

    Article  Google Scholar 

  • Giurfa M, Capaldi E (1999) Vectors, routes and maps: new discoveries about navigation in insects. Trends Neurosci 22:237–242

    Article  CAS  PubMed  Google Scholar 

  • Goldsmith TH, Wehner R (1977) Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J Gen Physiol 70:453–490

    Google Scholar 

  • Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257:343–366

    Google Scholar 

  • Hartmann G, Wehner R (1995) The ant’s path integration system: a neural architecture. Biol Cybern 73:483–497

    Article  Google Scholar 

  • Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594

    PubMed  Google Scholar 

  • Homberg U (1987) Structure and functions of the central complex in insects. In Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. Wiley, New York, pp 347–367

    Google Scholar 

  • Homberg U (1994a) 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

    Google Scholar 

  • Homberg U (1994b) Distribution of neurotransmitters in the insect brain. (Progress in Zoology 40) Fischer, Stuttgart

  • Homberg U, Hildebrand JG (1994) Postembryonic development of γ-aminobutyric acid-like immunoreactivity in the brain of the sphinx moth Manduca sexta. J Comp Neurol 339:132–149

    Google Scholar 

  • Homberg U, Paech A (2002) Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30:271–280

    Google Scholar 

  • 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 386:329–346

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Würden S, Dircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266:343–357

    Google Scholar 

  • 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 462:415–430

    Article  PubMed  Google Scholar 

  • Homberg U, Reischig T, Stengl M (2003b) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591

    Article  CAS  PubMed  Google Scholar 

  • Horváth G, Varjú D (2003) Polarization patterns in nature and polarized light in animal vision. Springer, Berlin Heidelberg New York

  • Israelachvili JN, Wilson M (1976) Absorption characteristics of oriented photopigments in microvilli. Biol Cybern 21:9–15

    CAS  PubMed  Google Scholar 

  • Kanzaki R (1998) Coordination of wing motion and walking suggests common control of zigzag motor program in a male silkworm moth. J Comp Physiol A 182:267–276

    Article  Google Scholar 

  • Kennedy JS (1945) Observations on the mass migration of desert locust hoppers. Trans R Entomol Soc Lond 95:247–262

    Google Scholar 

  • Kennedy JS (1951) The migration of the desert locust (Schistocerca gregaria FORSK.). I. The behaviour of swarms. II. A theory of long-range migrations. Philos Trans R Soc Ser B 235:163–290

    Google Scholar 

  • Labhart T (1988) Polarization-opponent interneurones in the insect visual system. Nature 331:435–437

    Article  Google Scholar 

  • Labhart T (1996) How polarization-sensitive interneurones of crickets perform at low degrees of polarization. J Exp Biol 199:1467–1475

    PubMed  Google Scholar 

  • Labhart T (2000) Polarization-sensitive interneurons in the optic lobe of the desert ant Cataglyphis bicolor. Naturwissenschaften 87:133–136

    Google Scholar 

  • 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 47:368–379

    Article  CAS  PubMed  Google Scholar 

  • Labhart T, Meyer EP (2002) Neural mechanisms in insect navigation: polarization compass and odometer. Curr Opin Neurobiol 12:707–714

    Article  CAS  PubMed  Google Scholar 

  • Labhart T, Petzold J (1993) Processing of polarized light information in the visual system of crickets. In Wiese K, Gribakin F, Popov AV, Renninger G (eds) Sensory system of arthropods. Birkhäuser, Basel, pp 158–168

  • Labhart T, Petzold J, Helbling H (2001) Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J Exp Biol 204:2423–2430

    Google Scholar 

  • Lambrinos D (2003) Navigation in desert ants: the robotic solution. Robotica 21:407–426

    Article  Google Scholar 

  • Lindauer M (1954) Dauertänze im Bienenstock und ihre Beziehung zur Sonnenbahn. Naturwissenschaften 41:506–507

    Google Scholar 

  • Lindauer M (1960) Time-compensated sun orientation in bees. Cold Spring Harbor Symp Quant Biol 25:371–377

    CAS  PubMed  Google Scholar 

  • Loesel R, Homberg U (2001) Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach Leucophaea maderae. J Comp Neurol 439:193–207

    Article  CAS  PubMed  Google Scholar 

  • Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190:61–68

    Article  CAS  Google Scholar 

  • Meinertzhagen IA, Sorra KE (2001) Synaptic organization in the fly’s optic lamina: few cells, many synapses and divergent microcircuits. In: Kolb H, Robbs H, Wu S (eds) Progress in brain research, vol 131. Elsevier, New York, pp 53–69

  • Mishima T, Kanzaki R (1998) Coordination of flipflopping neural signals and head turning during pheromone-mediated walking in a male silkworm moth Bombyx mori. J Comp Physiol A 183:273–282

    Article  Google Scholar 

  • Mishima T, Kanzaki R (1999) Physiological and morphological characterization of olfactory descending interneurons of the male silkworm moth, Bombyx mori. J Comp Physiol A 184:143–160

    Article  Google Scholar 

  • Mouritsen H (2001) Navigation in birds and other animals. Image Vis Comput 19:713–731

    Article  Google Scholar 

  • Mouritsen H, Frost, BJ (2002) Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proc Natl Acad Sci USA 99:10162–10166

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Homberg U, Kühn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288:159–176

    PubMed  Google Scholar 

  • Nilsson D, Labhart T, Meyer EP (1987) Photoreceptor design and optical properties affecting polarization sensitivity in ants and crickets. J Comp Physiol A 161:645–658

    Google Scholar 

  • Panov AA (1959) Structure of the insect brain at successive stages of postembryonic development. II. The central body. Entomol Rev URSS 38:276–284

    Google Scholar 

  • Papi F (1992) Animal homing. Chapman and Hall, London

  • Petzold J (2001) Polarisationsempfindliche Neuronen im Sehsystem der Feldgrille, Gryllus campestris: Elektrophysiologie, Anatomie und Modellrechnungen. PhD thesis, University of Zurich

  • Pfeiffer K, Homberg U (2003) Neurons of the anterior optic tubercle of the locust Schistocerca gregaria are sensitive to the plane of polarized light. In Elsner N, Zimmermann N (eds) The neurosciences from basic research to therapy. Thieme, Stuttgart, pp 567–568

  • Riley JR, Reynolds DR (1986) Orientation at night by high-flying insects. In Danthanarayana W (ed) Insect flight: dispersal and migration. Springer, Berlin Heidelberg New York, pp 71–87

    Google Scholar 

  • Riley JR, Greggers U, Smith AD, Stach S, Reynolds DR, Stollhoff N, Brandt R, Schaupp F, Menzel R (2003) The automatic pilot of honeybees. Proc R Soc Lond B 270:2421–2424

    Article  CAS  PubMed  Google Scholar 

  • Rossel S, Wehner R (1987) The bee’s e-vector compass. In Menzel R, Mercer A (eds) Neurobiology and behaviour of honeybees. Springer, Berlin Heidelberg New York, pp 76–93

  • Schaefer GW (1976) Radar observations of insect flight. In Rainey RC (ed) Insect flight. (Symposium of the Royal Entomological Society vol 7) Blackwell, Oxford, pp 157–197

  • Sharp PE, Blair HT, Cho J (2001) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289–294

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan VM, Zhang SW, Altwen M, Tautz J (2000) Honeybee navigation: nature and calibration of the odometer. Science 287:851–853

    CAS  PubMed  Google Scholar 

  • Strausfeld NJ (1999) A brain region in insects that supervises walking. In Binder MD (ed) Progress in brain research, vol 123. Elsevier, Amsterdam, pp. 273–284

  • Strausfeld NJ, Blest AD (1970) Golgi studies on insects. Part I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond Ser B 258:81–134

    Google Scholar 

  • Strausfeld NJ, Nässel DR (1981) Neuroarchitectures serving compound eyes of Crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 1–132

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    Article  CAS  PubMed  Google Scholar 

  • Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852–1861

    CAS  PubMed  Google Scholar 

  • Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225–256

    CAS  PubMed  Google Scholar 

  • Tinbergen N (1932) Über die Orientierung des Bienenwolfes (Philanthus triangulum Fabr.). Z Vgl Physiol 16:305–334

    Google Scholar 

  • Uvarov BP (1966) Grasshoppers and locusts, vol 1. Cambridge University Press, New York

  • Vitzthum H, Homberg U (1998) Locustatachykinin I/II-immunoreactive neurons in the central complex of the locust brain. J Comp Neurol 390:455–469

    Article  CAS  PubMed  Google Scholar 

  • Vitzthum H, Homberg U, Agricola H (1996) Distribution of Dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369:419–437

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wang RF, Spelke ES (2002) Human spatial representation: insights from animals. Trends Cogn Sci 6:1114–1125

    Google Scholar 

  • Waterman TH (1989) Animal navigation. Freeman, New York

  • Wehner R (1984) Astronavigation in insects. Annu Rev Entomol 29:277–298

    Google Scholar 

  • Wehner R (1992) Arthropods. In: Papi F (ed) Animal homing. Chapman and Hall, London, pp 45–144

  • Wehner R (1994) The polarization-vision project: championing organismic biology. In: Schildberger K, Elsner N (eds) Neural basis of behavioural adaptations. Fischer, Stuttgart, pp 103–143

  • Wehner R (1997) The ant’s celestial compass system: spectral and polarization channels. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, Basel, pp 145–185

  • Wehner R (2001) Polarization vision: a uniform sensory capacity? J Exp Biol 204:2589–2596

    CAS  PubMed  Google Scholar 

  • Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588

    CAS  Google Scholar 

  • Wehner R, Bernhard GD (1993) Photoreceptor twist: a solution to the false color problem. Proc Natl Acad Sci USA 90:4132–4135

    CAS  PubMed  Google Scholar 

  • Wehner R, Michel B, Antonsen P (1996) Visual navigation in insects: coupling of egocentric and geocentric information. J Exp Biol 199:129–140

    PubMed  Google Scholar 

  • Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool 76:67–86

    Google Scholar 

  • Wittmann T, Schwegler H (1995) Path integration: a network model. Biol Cybern 73:569–575

    Article  Google Scholar 

  • Wohlgemuth S, Ronacher B, Wehner R (2002) Distance estimation in the third dimension in desert ants. J Comp Physiol A 188:273–281

    Google Scholar 

  • Würden S, Homberg U (1995) Immunocytochemical mapping of serotonin and neuropeptides in the accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol 362:305–319

    PubMed  Google Scholar 

  • Zufall F, Schmitt M, Menzel R (1989) Spectral and polarized light sensitivity of photoreceptors in the compound eye of the cricket (Gryllus bimaculatus). J Comp Physiol A 164:597–608

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I am grateful to Dr. Monika Stengl for her helpful comments on the manuscript and to Sascha Gotthardt for providing Fig. 3E, F. The research described in this paper is supported by the Deutsche Forschungsgemeinschaft, currently HO 950/13-2 and HO 950/14-1.

Author information

Authors and Affiliations

  1. Fachbereich Biologie/Tierphysiologie, Philipps-Universität Marburg, 35032, Marburg, Germany

    Uwe Homberg

Authors
  1. Uwe Homberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uwe Homberg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Homberg, U. In search of the sky compass in the insect brain. Naturwissenschaften 91, 199–208 (2004). https://doi.org/10.1007/s00114-004-0525-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-004-0525-9

Keywords

Search

Navigation