Skip to main content
SpringerLink
Log in

Integration of polarization and chromatic cues in the insect sky compass

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Animals relying on a celestial compass for spatial orientation may use the position of the sun, the chromatic or intensity gradient of the sky, the polarization pattern of the sky, or a combination of these cues as compass signals. Behavioral experiments in bees and ants, indeed, showed that direct sunlight and sky polarization play a role in sky compass orientation, but the relative importance of these cues are species-specific. Intracellular recordings from polarization-sensitive interneurons in the desert locust and monarch butterfly suggest that inputs from different eye regions, including polarized-light input through the dorsal rim area of the eye and chromatic/intensity gradient input from the main eye, are combined at the level of the medulla to create a robust compass signal. Conflicting input from the polarization and chromatic/intensity channel, resulting from eccentric receptive fields, is eliminated at the level of the anterior optic tubercle and central complex through internal compensation for changing solar elevations, which requires input from a circadian clock. Across several species, the central complex likely serves as an internal sky compass, combining E-vector information with other celestial cues. Descending neurons, likewise, respond both to zenithal polarization and to unpolarized cues in an azimuth-dependent way.

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. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 

  • Brines ML, Gould JL (1979) Bees have rules. Science 206:571–573

    Article  CAS  PubMed  Google Scholar 

  • Coemans MAJM, Vos Hzn JJ, Nuboer JFW (1994) The relation between celestial colour gradients and the position of the sun, with regard to the sun compass. Vis Res 34:1461–1470

    Article  CAS  PubMed  Google Scholar 

  • Dacke M, Nordström P, Scholtz CH, Warrant E (2002) A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum. J Comp Physiol A 188:211–216

    Article  CAS  Google Scholar 

  • Dacke M, el Jundi B, Smolka J, Byrne M, Baird E (2014) The role of the sun in the celestial compass of dung beetles. Philos Trans R Soc B 369:20130036

    Article  CAS  Google Scholar 

  • Edrich W, Neumeyer C, von Helversen O (1979) “Anti-sun orientation” of bees with regard to a field of ultraviolet light. J Comp Physiol 134:151–157

    Article  Google Scholar 

  • el Jundi B, Homberg U (2010) Evidence for the possible existence of a second polarization-vision pathway in the locust brain. J Insect Physiol 56:971–979

    Article  PubMed  Google Scholar 

  • el Jundi B, Homberg U (2012) Receptive field properties and intensity-response functions of polarization-sensitive neurons of the optic tubercle in gregarious and solitarious locusts. J Neurophysiol 108:1695–1710

    Article  PubMed  Google Scholar 

  • el Jundi B, Heinze S, Kurylas A, Lenschow C, Rohlfing R, Homberg U (2010) The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3:21

    PubMed Central  PubMed  Google Scholar 

  • el Jundi B, Pfeiffer K, Homberg U (2011) A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PLoS One 6:e27855

    Article  PubMed Central  PubMed  Google Scholar 

  • el Jundi B, Smolka J, Baird E, Byrne M, Dacke M (2014) Diurnal dung beetles use the intensity gradient and polarization pattern of the sky for orientation. J Exp Biol (in revision)

  • Frost BJ, Mouritsen H (2006) The neural mechanisms of long distance animal navigation. Curr Opin Neurobiol 16:481–488

    Google Scholar 

  • Gould JL (1998) Sensory bases of navigation. Curr Biol 8:R731–R738

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–997

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454–478

    Article  PubMed  Google Scholar 

  • Heinze S, Homberg U (2009) Linking the input to the output: new sets of neurons complement the polarization vision network in the locust central complex. J Neurosci 29:4911–4921

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Reppert SM (2011) Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–358

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Gotthardt S, Homberg U (2009) Transformation of polarized light information in the central complex of the locust. J Neurosci 29:11783–11793

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Florman J, Asokaraj S, el Jundi B, Reppert SM (2013) Anatomical basis of sun compass navigation II: the neuronal composition of the central complex of the monarch butterfly. J Comp Neurol 521:267–298

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Henze MJ, Dannenhauer K, Kohler M, Labhart T, Gesemann M (2012) Opsin evolution and expression in arthropod compound eyes and ocelli: insights from the cricket Gryllus bimaculatus. BMC Evol Biol 12:163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifera, L.). J Insect Physiol 31:251–264

    Article  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

    Article  PubMed  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, Hofer S, Pfeiffer K, Gebhardt S (2003) 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, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B (2011) Central neural coding of sky polarization in insects. Philos Trans R Soc B 366:680–687

    Article  Google Scholar 

  • Kinoshita M, Pfeiffer K, Homberg U (2007) Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210:1350–1361

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Labhart T (1986) The electrophysiology of photoreceptors in different eye regions of the desert ant, Cataglyphis bicolor. J Comp Physiol A 158:1–7

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Labhart T (1996) How polarization-sensitive interneurons 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

    Article  CAS  PubMed  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, Hodel B, Valenzuela I (1984) The physiology of the cricket’s compound eye with particular reference to the anatomically specialized dorsal rim area. J Comp Physiol A 155:289–296

    Article  Google Scholar 

  • Labhart T, Meyer EP, Schenker L (1992) Specialized ommatidia for polarization vision in the compound eye of cockchafers, Melolontha melolontha (Coleoptera, Scarabaeidae). Cell Tissue Res 268:419–429

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Labhart T, Baumann F, Bernard GD (2009) Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta. Cell Tissue Res 338:391–400

    Article  PubMed Central  PubMed  Google Scholar 

  • Lin C-Y, Chuang C-C, Hua T-E, Chen C-C, Dickson BJ, Greenspan RJ, Chiang A-S (2013) A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Rep 3:1739–1753

    Article  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 

  • Pfeiffer K, Homberg U (2007) Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17:960–965

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer K, Kinoshita M (2012) Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus). J Comp Neurol 520:212–229

    Article  PubMed  Google Scholar 

  • 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 94:3903–3915

    Article  PubMed  Google Scholar 

  • Pfeiffer K, Negrello M, Homberg U (2011) 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

    Article  PubMed  Google Scholar 

  • Reppert SM, Zhu H, White RH (2004) Polarized light helps monarch butterflies navigate. Curr Biol 14:155–158

    Article  CAS  PubMed  Google Scholar 

  • Roberts NW, Porter ML, Cronin TW (2011) The molecular basis of mechanisms underlying polarization vision. Philos Trans R Soc B 366:627–637

    Article  CAS  Google Scholar 

  • Rosner R, Homberg U (2013) Widespread sensitivity to looming stimuli and small moving objects in the central complex of an insect brain. J Neurosci 33:8172

    Article  Google Scholar 

  • Rossel S, Wehner R (1984) Celestial orientation in bees: the use of spectral cues. J Comp Physiol 155:605–613

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Seelig JD, Jayaraman V (2013) Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–266

    CAS  PubMed  Google Scholar 

  • Stalleicken J, Mukhida M, Labhart T, Wehner R, Frost B, Mouritsen H (2005) Do monarch butterflies use polarized skylight for migratory orientation? J Exp Biol 208:2399–2408

    Article  PubMed  Google Scholar 

  • Stalleicken J, Labhart T, Mouritsen H (2006) Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J Comp Physiol A 192:321–331

    Article  Google Scholar 

  • Träger U, Homberg U (2011) Polarization-sensitive descending neurons in the locust: connecting the brain to thoracic ganglia. J Neurosci 31:2238–2247

    Article  PubMed  Google Scholar 

  • Träger U, Wagner R, Bausenwein B, Homberg U (2008) A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506:288–300

    Article  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 

  • von Frisch K (1949) Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5:142–148

    Article  CAS  PubMed  Google Scholar 

  • von Frisch K (1965) Tanzsprache und Orientierung der Bienen. Springer, Berlin

    Book  Google Scholar 

  • 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

    Chapter  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. Proc Natl Acad Sci 103:12575–12579

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wehner R, Bernard GD, Geiger E (1975) Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee. J Comp Physiol 104:225–245

    Article  Google Scholar 

  • Wernet MF, Velez MM, Clark DA, Baumann-Klausener F, Brown JR, Klovstad M, Labhart T, Clandinin TR (2012) Genetic dissection reveals two separate retinal substrates for polarization vision in Drosophila. Curr Biol 22:12–20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Deutsche Forschungsgemeinschaft (HO 950/16-1, 16-2 and 16-3) to UH.

Author information

Authors and Affiliations

  1. Faculty of Biology, Animal Physiology, Philipps-University of Marburg, 35032, Marburg, Germany

    Keram Pfeiffer & Uwe Homberg

  2. Vision Group, Department of Biology, Lund University, Sölvegatan 35, 22362, Lund, Sweden

    Basil el Jundi & Stanley Heinze

Authors
  1. Basil el Jundi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Keram Pfeiffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stanley Heinze
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. 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

el Jundi, B., Pfeiffer, K., Heinze, S. et al. Integration of polarization and chromatic cues in the insect sky compass. J Comp Physiol A 200, 575–589 (2014). https://doi.org/10.1007/s00359-014-0890-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-014-0890-6

Keywords

Search

Navigation