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Visual but not trigeminal mediation of magnetic compass information in a migratory bird

Nature volume 461, pages 1274–1277 (2009)Cite this article

Abstract

Magnetic compass information has a key role in bird orientation1,2,3, but the physiological mechanisms enabling birds to sense the Earth’s magnetic field remain one of the unresolved mysteries in biology2,4. Two biophysical mechanisms have become established as the most promising magnetodetection candidates. The iron-mineral-based hypothesis suggests that magnetic information is detected by magnetoreceptors in the upper beak and transmitted through the ophthalmic branch of the trigeminal nerve to the brain5,6,7,8,9,10. The light-dependent hypothesis suggests that magnetic field direction is sensed by radical pair-forming photopigments in the eyes11,12,13,14,15 and that this visual signal is processed in cluster N, a specialized, night-time active, light-processing forebrain region16,17,18,19. Here we report that European robins with bilateral lesions of cluster N are unable to show oriented magnetic-compass-guided behaviour but are able to perform sun compass and star compass orientation behaviour. In contrast, bilateral section of the ophthalmic branch of the trigeminal nerve in European robins did not influence the birds’ ability to use their magnetic compass for orientation. These data show that cluster N is required for magnetic compass orientation in this species and indicate that it may be specifically involved in processing of magnetic compass information. Furthermore, the data strongly suggest that a vision-mediated mechanism underlies the magnetic compass in this migratory songbird, and that the putative iron-mineral-based receptors in the upper beak connected to the brain by the trigeminal nerve6,7,8 are neither necessary nor sufficient for magnetic compass orientation in European robins.

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Figure 1: Bilateral sectioning of the ophthalmic branch of the trigeminal nerve does not affect magnetic compass orientation in European robins.
Figure 2: Bilateral lesions of cluster N disrupt magnetic compass orientation in European robins.
Figure 3: Birds with cluster N lesions can use their star and sun compasses, but not their magnetic compass.

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Acknowledgements

We thank M. Bourdonnais, D. Hugo, A. Kittel, C. Mora and several volunteer students for assistance, E. Jarvis for scientific discussions, Blumberg GmbH, Rattingen, Germany for providing the thermal paper, the workshops of the University of Oldenburg for building huts, magnetic coil systems and electronic controls and J. Rahn for assistance in the planetarium of the Fachhochschule Oldenburg/Elsfleth. Financial support was provided by the Volkswagenstiftung (to H.M. and D.H.) and by the Deutsche Forschungsgemeinschaft (to H.M.).

Author Contributions H.M. designed and supervised the study. M.Z., C.M.H., S.E. and J.H. performed and M.Z. and C.M.H. supervised the majority of the orientation experiments. M.Z., C.M.H., S.E., J.H. and H.M. analysed the orientation results. J.M.W. and D.H. performed the surgeries. D.H. did the post-mortem histological analyses. D.D. performed the lesion analyses using AMIRA. S.W. and D.K. performed and analysed the operant conditioning. N.-L.S. suggested and made crucial improvements to the experimental set-up. H.M., M.Z., J.M.W. and D.H. wrote most of the paper. All authors read and commented on the manuscript.

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Authors and Affiliations

  1. AG Neurosensorik/Animal Navigation, IBU, University of Oldenburg, D-26111 Oldenburg, Germany

    Manuela Zapka, Dominik Heyers, Christine M. Hein, Svenja Engels, Nils-Lasse Schneider, Jörg Hans, Simon Weiler, David Dreyer, Dmitry Kishkinev & Henrik Mouritsen

  2. Department of Anatomy, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand,

    J. Martin Wild

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Correspondence to Henrik Mouritsen.

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Zapka, M., Heyers, D., Hein, C. et al. Visual but not trigeminal mediation of magnetic compass information in a migratory bird . Nature 461, 1274–1277 (2009). https://doi.org/10.1038/nature08528

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