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Published July 24, 2012 | Published + Supplemental Material
Journal Article Open

Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells

Abstract

Over the past 50 y, behavioral experiments have produced a large body of evidence for the existence of a magnetic sense in a wide range of animals. However, the underlying sensory physiology remains poorly understood due to the elusiveness of the magnetosensory structures. Here we present an effective method for isolating and characterizing potential magnetite-based magnetoreceptor cells. In essence, a rotating magnetic field is employed to visually identify, within a dissociated tissue preparation, cells that contain magnetic material by their rotational behavior. As a tissue of choice, we selected trout olfactory epithelium that has been previously suggested to host candidate magnetoreceptor cells. We were able to reproducibly detect magnetic cells and to determine their magnetic dipole moment. The obtained values (4 to 100 fAm^2) greatly exceed previous estimates (0.5 fAm^2). The magnetism of the cells is due to a μm-sized intracellular structure of iron-rich crystals, most likely single-domain magnetite. In confocal reflectance imaging, these produce bright reflective spots close to the cell membrane. The magnetic inclusions are found to be firmly coupled to the cell membrane, enabling a direct transduction of mechanical stress produced by magnetic torque acting on the cellular dipole in situ. Our results show that the magnetically identified cells clearly meet the physical requirements for a magnetoreceptor capable of rapidly detecting small changes in the external magnetic field. This would also explain interference of ac powerline magnetic fields with magnetoreception, as reported in cattle.

Additional Information

© 2012 by the National Academy of Sciences. Edited by Dennis approved June 8, 2012 (received for review April 4, 2012). We thank Marianne Hanzlik for assistance with electron microscopy and Valera Shcherbakov, Gil Westmeyer, and David Keays for discussions. This work was supported by the Human Frontier Science Organization (HFSP Grant RGP 28/2007 to J.L.K., P.A.M., and M.W.), Deutsche Forschungsgemeinschaft (DFG Grant Wi 1828/4-1 to M.W.), and the University of Malaya and Ministry of Higher Education Malaysia (to A.M.). Author contributions: S.H.E., H.C., P.A.M, J.L.K., and M.W. designed research; S.H.E., H.C., A.M., and M.W. performed research; M.W. analyzed data; M.W. wrote SI Text; and S.H.E., H.C., J.L.K., and M.W. wrote the paper. The authors declare no conflict of interest.

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Published - PNAS-2012-Eder-12022-7.pdf

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Supplemental Material - SM02.avi

Supplemental Material - pnas.1205653109_SI.pdf

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