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Research ArticleNew Research, Sensory and Motor Systems

Transduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain

Connie X. Wang, Isaac A. Hilburn, Daw-An Wu, Yuki Mizuhara, Christopher P. Cousté, Jacob N. H. Abrahams, Sam E. Bernstein, Ayumu Matani, Shinsuke Shimojo and Joseph L. Kirschvink
eNeuro 18 March 2019, 6 (2) ENEURO.0483-18.2019; DOI: https://doi.org/10.1523/ENEURO.0483-18.2019
Connie X. Wang
1Computation and Neural Systems, California Institute of Technology, Pasadena, CA, 91125
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Isaac A. Hilburn
2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, 91125
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Daw-An Wu
1Computation and Neural Systems, California Institute of Technology, Pasadena, CA, 91125
3Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125
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Yuki Mizuhara
4Graduate School of Information Science and Technology, The University of Tokyo, Bunkyo-ku, Tokyo 113-8654, Japan
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Christopher P. Cousté
2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, 91125
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Jacob N. H. Abrahams
2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, 91125
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Sam E. Bernstein
5Department of Computer Science, Princeton University, Princeton, NJ 08544
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Ayumu Matani
4Graduate School of Information Science and Technology, The University of Tokyo, Bunkyo-ku, Tokyo 113-8654, Japan
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Shinsuke Shimojo
1Computation and Neural Systems, California Institute of Technology, Pasadena, CA, 91125
3Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, 91125
6Tohoku University Graduate School of Life Sciences, Sendai, Miyagi 980-8577, Japan
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Joseph L. Kirschvink
2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, 91125
7Earth-Life Science Institute, Tokyo Institute of Technology, Meguro, Tokyo 152-8550, Japan
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Abstract

Magnetoreception, the perception of the geomagnetic field, is a sensory modality well-established across all major groups of vertebrates and some invertebrates, but its presence in humans has been tested rarely, yielding inconclusive results. We report here a strong, specific human brain response to ecologically-relevant rotations of Earth-strength magnetic fields. Following geomagnetic stimulation, a drop in amplitude of electroencephalography (EEG) alpha-oscillations (8–13 Hz) occurred in a repeatable manner. Termed alpha-event-related desynchronization (alpha-ERD), such a response has been associated previously with sensory and cognitive processing of external stimuli including vision, auditory and somatosensory cues. Alpha-ERD in response to the geomagnetic field was triggered only by horizontal rotations when the static vertical magnetic field was directed downwards, as it is in the Northern Hemisphere; no brain responses were elicited by the same horizontal rotations when the static vertical component was directed upwards. This implicates a biological response tuned to the ecology of the local human population, rather than a generic physical effect. Biophysical tests showed that the neural response was sensitive to static components of the magnetic field. This rules out all forms of electrical induction (including artifacts from the electrodes) which are determined solely on dynamic components of the field. The neural response was also sensitive to the polarity of the magnetic field. This rules out free-radical “quantum compass” mechanisms like the cryptochrome hypothesis, which can detect only axial alignment. Ferromagnetism remains a viable biophysical mechanism for sensory transduction and provides a basis to start the behavioral exploration of human magnetoreception.

  • alpha-ERD
  • biogenic magnetite
  • biophysics
  • EEG
  • magnetoreception
  • quantum compass

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Human Frontiers Science Program Grant HFSP-RGP0054/2014 (to S.S., J.L.K. and A.M.), and more recent analysis of data was supported by the Defense Advanced Research Projects Agency (DARPA) RadioBio Program Grant D17AC00019 (to J.L.K. and S.S.) and the Japan Society for the Promotion of Science (JSPS) KAKENHI Grant 18H03500 (to A.M.). Previous support to J.L.K. from the Fetzer institute allowed construction of an earlier version of the 2-m Merritt coil system. C.X.W. and S.S. have been partly supported by the Japan Science and Technology Agency, Core Research for Evolutional Science and Technology (JST.CREST).

  • All digital data are available at https://doi.org/10.22002/d1.930 and https://doi.org/10.22002/d1.931, including MATLAB scripts used for the automatic data analysis.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Transduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain
Connie X. Wang, Isaac A. Hilburn, Daw-An Wu, Yuki Mizuhara, Christopher P. Cousté, Jacob N. H. Abrahams, Sam E. Bernstein, Ayumu Matani, Shinsuke Shimojo, Joseph L. Kirschvink
eNeuro 18 March 2019, 6 (2) ENEURO.0483-18.2019; DOI: 10.1523/ENEURO.0483-18.2019

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Transduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain
Connie X. Wang, Isaac A. Hilburn, Daw-An Wu, Yuki Mizuhara, Christopher P. Cousté, Jacob N. H. Abrahams, Sam E. Bernstein, Ayumu Matani, Shinsuke Shimojo, Joseph L. Kirschvink
eNeuro 18 March 2019, 6 (2) ENEURO.0483-18.2019; DOI: 10.1523/ENEURO.0483-18.2019
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Keywords

  • alpha-ERD
  • biogenic magnetite
  • biophysics
  • EEG
  • magnetoreception
  • quantum compass

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