Transduction of the Geomagnetic Field as Evidenced from Alpha-band Activity in the Human Brain
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 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.
© 2019 Wang et al. 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. Received: 6 December 2018; Revised: 15 February 2019; Accepted: 26 February 2019; Published: 18 March 2019. We thank Dragos Harabor, James Martin, Kristján Jónsson, Mara Green, and Sarah Crucilla for work on earlier versions of this project and other members of the Kirschvink, Shimojo, and Matani labs for discussions and suggestions. We also thank James Randi, co-founder of the Committee for the Scientific Investigation of Claims of the Paranormal (CSICOP), for advice on minimizing potential artifacts in the experimental design. Dr. Heinrich Mouritsen of the University of Oldenberg gave valuable advice for construction of the Faraday cage and input on an earlier draft of this manuscript. S.S. is also affiliated with Kyoto University KOKORO Center and Tamagawa University Brain Science Institute. 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.
Published - ENEURO.0483-18.2019.full.pdf
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