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Transduction of the Geomagnetic Field as Evidenced from Alpha-band Activity in the Human Brain

Wang, Connie X. and Hilburn, Isaac A. and Wu, Daw-An and Mizuhara, Yuki and Cousté, Christopher P. and Abrams, Jacob N. H. and Bernstein, Sam E. and Matani, Ayumu and Shimojo, Shinsuke and Kirschvink, Joseph L. (2019) Transduction of the Geomagnetic Field as Evidenced from Alpha-band Activity in the Human Brain. eNeuro . ISSN 2373-2822. (In Press) http://resolver.caltech.edu/CaltechAUTHORS:20181029-152155020

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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 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/ENEURO.0483-18.2019DOIArticle
http://www.eneuro.org/content/early/2019/03/18/ENEURO.0483-18.2019PublisherArticle
https://doi.org/10.1101/448449DOIDiscussion Paper
https://data.caltech.edu/records/930Related ItemData
https://data.caltech.edu/records/931Related ItemData
ORCID:
AuthorORCID
Wu, Daw-An0000-0003-4296-3369
Additional Information:© 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. Author contributions: C.X.W., I.A.H., D.-A.W., Y.M., C.P.C., J.N.H.A., S.E.B., A.M., S.S., and J.L.K. designed research; C.X.W., I.A.H., D.-A.W., Y.M., C.P.C., J.N.H.A., A.M., S.S., and J.L.K. performed research; C.X.W., I.A.H., D.-A.W., A.M., S.S., and J.L.K. analyzed data; C.X.W., I.A.H., D.-A.W., Y.M., C.P.C., J.N.H.A., S.E.B., A.M., S.S., and J.L.K. wrote the paper. Authors report no conflict of interest. This work was supported directly by 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 DARPA RadioBio Program grant (D17AC00019) to JLK and SS, and Japan Society for the Promotion of Science (JSPS) KAKENHI grant 18H03500 to AM. 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 JST.CREST. SS is also affiliated with Kyoto University KOKORO Center, Tohoku University Graduate School of Life Sciences, and Tamagawa University Brain Science Institute. Participants were 34 adult volunteers (24 male, 12 female) recruited from the local population which will be identified if the article is published. This participant pool included persons of European, Asian, African and Native American descent. Ages ranged from 18 to 68 years. Each participant gave written informed consent of study procedures approved by the Institutional Review Board. All experiments were performed in accordance with relevant guidelines and regulations following NIH protocols for human experimentation, as reviewed and approved periodically by the Administrative Committee for the Protection of Human Subjects (Caltech IRB, protocols 13-0420, 17-0706, and 17-0734). All methods were carried out in accordance with relevant guidelines and regulations. Informed consent using forms approved by the Institutional Review Board was obtained from all subjects. No subjects under the age of 18 were used in these experiments. All digital data are available at https://data.caltech.edu/records/930 and https://data.caltech.edu/records/931, including MatLabTM scripts used for the automatic data analysis.
Funders:
Funding AgencyGrant Number
Human Frontier Science ProgramHFSP-RGP0054/2014
Defense Advanced Research Projects Agency (DARPA)D17AC00019
Japan Society for the Promotion of Science (JSPS)18H03500
Japan Science and Technology AgencyUNSPECIFIED
Subject Keywords:alpha-ERD; Biogenic Magnetite; Biophysics; EEG; Magnetoreception; Quantum Compass
Record Number:CaltechAUTHORS:20181029-152155020
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20181029-152155020
Official Citation: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. doi: 10.1523/ENEURO.0483-18.2019
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90480
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:30 Oct 2018 01:51
Last Modified:18 Mar 2019 18:21

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