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.
Significance Statement Although many migrating and homing animals are sensitive to Earth’s magnetic field, most humans are not consciously aware of the geomagnetic stimuli that we encounter in everyday life. Either we have lost a shared, ancestral magnetosensory system, or the system lacks a conscious component with detectable neural activity but no apparent perceptual awareness by us. We found two classes of ecologically-relevant rotations of Earth-strength magnetic fields that produce strong, specific and repeatable effects on human brainwave activity in the EEG alpha band (8-13 Hz); EEG discriminates in response to different geomagnetic field stimuli. Biophysical tests rule out all except the presence of a ferromagnetic transduction element, such as biologically-precipitated crystals of magnetite (Fe3O4).
Footnotes
* 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.
* 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.
* 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.
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