The compass response simply uses the geomagnetic field as an indicator to orient the animal relative to the local magnetic north/south direction ( Wiltschko and Wiltschko, 1995a Lohmann et al., 2001).
In animals, geomagnetic navigation is thought to involve both a compass and map response ( Kramer, 1953). Animal findings provide a potential feature space for exploring human magnetoreception, the physical parameters and coordinate frames to be manipulated in human testing ( Wiltschko, 1972 Kirschvink et al., 1997). An ever-expanding list of experiments on magnetically-sensitive organisms has revealed physiologically-relevant stimuli as well as environmental factors that may interfere with magnetosensory processing ( Wiltschko and Wiltschko, 1995a Lohmann et al., 2001 Walker et al., 2002). In the meantime, there have been major advances in our understanding of animal geomagnetic sensory systems. Twenty to 30 years after these previous flurries of research, the question of human magnetoreception remains unanswered. Attempts to detect human brain responses using electroencephalography (EEG) were limited by the computational methods that were used ( Sastre et al., 2002). Behavioral results suggesting that geomagnetic fields influence human orientation during displacement experiments ( Baker, 1980, 1982, 1987) were not replicated ( Gould and Able, 1981 Able and Gergits, 1985 Westby and Partridge, 1986). Magnetoreception is a well-known sensory modality in bacteria ( Frankel and Blakemore, 1980), protozoans ( Bazylinski et al., 2000) and a variety of animals ( Wiltschko and Wiltschko, 1995a Walker et al., 2002 Johnsen and Lohmann, 2008), but whether humans have this ancient sensory system has never been conclusively established. Ferromagnetism remains a viable biophysical mechanism for sensory transduction and provides a basis to start the behavioral exploration of human magnetoreception. This rules out free-radical “quantum compass” mechanisms like the cryptochrome hypothesis, which can detect only axial alignment. The neural response was also sensitive to the polarity 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. Biophysical tests showed that the neural response was sensitive to static components of the magnetic field. This implicates a biological response tuned to the ecology of the local human population, rather than a generic physical effect. 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. 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. Following geomagnetic stimulation, a drop in amplitude of electroencephalography (EEG) alpha-oscillations (8–13 Hz) occurred in a repeatable manner. We report here a strong, specific human brain response to ecologically-relevant rotations of Earth-strength magnetic fields. 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. If the magnetoreception mechanism is based on electrical induction, the same response should occur in conditions with identical ∂B/∂t ( and ), but the response was observed only in one of these conditions: a result that contradicts the predictions of the electrical induction hypothesis. The CCW rotation of a downwards-directed field () caused a strong, repeatable alpha-ERD (lower left panel, p < 0.01 at Fz) weak alpha -power fluctuations observed in other conditions (DecDn.CW.N,, DecUp.CW.N,, and ) were not consistent across multiple runs of the same experiment. Scalp topography changes from –0.25 s pre-stimulus to +1 s post-stimulus. Bottom row shows the, DecDn.CW.N and conditions (64 trials per condition) of the DecDn.N experiment top row shows the corresponding conditions for the DecUp.N experiment.
Movie 1: Test of the electrical induction mechanism of magnetoreception using data from a participant with a strong, repeatable alpha-ERD magnetosensory response.