Research Article: Blue light-dependent human magnetoreception in geomagnetic food orientation

Date Published: February 14, 2019

Publisher: Public Library of Science

Author(s): Kwon-Seok Chae, In-Taek Oh, Sang-Hyup Lee, Soo-Chan Kim, Thorsten Ritz.

http://doi.org/10.1371/journal.pone.0211826

Abstract

The Earth’s geomagnetic field (GMF) is known to influence magnetoreceptive creatures, from bacteria to mammals as a sensory cue or a physiological modulator, despite it is largely thought that humans cannot sense the GMF. Here, we show that humans sense the GMF to orient their direction toward food in a self-rotatory chair experiment. Starved men, but not women, significantly oriented toward the ambient/modulated magnetic north or east, directions which had been previously food-associated, without any other helpful cues, including sight and sound. The orientation was reproduced under blue light but was abolished under a blindfold or a longer wavelength light (> 500 nm), indicating that blue light is necessary for magnetic orientation. Importantly, inversion of the vertical component of the GMF resulted in orientation toward the magnetic south and blood glucose levels resulting from food appeared to act as a motivator for sensing a magnetic field direction. The results demonstrate that male humans sense GMF in a blue light-dependent manner and suggest that the geomagnetic orientations are mediated by an inclination compass.

Partial Text

Magnetoreceptive creatures—ranging from magnetotactic bacteria [1], to plants [2], to animals [3, 4] including certain birds, reptiles, insects, and mammals—are known to use the geomagnetic field (GMF) as a sensory cue for migration [3,4,5,6], short-distance movement [7–10], or as a physiological modulator [2], depending on the species. Evidence suggests that in magnetosensitive creatures, the GMF is sensed by either flavoprotein cryptochromes in the retina of the eyes or iron-containing biogenic magnetite in the head, which confers an inclination or polarity compass for navigation [3, 4]. Cryptochromes, in particular, need blue light (400–500 nm) when the GMF is sensed through a radical pair mechanism [11, 12], whereas light is not required for magnetite-mediated magnetoreception [3, 4]. For cryptochromes, light absorption by the prosthetic group, flavin adenine dinucleotide (FAD), triggers intramolecular electron transfer to form a spin-correlated radical pair whose spin-selective reactivity leads to magnetically sensitive reaction product yields [12]. In the process, a FAD-Trp radical pair is formed through photo-excitation of the FAD in its fully oxidized state, which has an absorption maximum of 450 nm and very weak absorption above 500 nm.

Our findings show that, as a group, starved men can sense the GMF during food consumption and use it to identify the direction in which food can be obtained, even though significant individual orientation for food was not observed in most men. Importantly, unlike previous studies on human magnetoreception, magnetic field sensing and selective orientation through the subject’s voluntary rotational direction search and hand raising behaviors in the present study demonstrated a distinct and active magnetic responsiveness. As evidence for geomagnetic orientation in starved men, the antiparallel current condition that did not generate a supposedly modulated magnetic north, failed to produce a significant orientation in the subjects, unlike that seen under the normal condition (Table 1). It is conceivable that, if the subjects could detect the GMF direction, they should have oriented toward the ambient magnetic north in not only the normal condition but also the antiparallel condition. However, the result from the antiparallel condition suggests that the potential tendency of the subjects’ orientation toward the ambient magnetic north was not strong enough to override the influence of the pre-experiment instruction given to the subjects to indicate the direction of the modulated magnetic north. Particularly, the instruction may have led the subjects to expect a substantial extent of modulated magnetic north (~3/4 of total trials) besides the ambient GMF (~1/4 of total trials), thereby biasing them mostly away from alignment with the ambient magnetic north. In addition, the subjects showed a significant orientation toward all the modulated magnetic norths, including the ambient magnetic north (0°) under the normal condition (Table 1). In fact, the magnetic fields produced by the Helmholtz coil system in the present study were not entirely homogeneous and not the same as the GMF. Therefore, the results suggest that men could sense the ambient GMF north during the association period and used this information to identify the magnetic north direction of both the ambient GMF and the relatively inhomogeneous modulated magnetic fields generated by the Helmholtz coils during the test period.

 

Source:

http://doi.org/10.1371/journal.pone.0211826

 

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