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J Neurosci. 2016 Oct 19;36(42):10742-10749.

Magnetic Fields Modulate Blue-Light-Dependent Regulation of Neuronal Firing by Cryptochrome.

Author information

1
Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom.
2
Manchester Institute of Biotechnology, University of Manchester, Manchester M1 7DN, United Kingdom, and.
3
Photon Science Institute and.
4
Manchester Institute of Biotechnology, University of Manchester, Manchester M1 7DN, United Kingdom, and alex.jones-2@manchester.ac.uk richard.baines@manchester.ac.uk.
5
School of Chemistry, University of Manchester, Manchester M13 9PL, United Kingdom.
6
Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom, alex.jones-2@manchester.ac.uk richard.baines@manchester.ac.uk.

Abstract

Many animals are able to sense the Earth's geomagnetic field to enable behaviors such as migration. It is proposed that the magnitude and direction of the geomagnetic field modulates the activity of cryptochrome (CRY) by influencing photochemical radical pair intermediates within the protein. However, this proposal will remain theoretical until a CRY-dependent effect on a receptor neuron is shown to be modified by an external magnetic field (MF). It is established that blue-light (BL) photoactivation of CRY is sufficient to depolarize and activate Drosophila neurons. Here, we show that this CRY-dependent effect is significantly potentiated in the presence of an applied MF (100 mT). We use electrophysiological recordings from larval identified motoneurons, in which CRY is ectopically expressed, to show that BL-dependent depolarization of membrane potential and increased input resistance are markedly potentiated by an MF. Analysis of membrane excitability shows that these effects of MF exposure evoke increased action potential firing. Almost nothing is known about the mechanism by which a magnetically induced change in CRY activity might produce a behavioral response. We further report that specific structural changes to the protein alter the impact of the MF in ways that are strikingly similar to those from recent behavioral studies into the magnetic sense of Drosophila These observations provide the first direct experimental evidence to support the hypothesis that MF modulation of CRY activity is capable of influencing neuron activity to allow animal magnetoreception.

SIGNIFICANCE STATEMENT:

The biophysical mechanism of animal magnetoreception is still unclear. The photoreceptor protein cryptochrome has risen to prominence as a candidate magnetoreceptor molecule based on multiple reports derived from behavioral studies. However, the role of cryptochrome as a magnetoreceptor remains controversial primarily because of a lack of direct experimental evidence linking magnetic field (MF) exposure to a change in neuronal activity. Here, we show that exposure to an MF (100 mT) is sufficient to potentiate the ability of light-activated cryptochrome to increase neuronal action potential firing. Our results provide critical missing evidence to show that the activity of cryptochrome is sensitive to an external MF that is capable of modifying animal behavior.

KEYWORDS:

Drosophila; action potential; cryptochrome; depolarization; magnetic field; radical pair

PMID:
27798129
PMCID:
PMC5083005
DOI:
10.1523/JNEUROSCI.2140-16.2016
[Indexed for MEDLINE]
Free PMC Article

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