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

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.

Electrophysiological validation of premotor interneurons monosynaptically connected to the aCC motoneuron in the Drosophila larval CNS

“…We have, in this study, adopted a traditional electrophysiological approach to screen a range of interneuron driver lines that have been suggested to monosynaptically-connect with a specific motoneuron, termed the anterior corner cell (aCC). Because of its larger soma and midline-dorsal location, this cell has been the subject of numerous studies and remains a key focus of many groups (Worrell and Levine, 2008;Ryglewski et al, 2012;Srinivasan et al, 2012a, b;Giachello and Baines, 2015;Giachello et al, 2016). We confirm that aCC is monosynaptically driven by two excitatory premotor cholinergic interneurons (A27h and A18a/CLI2), in addition to two GABAergic premotor interneurons, A23a and A31k.…”

On the optimal relative orientation of radicals in the cryptochrome magnetic compass

“…by dedicated mutations. In fact, Cry has previously been used as an optogenetic tool [60] and can render the activity of a system that do not naturally contain Cry magnetically-sensitive [61]. Additionally this research could guide endeavors to experimentally observe anisotropic MFEs in cryptochromes in vitro or in chemically engineered model compounds such as that reported in [62,63].…”

One Actor, Multiple Roles: The Performances of Cryptochrome in Drosophila

“…Moreover, this strong seizure phenotype is associated with increased synaptic excitation in the locomotor circuitry, as it may be blocked by antiepileptic drugs (Marley and Baines, 2011;Lin et al, 2012). Indeed, the CRY-and lightdependent magnetic field modulates the action potential firing of individual neurons, by increasing input resistance and depolarization of the membrane potential of "anterior Corner Cell" (aCC) and "Raw Prawn 2" (RP2) motoneurons (Giachello et al, 2016).…”