Magnetic Strategies for Nervous System Control.

Magnetic fields pass through tissue undiminished and without producing harmful effects, motivating their use as a wireless, minimally invasive means to control neural activity. Here, we review mechanisms and techniques coupling magnetic fields to changes in electrochemical potentials across neuronal membranes. Biological magnetoreception, although incompletely understood, is discussed as a potential source of inspiration. The emergence of magnetic properties in materials is reviewed to clarify the distinction between biomolecules containing transition metals and ferrite nanoparticles that exhibit significant net moments. We describe recent developments in the use of magnetic nanomaterials as transducers converting magnetic stimuli to forms readily perceived by neurons and discuss opportunities for multiplexed and bidirectional control as well as the challenges posed by delivery to the brain. The variety of magnetic field conditions and mechanisms by which they can be coupled to neuronal signaling cascades highlights the desirability of continued interchange between magnetism physics and neurobiology.

Upper bound for broadband radiofrequency field disruption of magnetic compass orientation in night-migratory songbirds.

Night-migratory songbirds have a light-dependent magnetic compass sense, the mechanism of which is thought to depend on the photochemical formation of radical pairs in cryptochrome (Cry) proteins located in the retina. The finding that weak radiofrequency (RF) electromagnetic fields can prevent birds from orienting in the Earth's magnetic field has been regarded as a diagnostic test for this mechanism and as a potential source of information on the identities of the radicals. The maximum frequency that could cause such disorientation has been predicted to lie between 120 and 220 MHz for a flavin-tryptophan radical pair in Cry. Here we show that the magnetic orientation capabilities of Eurasian blackcaps (Sylvia atricapilla) are not affected by RF noise in the frequency bands 140 to 150 MHz and 235 to 245 MHz. From a consideration of its internal magnetic interactions, we argue that RF field effects on a flavin-containing radical-pair sensor should be approximately independent of frequency up to 116 MHz and that birds' sensitivity to RF disorientation should fall by about two orders of magnitude when the frequency exceeds 116 MHz. Taken together with our earlier finding that 75 to 85 MHz RF fields disrupt the magnetic orientation of blackcaps, these results provide compelling evidence that the magnetic compass of migratory birds operates by a radical pair mechanism.

Identifying Cellular and Molecular Mechanisms for Magnetosensation.

Diverse animals ranging from worms and insects to birds and turtles perform impressive journeys using the magnetic field of the earth as a cue. Although major cellular and molecular mechanisms for sensing mechanical and chemical cues have been elucidated over the past three decades, the mechanisms that animals use to sense magnetic fields remain largely mysterious. Here we survey progress on the search for magnetosensory neurons and magnetosensitive molecules important for animal behaviors. Emphasis is placed on magnetosensation in insects and birds, as well as on the magnetosensitive neuron pair AFD in the nematode Caenorhabditis elegans. We also review conventional criteria used to define animal magnetoreceptors and suggest how approaches used to identify receptors for other sensory modalities may be adapted for magnetoreceptors. Finally, we discuss prospects for underutilized and novel approaches to identify the elusive magnetoreceptors in animals.

Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing.

Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.

Possibility of two-dimensional ordering of cryptochrome 4a from European robin.

Cryptochrome (Cry) in some species could act as a quantum senser to detect the inclination angle of geomagnetic field, the function of which attributes the magnetic sensitivity of spins of unpaired electrons in radical pair (RP) in CRY generated by blue light irradiation. However, the effect of blue light on the structure and molecular behavior of Cry has not been well investigated. We conducted the size exclusion chromatography (SEC) and small-angle X-ray scattering (SAXS) analyses to inspect the molecular structure and behavior of cryptochrome 4a (ErCry4a) from European robin, a representative magnetosensory animal. The results indicated that ErCry4a could form flat-shape oligomers. Moreover, blue light irradiation induced the contraction of the ErCry4a molecule at the monomer scale and simultaneously accelerated the two-dimensional oligomerization of ErCry4a. This oligomerization may enhance the regularity of the two-dimensional arrangement of ErCry4a molecules, providing a positive effect for detecting the inclination angle.

Adaptive evolution and loss of a putative magnetoreceptor in passerines.

Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, and Cry4a from a migratory songbird seems to show enhanced magnetic sensitivity in vitro compared to Cry4a from resident species. We investigate Cry and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modelling. Our analysis is based on 363 bird genomes and identifies different selection regimes in passerines. We show that Cry4a is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that are likely to have facilitated the evolution of an optimized sensory protein for night-time orientation in songbirds. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines), and thus identified a gene deletion, which might facilitate testing the function of Cry4a in birds. In contrast, the other avian Cry (Cry1 and Cry2) were highly conserved across all species, indicating basal, non-sensory functions. Our results support a specialization or functional differentiation of Cry4 in songbirds which could be magnetosensation.

The Effect of Spin Relaxation on Magnetic Compass Sensitivity in ErCry4a.

This study explores the impact of thermal motion on the magnetic compass mechanism in migratory birds, focusing on the radical pair mechanism within cryptochrome photoreceptors. The coherence of radical pairs, crucial for magnetic field inference, is curbed by spin relaxation induced by intra-protein motion. Molecular dynamics simulations, density-functional-theory-based calculations, and spin dynamics calculations were employed, utilizing Bloch-Redfield-Wangsness (BRW) relaxation theory, to investigate compass sensitivity. Previous research hypothesized that European robin's cryptochrome 4a (ErCry4a) optimized intra-protein motion to minimize spin relaxation, enhancing magnetic sensing compared to the plant Arabidopsis thaliana's cryptochrome 1 (AtCry1). Different correlation times of the nuclear hyperfine coupling constants in AtCry1 and ErCry4a were indeed found, leading to distinct radical pair yields in the two species, with ErCry4a showing optimized sensitivity. However, this optimization is likely negligible in realistic spin systems with numerous nuclear spins. Beyond insights in magnetic sensing, the study presents a detailed method employing molecular dynamics simulations to assess spin relaxation effects on chemical reactions with realistically modelled protein motion, relevant for studying radical pair reactions at finite temperature.

European common frogs determine migratory direction by inclination magnetic compass and show diurnal variation in orientation.

Animals can use two variants of the magnetic compass: the 'polar compass' or the 'inclination compass'. Among vertebrates, the compass type has been identified for salmon, mole rats, birds, turtles and urodeles. However, no experiments have been conducted to determine the compass variant in anurans. To elucidate this, we performed a series of field and laboratory experiments on males of the European common frog during the spawning season. In field experiments in a large circular arena, we identified the direction of the stereotypic migration axis for a total of 581 frogs caught during migration from river to pond or in a breeding pond. We also found that motivation of the frogs varied throughout the day, probably to avoid deadly night freezes, which are common in spring. The laboratory experiments were conducted on a total of 450 frogs in a T-maze placed in a three-axis Merritt coil system. The maze arms were positioned parallel to the natural migration axis inferred on the basis of magnetic field. Both vertical and horizontal components of the magnetic field were altered, and frogs were additionally tested in a vertical magnetic field. We conclude that European common frogs possess an inclination magnetic compass, as for newts, birds and sea turtles, and potentially use it during the spring migration. The vertical magnetic field confuses the frogs, apparently as a result of the inability to choose a direction. Notably, diurnal variation in motivation of the frogs was identical to that in nature, indicating the presence of internal rhythms controlling this process.

Swimming polarity inversion in uncultured magnetotactic cocci.

Magnetotactic bacteria are microorganisms that produce intracellular magnetic nanoparticles organized in chains, conferring a magnetic moment to the bacterial body that allows it to swim following the geomagnetic field lines. Magnetotactic bacteria usually display two swimming polarities in environmental samples: the South-seeking (SS) polarity and the North-seeking (NS) polarity, characterized by the bacteria swimming antiparallel or parallel to the magnetic field lines, respectively. It has been observed that in the presence of inhomogeneous magnetic fields, NS magnetotactic bacteria can change their swimming polarity to SS or vice versa. The present study analyzes populations of NS cocci obtained from SS cocci isolated in the presence of a magnet. The aim was to study differences in the swimming characteristics and magnetic moment among both populations of cocci. For that, trajectories were recorded and the velocity and angle among the velocity and the applied magnetic field were calculated. In addition, micrographs from both SS and NS cocci were obtained and their magnetosomes were measured to analyze their length, width, aspect ratio and magnetic moment, to finally obtain the magnetic moment for each coccus. The results showed the following properties of NS relative to SS cocci: higher velocities, narrow bacterial magnetic moment distribution, higher dispersion in the distribution of angles among the velocity and the applied magnetic field and lower magnetic field sensibility. Those differences cannot be explained by the simple change in magnetic polarity of the magnetosome chain and can be related to the existence of an active magnetoreceptive process in magnetotactic bacteria.

Quantum magnetic imaging of iron organelles within the pigeon cochlea.

The ability of pigeons to sense geomagnetic fields has been conclusively established despite a notable lack of determination of the underlying biophysical mechanisms. Quasi-spherical iron organelles previously termed "cuticulosomes" in the cochlea of pigeons have potential relevance to magnetoreception due to their location and iron composition; however, data regarding the magnetic susceptibility of these structures are currently limited. Here quantum magnetic imaging techniques are applied to characterize the magnetic properties of individual iron cuticulosomes in situ. The stray magnetic fields emanating from cuticulosomes are mapped and compared to a detailed analytical model to provide an estimate of the magnetic susceptibility of the individual particles. The images reveal the presence of superparamagnetic and ferrimagnetic domains within individual cuticulosomes and magnetic susceptibilities within the range 0.029 to 0.22. These results provide insights into the elusive physiological roles of cuticulosomes. The susceptibilities measured are not consistent with a torque-based model of magnetoreception, placing iron storage and stereocilia stabilization as the two leading putative cuticulosome functions. This work establishes quantum magnetic imaging as an important tool to complement the existing array of techniques used to screen for potential magnetic particle-based magnetoreceptor candidates.

Using electric fields to control insects: current applications and future directions.

Chemical-based interventions are mostly used to control insects that are harmful to human health and agriculture or that simply cause a nuisance. An overreliance on these insecticides however raises concerns for the environment, human health, and the development of resistance, not only in the target species. As such, there is a critical need for the development of novel nonchemical technologies to control insects. Electrocution traps using UV light as an attractant are one classical nonchemical approach to insect control but lack the specificity necessary to target only pest insects and to avoid harmless or beneficial species. Here we review the fundamental physics behind electric fields (EFs) and place them in context with electromagnetic fields more broadly. We then focus on how novel uses of strong EFs, some of which are being piloted in the field and laboratory, have the potential to repel, capture, or kill (electrocute) insects without the negative side effects of other classical approaches. As EF-insect science remains in its infancy, we provide recommendations for future areas of research in EF-insect science.

Magnetite in the abdomen and antennae of Apis mellifera honeybees.

The detection of magnetic fields by animals is known as magnetoreception. The ferromagnetic hypothesis explains magnetoreception assuming that magnetic nanoparticles are used as magnetic field transducers. Magnetite nanoparticles in the abdomen of Apis mellifera honeybees have been proposed in the literature as the magnetic field transducer. However, studies with ants and stingless bees have shown that the whole body of the insect contain magnetic material, and that the largest magnetization is in the antennae. The aim of the present study is to investigate the magnetization of all the body parts of honeybees as has been done with ants and stingless bees. To do that, the head without antennae, antennae, thorax, and abdomen obtained from Apis mellifera honeybees were analyzed using magnetometry and Ferromagnetic Resonance (FMR) techniques. The magnetometry and FMR measurements show the presence of magnetic material in all honeybee body parts. Our results present evidence of the presence of biomineralized magnetite nanoparticles in the honeybee abdomen and, for the first time, magnetite in the antennae. FMR measurements permit to identify the magnetite in the abdomen as biomineralized. As behavioral experiments reported in the literature have shown that the abdomen is involved in magnetoreception, new experimental approaches must be done to confirm or discard the involvement of the antennae in magnetoreception.

Migratory birds are able to choose the appropriate migratory direction under dim yellow narrowband light.

Currently, it is generally assumed that migratory birds are oriented in the appropriate migratory direction under UV, blue and green light (short-wavelength) and are unable to use their magnetic compass in total darkness and under yellow and red light (long-wavelength). However, it has also been suggested that the magnetic compass has two sensitivity peaks: in the short and long wavelengths, but with different intensities. In this project, we aimed to study the orientation of long-distance migrants, pied flycatchers (Ficedula hypoleuca), under different narrowband light conditions during autumn and spring migrations. The birds were tested in the natural magnetic field (NMF) and a changed magnetic field (CMF) rotated counterclockwise by 120° under dim green (autumn) and yellow (spring and autumn) light, which are on the 'threshold' between the short-wavelength and long-wavelength light. We showed that pied flycatchers (i) were completely disoriented under green light both in the NMF and CMF but (ii) showed the migratory direction in the NMF and the appropriate response to CMF under yellow light. Our data contradict the results of previous experiments under narrowband green and yellow light and raise doubts about the existence of only short-wavelength magnetoreception. The parameters of natural light change dramatically in spectral composition and intensity after local sunset, and the avian magnetic compass should be adapted to function properly under such constantly changing light conditions.

The Presidential Symposium at the International Congress of Neuroethology 2022 in Lisbon, Portugal.

In this special issue of articles from leading neuroethologists-all of whom gave outstanding presentations within the Presidential Symposium of the 2022 International Congress of Neuroethology held in Lisbon, Portugal-we learn about the role of cryptochrome molecules in the magnetic sense of animals, how honeybees construct their honeycombs, why fish eyes are built the way they are in species from different depths, how archerfish intercept their newly downed prey with a swift muscular curving of the body (known as a C-start) and how birds process optic flow information to control flight. Each contribution showcases how nervous systems have evolved to control behaviour, the raison d'être of neuroethology.

Insect magnetoreception: a Cry for mechanistic insights.

Migratory animals can detect and use the Earth's magnetic field for orientation and navigation, sometimes over distances spanning thousands of kilometers. How they do so remains, however, one of the greatest mysteries in all sensory biology. Here, the author reviews the progress made to understand the molecular bases of the animal magnetic sense focusing on insect species, the only species in which genetic studies have so far been possible. The central hypothesis in the field posits that magnetically sensitive radical pairs formed by photoexcitation of cryptochrome proteins are key to animal magnetoreception. The author provides an overview of our current state of knowledge for the involvement of insect light-sensitive type I and light-insensitive type II cryptochromes in this enigmatic sense, and highlights some of the unanswered questions to gain a comprehensive understanding of magnetoreception at the organismal level.

Migratory bats are sensitive to magnetic inclination changes during the compass calibration period.

The Earth's magnetic field is used as a navigational cue by many animals. For mammals, however, there are few data to show that navigation ability relies on sensing the natural magnetic field. In night-time migrating bats, experiments demonstrating a role for the solar azimuth at sunset in the calibration of the orientation system suggest that the magnetic field is a candidate for their compass. Here, we investigated how an altered magnetic field at sunset changes the nocturnal orientation of the bat Pipistrellus pygmaeus. We exposed bats to either the natural magnetic field, a horizontally shifted field (120°), or the same shifted field combined with a reversal of the natural value of inclination (70° to -70°). We later released the bats and found that the take-off orientation differed among all treatments. Bats that were exposed to the 120° shift were unimodally oriented northwards in contrast to controls which exhibited a bimodal north-south distribution. Surprisingly, the orientation of bats exposed to both a 120° shift and reverse inclination was indistinguishable from a uniform distribution. These results suggest that these migratory bats calibrate the magnetic field at sunset, and for the first time, they show that bats are sensitive to the angle of magnetic inclination.

Magnetic nanoparticles in the body parts of Polistes versicolor and Polybia paulista wasps are biomineralized: evidence from magnetization measurements and ferromagnetic resonance spectroscopy.

The detection of the geomagnetic field by animals to use as a cue in homing and migration is known as magnetoreception. The ferromagnetic hypothesis explains magnetoreception assuming that magnetic nanoparticles in cellular structures are used as magnetic field transducers. Considering magnetoreception in social insects, the most studied has been the honeybee Apis mellifera and only in two wasp species (Vespa orientalis and Polybia paulista) have been shown a magnetosensitive behavior. In the present report the body parts (abdomen, head and antennae) of Polistes versicolor and Polybia paulista wasps were studied aiming to find biomineralized magnetic nanoparticles, using magnetometry measurements and ferromagnetic resonance spectroscopy. The magnetometry measurements show the presence of magnetic nanoparticles in all body parts, being characterized as mixtures of superparamagnetic, single domain and pseudo-single domain nanoparticles. From the ferromagnetic resonance spectra were obtained the asymmetry ratio A and the effective g factor geff, and those parameters are consistent with the presence of biomineralized magnetic nanoparticles in both wasps. In the case of Polybia paulista, the magnetic nanoparticles can be associated with some sort of magnetosensor once this wasp is magnetosensitive. For Polistes versicolor, the results indicate that this wasp can be magnetosensitive as Polybia paulista once their magnetic nanoparticles are biomineralized in the body. Behavioral studies with Polistes versicolor wasps deserve to be performed.

Behavioral evidence for geomagnetic imprinting and transgenerational inheritance in fruit flies.

Certain long-distance migratory animals, such as salmon and sea turtles, are thought to imprint on the magnetic field of their natal area and to use this information to help them return as adults. Despite a growing body of indirect support for such imprinting, direct experimental evidence thereof remains elusive. Here, using the fruit fly as a magnetoreceptive model organism, we demonstrate that exposure to a specific geographic magnetic field during a critical period of early development affected responses to a matching magnetic field gradient later in life. Specifically, hungry flies that had imprinted on a specific magnetic field from 1 of 3 widely separated geographic locations responded to the imprinted field, but not other magnetic fields, by moving downward, a geotactic behavior associated with foraging. This same behavior occurred spontaneously in the progeny of the next generation: female progeny moved downward in response to the field on which their parents had imprinted, whereas male progeny did so only in the presence of these females. These results represent experimental evidence that organisms can learn and remember a magnetic field to which they were exposed during a critical period of development. Although the function of the behavior is not known, one possibility is that imprinting on the magnetic field of a natal area assists flies and their offspring in recognizing locations likely to be favorable for foraging and reproduction.

Spin Dynamics of Flavoproteins.

This short review reports the surprising phenomenon of nuclear hyperpolarization occurring in chemical reactions, which is called CIDNP (chemically induced dynamic nuclear polarization) or photo-CIDNP if the chemical reaction is light-driven. The phenomenon occurs in both liquid and solid-state, and electron transfer systems, often carrying flavins as electron acceptors, are involved. Here, we explain the physical and chemical properties of flavins, their occurrence in spin-correlated radical pairs (SCRP) and the possible involvement of flavin-carrying SCRPs in animal magneto-reception at earth's magnetic field.

The Geomagnetic Field (GMF) Is Required for Lima Bean Photosynthesis and Reactive Oxygen Species Production.

Plants evolved in the presence of the Earth's magnetic field (or geomagnetic field, GMF). Variations in MF intensity and inclination are perceived by plants as an abiotic stress condition with responses at the genomic and metabolic level, with changes in growth and developmental processes. The reduction of GMF to near null magnetic field (NNMF) values by the use of a triaxial Helmholtz coils system was used to evaluate the requirement of the GMF for Lima bean (Phaseolus lunatus L.) photosynthesis and reactive oxygen species (ROS) production. The leaf area, stomatal density, chloroplast ultrastructure and some biochemical parameters including leaf carbohydrate, total carbon, protein content and δ13C were affected by NNMF conditions, as were the chlorophyll and carotenoid levels. RubisCO activity and content were also reduced in NNMF. The GMF was required for the reaction center's efficiency and for the reduction of quinones. NNMF conditions downregulated the expression of the MagR homologs PlIScA2 and PlcpIScA, implying a connection between magnetoreception and photosynthetic efficiency. Finally, we showed that the GMF induced a higher expression of genes involved in ROS production, with increased contents of both H2O2 and other peroxides. Our results show that, in Lima bean, the GMF is required for photosynthesis and that PlIScA2 and PlcpIScA may play a role in the modulation of MF-dependent responses of photosynthesis and plant oxidative stress.