Magnetic Compass Orientation Research Articles

Magnetoreception of Directional Information in Birds Requires Nondegraded Vision

The magnetic compass orientation of birds is light dependent. The respective directional information, originating in radical pair processes, is mediated by the right eye. These findings suggest possible interactions between magnetoreception and vision, in particular with the perception of contours, because the right eye has been found to be dominant in discrimination tasks requiring object vision. Here we report tests in the local geomagnetic field with European robins wearing goggles equipped with a clear and a frosted foil of equal translucence of 70%. Robins with a clear foil on the right eye and a frosted foil on the left eye oriented in the migratory direction as well as birds using both eyes. Birds with a frosted foil that blurred vision on the right eye and a clear foil on the left eye, in contrast, were disoriented. These findings are the first to show that avian magnetoreception requires, in addition to light, a nondegraded image formation along the projectional streams of the right retina. This suggests crucial interactions between the processing of visual pattern information and the conversion of magnetic input into directional information.

Changing and shielded magnetic fields suppress c-Fos expression in the navigation circuit: input from the magnetosensory system contributes to the internal representation of space in a subterranean rodent

The neural substrate subserving magnetoreception and magnetic orientation in mammals is largely unknown. Previous experiments have demonstrated that the processing of magnetic sensory information takes place in the superior colliculus. Here, the effects of magnetic field conditions on neuronal activity in the rodent navigation circuit were assessed by quantifying c-Fos expression. Ansell's mole-rats (Fukomys anselli), a mammalian model to study the mechanisms of magnetic compass orientation, were subjected to natural, periodically changing, and shielded magnetic fields while exploring an unfamiliar circular arena. In the undisturbed local geomagnetic field, the exploration of the novel environment and/or nesting behaviour induced c-Fos expression throughout the head direction system and the entorhinal-hippocampal spatial representation system. This induction was significantly suppressed by exposure to periodically changing and/or shielded magnetic fields; discrete decreases in c-Fos were seen in the dorsal tegmental nucleus, the anterodorsal and the laterodorsal thalamic nuclei, the postsubiculum, the retrosplenial and entorhinal cortices, and the hippocampus. Moreover, in inactive animals, magnetic field intensity manipulation suppressed c-Fos expression in the CA1 and CA3 fields of the hippocampus and the dorsal subiculum, but induced expression in the polymorph layer of the dentate gyrus. These findings suggest that key constituents of the rodent navigation circuit contain populations of neurons responsive to magnetic stimuli. Thus, magnetic information may be integrated with multimodal sensory and motor information into a common spatial representation of allocentric space within this circuit.

Light-dependent magnetic compass orientation in amphibians and insects: candidate receptors and candidate molecular mechanisms

Magnetic compass orientation by amphibians, and some insects, is mediated by a light-dependent magnetoreception mechanism. Cryptochrome photopigments, best known for their role in circadian rhythms, are proposed to mediate such responses. In this paper, we explore light-dependent properties of magnetic sensing at three levels: (i) behavioural (wavelength-dependent effects of light on magnetic compass orientation), (ii) physiological (photoreceptors/photopigment systems with properties suggesting a role in magnetoreception), and (iii) molecular (cryptochrome-based and non-cryptochrome-based signalling pathways that are compatible with behavioural responses). Our goal is to identify photoreceptors and signalling pathways that are likely to play a specialized role in magnetoreception in order to definitively answer the question of whether the effects of light on magnetic compass orientation are mediated by a light-dependent magnetoreception mechanism, or instead are due to input from a non-light-dependent (e.g. magnetite-based) magnetoreception mechanism that secondarily interacts with other light-dependent processes.

Lateralization of magnetic compass orientation in pigeons

The aim of our study was to test for lateralization of magnetic compass orientation in pigeons. Having shown that pigeons are capable of learning magnetic compass directions in an operant task, we wanted to know whether the brain hemispheres contribute differently and how the lateralization pattern relates to findings in other avian species. Birds that had learnt to locate food in an operant chamber by means of magnetic directions were tested for lateralization of magnetic compass orientation by temporarily covering one eye. Successful orientation occurred under all conditions of viewing. Thus, pigeons can perceive and process magnetic compass directions with the right eye and left brain hemisphere as well as the left eye and right brain hemisphere. However, while the right brain hemisphere tended to confuse the learned direction with its opposite (axial response), the left brain hemisphere specifically preferred the correct direction. Our findings demonstrate bilateral processing of magnetic information, but also suggest qualitative differences in how the left and the right brain deal with magnetic cues.

Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes

Several studies have suggested that the magnetic compass of birds is located only in the right eye. However, here we show that night-migrating garden warblers (Sylvia borin) are able to perform magnetic compass orientation with both eyes open, with only the left eye open and with only the right eye open. We did not observe any clear lateralization of magnetic compass orientation behaviour in this migratory songbird, and, therefore, it seems that the suggested all-or-none lateralization of magnetic compass orientation towards the right eye only cannot be generalized to all birds, and that the answer to the question of whether magnetic compass orientation in birds is lateralized is probably not as simple as suggested previously.

Visual but not trigeminal mediation of magnetic compass information in a migratory bird

Magnetic compass information has a key role in bird orientation, but the physiological mechanisms enabling birds to sense the Earth's magnetic field remain one of the unresolved mysteries in biology. Two biophysical mechanisms have become established as the most promising magnetodetection candidates. The iron-mineral-based hypothesis suggests that magnetic information is detected by magnetoreceptors in the upper beak and transmitted through the ophthalmic branch of the trigeminal nerve to the brain. The light-dependent hypothesis suggests that magnetic field direction is sensed by radical pair-forming photopigments in the eyes and that this visual signal is processed in cluster N, a specialized, night-time active, light-processing forebrain region. Here we report that European robins with bilateral lesions of cluster N are unable to show oriented magnetic-compass-guided behaviour but are able to perform sun compass and star compass orientation behaviour. In contrast, bilateral section of the ophthalmic branch of the trigeminal nerve in European robins did not influence the birds' ability to use their magnetic compass for orientation. These data show that cluster N is required for magnetic compass orientation in this species and indicate that it may be specifically involved in processing of magnetic compass information. Furthermore, the data strongly suggest that a vision-mediated mechanism underlies the magnetic compass in this migratory songbird, and that the putative iron-mineral-based receptors in the upper beak connected to the brain by the trigeminal nerve are neither necessary nor sufficient for magnetic compass orientation in European robins.

Cryptochrome Mediates Light-Dependent Magnetosensitivity of Drosophila's Circadian Clock

Since 1960, magnetic fields have been discussed as Zeitgebers for circadian clocks, but the mechanism by which clocks perceive and process magnetic information has remained unknown. Recently, the radical-pair model involving light-activated photoreceptors as magnetic field sensors has gained considerable support, and the blue-light photoreceptor cryptochrome (CRY) has been proposed as a suitable molecule to mediate such magnetosensitivity. Since CRY is expressed in the circadian clock neurons and acts as a critical photoreceptor of Drosophila's clock, we aimed to test the role of CRY in magnetosensitivity of the circadian clock. In response to light, CRY causes slowing of the clock, ultimately leading to arrhythmic behavior. We expected that in the presence of applied magnetic fields, the impact of CRY on clock rhythmicity should be altered. Furthermore, according to the radical-pair hypothesis this response should be dependent on wavelength and on the field strength applied. We tested the effect of applied static magnetic fields on the circadian clock and found that flies exposed to these fields indeed showed enhanced slowing of clock rhythms. This effect was maximal at 300 μT, and reduced at both higher and lower field strengths. Clock response to magnetic fields was present in blue light, but absent under red-light illumination, which does not activate CRY. Furthermore, cryb and cryOUT mutants did not show any response, and flies overexpressing CRY in the clock neurons exhibited an enhanced response to the field. We conclude that Drosophila's circadian clock is sensitive to magnetic fields and that this sensitivity depends on light activation of CRY and on the applied field strength, consistent with the radical pair mechanism. CRY is widespread throughout biological systems and has been suggested as receptor for magnetic compass orientation in migratory birds. The present data establish the circadian clock of Drosophila as a model system for CRY-dependent magnetic sensitivity. Furthermore, given that CRY occurs in multiple tissues of Drosophila, including those potentially implicated in fly orientation, future studies may yield insights that could be applicable to the magnetic compass of migratory birds and even to potential magnetic field effects in humans.

The puzzle of magnetic resonance effect on the magnetic compass of migratory birds

Experiments on the effect of radio-frequency (RF) magnetic fields on the magnetic compass orientation of migratory birds are analyzed using the theory of magnetic resonance. The results of these experiments were earlier interpreted within the radical-pair model of magnetoreception. However, the consistent analysis shows that the amplitudes of the RF fields used are far too small to noticeably influence electron spins in organic radicals. Other possible agents that could mediate the birds' response to the RF fields are discussed, but apparently no known physical system can be responsible for this effect.

Effect of light wavelength spectrum on magnetic compass orientation in Tenebrio molitor

In many animal species, geomagnetic compass sensitivity has been demonstrated to depend on spectral composition of light to which moving animals are exposed. Besides a loss of magnetic orientation, cases of a shift in the compass direction by 90 degrees following a change in the colour of light have also been described. This hitherto unclear phenomenon can be explained either as a change in motivation or as a side effect of a light-dependent reception mechanism. Among the invertebrates, the 90 degrees shift has only been described in Drosophila. In this paper, another evidence of the phenomenon is reported. Learned compass orientation in the Tenebrio molitor was tested. If animals were trained to remember the magnetic position of a source of shortwave UV light and then tested in a circular arena in diffuse light of the same wavelength, they oriented according to the learned magnetic direction. If, however, they were tested in blue-green light after UV light training, their magnetic orientation shifted by 90 degrees CW. This result is being discussed as one of a few cases of 90 degrees shift reported to date, and as an argument corroborating the hypothesis of a close connection between photoreception and magnetoreception in insects.

Orientation of Birds in Total Darkness

Magnetic compass orientation of migratory birds is known to be light dependent, and radical-pair processes have been identified as the underlying mechanism. Here we report for the first time results of tests with European robins, Erithacus rubecula, in total darkness and, as a control, under 565 nm green light. Under green light, the robins oriented in their normal migratory direction, with southerly headings in autumn and northerly headings in spring. By contrast, in darkness they significantly preferred westerly directions in spring as well as autumn. This failure to show the normal seasonal change characterizes the orientation in total darkness as a "fixed direction" response. Tests in magnetic fields with the vertical or the horizontal component inverted showed that the preferred direction depended on the magnetic field but did not involve the avian inclination compass. A high-frequency field of 1.315 MHz did not affect the behavior, whereas local anesthesia of the upper beak resulted in disorientation. The behavior in darkness is thus fundamentally different from normal compass orientation and relies on another source of magnetic information: It does not involve the radical-pair mechanism but rather originates in the iron-containing receptors in the upper beak.

Magnetic compass orientation by larval Drosophila melanogaster

We report evidence for magnetic compass orientation by larval Drosophila melanogaster. Groups of larvae were exposed from the time of hatching to directional ultraviolet (365 nm) light emanating from one of four magnetic directions. Larvae were then tested individually on a circular agar plate under diffuse light in one of four magnetic field alignments. The larvae exhibited magnetic compass orientation in a direction opposite that of the light source in training. Evidence for a well-developed magnetic compass in a larval insect that moves over distances of at most a few tens of centimeters has important implications for understanding the adaptive significance of orientation mechanisms like the magnetic compass. Moreover, the development of an assay for studying magnetic compass orientation in larval D. melanogaster will make it possible to use a wide range of molecular genetic techniques to investigate the neurophysiological, biophysical, and molecular mechanisms underlying the magnetic compass.

Green Light for Nocturnally Migrating Birds

Poot, H., B. J. Ens, H. de Vries, M. A. H. Donners, M. R. Wernand, and J. M. Marquenie. 2008. Green light for nocturnally migrating birds. Ecology and Society 13(2): 47. https://doi.org/10.5751/ES-02720-130247

Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs.

Cryptochromes (Cry) have been suggested to form the basis of light-dependent magnetic compass orientation in birds. However, to function as magnetic compass sensors, the cryptochromes of migratory birds must possess a number of key biophysical characteristics. Most importantly, absorption of blue light must produce radical pairs with lifetimes longer than about a microsecond. Cryptochrome 1a (gwCry1a) and the photolyase-homology-region of Cry1 (gwCry1-PHR) from the migratory garden warbler were recombinantly expressed and purified from a baculovirus/Sf9 cell expression system. Transient absorption measurements show that these flavoproteins are indeed excited by light in the blue spectral range leading to the formation of radicals with millisecond lifetimes. These biophysical characteristics suggest that gwCry1a is ideally suited as a primary light-mediated, radical-pair-based magnetic compass receptor.

A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds

The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, “Cluster N”, show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds “see” the reference compass direction provided by the geomagnetic field.

Lateralized response of chicks to magnetic cues

Previous research has shown that the ability to orient with the use of directional cues from the geomagnetic field is lateralized in three avian species: orientation is possible when the birds are restricted to use of their right eye, but not when they have to use their left eye. This has been interpreted as possible lateralization of the perception mechanisms for magnetic cues in favour of the right eye. Recent discovery of magnetic compass orientation in domestic chicks, a species in which lateralization has been well studied, has made available a model system in which to explore these lateralized processes more fully. Hence we tested chicks monocularly in the same test conditions as used previously to demonstrate the chick's use of a magnetic compass. In a magnetic field with North shifted by 90°, chicks using their right eye oriented according to magnetic cues, whereas chicks using the left eye did not, but continued to prefer the original direction. Analysis of the times taken to respond indicated longer latencies in the chicks using their left eye, suggesting a possible conflict between cues. The different behaviour of the chicks using their left eye might not be a matter of a right eye-left hemisphere specialization for detecting magnetic directions, but of hemispheric specialization for attending to specific types of cues.

Magnetic Compass Orientation in Larval Iberian Green Frogs, Pelophylax Perezi

AbstractExperiments were carried out to investigate whether Iberian green frog tadpoles Pelophylax perezi (formerly Rana perezi) are able of using the geomagnetic field for y‐axis orientation (i.e. orientation toward and away from shore). Tadpoles were trained outdoor for 5 d, in two different training configurations: (i) a training tank aligned along the magnetic north–south axis, with shore facing south, and (ii) a training tank aligned along the magnetic east–west axis, with shore located east, and similar to the shore–deep water axis (‘y‐axis’) found in their home stream, which flows from south to north. After training, tadpoles were individually tested for magnetic orientation in a water‐filled circular outdoor arena surrounded by a pair of orthogonally aligned cube‐surface‐coils used to alter the alignment of the earth's magnetic field. Tadpoles held in the east–west training tank oriented towards shore, indicating that they were able to distinguish between the shoreward and waterward direction along the y‐axis. Tadpoles trained in the tank that was aligned along the north–south axis showed bimodal magnetic compass orientation along the shore–deep water magnetic axis. These findings provide evidence for the use of magnetic compass cues for y‐axis orientation by P. perezi tadpoles.

Lateralized activation of Cluster N in the brains of migratory songbirds

Cluster N is a cluster of forebrain regions found in night-migratory songbirds that shows high activation of activity-dependent gene expression during night-time vision. We have suggested that Cluster N may function as a specialized night-vision area in night-migratory birds and that it may be involved in processing light-mediated magnetic compass information. Here, we investigated these ideas. We found a significant lateralized dominance of Cluster N activation in the right hemisphere of European robins (Erithacus rubecula). Activation predominantly originated from the contralateral (left) eye. Garden warblers (Sylvia borin) tested under different magnetic field conditions and under monochromatic red light did not show significant differences in Cluster N activation. In the fairly sedentary Sardinian warbler (Sylvia melanocephala), which belongs to the same phyolgenetic clade, Cluster N showed prominent activation levels, similar to that observed in garden warblers and European robins. Thus, it seems that Cluster N activation occurs at night in all species within predominantly migratory groups of birds, probably because such birds have the capability of switching between migratory and sedentary life styles. The activation studies suggest that although Cluster N is lateralized, as is the dependence on magnetic compass orientation, either Cluster N is not involved in magnetic processing or the magnetic modulations of the primary visual signal, forming the basis for the currently supported light-dependent magnetic compass mechanism, are relatively small such that activity-dependent gene expression changes are not sensitive enough to pick them up.

Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal

The mechanism of signal transduction during magnetic compass orientation is rarely evident in vertebrates and is as yet unknown in mammals. This transmission has been associated with magnetite-based receptors innervated by the ophthalmic nerve or with the involvement of the eye, particularly the retina. We provide the first behavioural support for the cornea carrying the respective primary sensors in mole-rats (Fukomys anselli) by showing that local anaesthesia disrupts their normal directional magnetic orientation. During corneal anaesthesia in normal geomagnetic conditions, mole-rats did not maintain their preferred nesting direction, but displayed a random orientation pattern. A second experiment showed that the ability of the mole-rat to discriminate between light and dark was not impeded by the same anaesthetic treatment, suggesting no retinal involvement in mole-rat magnetic orientation. Our study restricts the peripheral primary sensors in mole-rats to the ophthalmic region, probably the cornea and indicates magnetite as the responsible signal mediator.

Innate preference for magnetic compass direction in the Alpine newt, Triturus alpestris (Salamandridae, Urodela)?

Magnetic compass orientation was first discovered for migrating/homing birds in which all individuals of a population or species prefer a predictable magnetic direction during a particular migratory situation. If all other sensory cues are absent, the Earth’s magnetic field may serve as a reference for other orientation mechanisms. It will be demonstrated that alpine newts (Triturus alpestris, Salamandridae) spontaneously align according to the natural or the deviated magnetic field lines of the Earth. They are able to do this in the dark and by apparently seeking to maintain a specific angle with respect to the magnetic field vector. When the horizontal component of the magnetic vector was eliminated, animals became disoriented, and orientation became random. We infer that the animals observed had learned to prefer a particular magnetic direction following environmental/geographical cues. Alternatively, the magnetic directional alignments are innate as, e.g. in migrating birds, but these may be modified/altered according to season, age, hormonal status, and environmental factors such as “landmarks”, light-, sound-, or olfactory cues. Numerous observations of the aligning showed that the preference for a certain magnetic compass direction/axis was not only individual but also specific for the population-subgroups tested. Specimens roughly preferred magnetic directions close to east or west. However, the larvae were able to learn to align to obviously attractive hiding spots (tubes) that were provided in a direction that deviated with respect to the first magnetic preference. The new conditioned alignments were, again, referred to magnetically by the animals and remained stable, even if the hiding tubes were absent. Animals preferred that direction until, eventually, a new directional cue became attractive.

Calibration of magnetic and celestial compass cues in migratory birds - a review of cue-conflict experiments

Migratory birds use multiple sources of compass information for orientation, including the geomagnetic field, the sun, skylight polarization patterns and star patterns. In this paper we review the results of cue-conflict experiments designed to determine the relative importance of the different compass mechanisms, and how directional information from these compass mechanisms is integrated. We focus on cue-conflict experiments in which the magnetic field was shifted in alignment relative to natural celestial cues. Consistent with the conclusions of earlier authors, our analyses suggest that during the premigratory season, celestial information is given the greatest salience and used to recalibrate the magnetic compass by both juvenile and adult birds. Sunset polarized light patterns from the region of the sky near the horizon appear to provide the calibration reference for the magnetic compass. In contrast, during migration, a majority of experiments suggest that birds rely on the magnetic field as the primary source of compass information and use it to calibrate celestial compass cues, i.e. the relative saliency of magnetic and celestial cues is reversed. An alternative possibility, however, is suggested by several experiments in which birds exposed to a cue conflict during migration appear to have recalibrated the magnetic compass, i.e. their response is similar to that of birds exposed to cue conflicts during the premigratory season. The general pattern to emerge from these analyses is that birds exposed to the cue conflict with a view of the entire sunset sky tended to recalibrate the magnetic compass, regardless of whether the cue conflict occurred during the premigratory or migratory period. In contrast, birds exposed to the cue conflict in orientation funnels and registration cages that restricted their view of the region of sky near the horizon (as was generally the case in experiments carried out during the migratory season) did not recalibrate the magnetic compass but, instead, used the magnetic compass to calibrate the other celestial compass systems. If access to critical celestial cues, rather than the timing of exposure to the cue conflict (i.e. premigratory vs migratory), determines whether recalibration of the magnetic compass occurs, this suggests that under natural conditions there may be a single calibration reference for all of the compass systems of migratory birds that is derived from sunset (and possibly also sunrise) polarized light cues from the region of sky near the horizon. In cue-conflict experiments carried out during the migratory season, there was also an interesting asymmetry in the birds' response to magnetic fields shifted clockwise and counterclockwise relative to celestial cues. We discuss two possible explanations for these differences: (1) lateral asymmetry in the role of the right and left eye in mediating light-dependent magnetic compass orientation and (2) interference from the spectral and intensity distribution of skylight at sunset with the response of the light-dependent magnetic compass.