the physics and neurobiology of magnetore

8/3/2019 The Physics and Neurobiology of Magnetore

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*Department of Biology,Duke University, Durham,

North Carolina 27708,USA. Department ofBiology, University of NorthCarolina, Chapel Hill,

North Carolina 27599, USA.Correspondence to S.J.e-mail: [email protected]:10.1038/nrn1745Published online15 August 2005

MAGNETORECEPTOR

A biological structure that cantransduce the strength and/ororientation of the localmagnetic field to an animalsnervous system.

THE PHYSICS AND NEUROBIOLOGYOF MAGNETORECEPTION

Snke Johnsen* and Kenneth J. Lohmann

Abstract | Diverse animals can detect magnetic fields but little is known about how they do so.

Three main hypotheses of magnetic field perception have been proposed. Electrosensitive

marine fish might detect the Earths field through electromagnetic induction, but direct

evidence that induction underlies magnetoreception in such fish has not been obtained.

Studies in other animals have provided evidence that is consistent with two other mechanisms:

biogenic magnetite and chemical reactions that are modulated by weak magnetic fields.

Despite recent advances, however, magnetoreceptors have not been identified with certainty

in any animal, and the mode of transduction for the magnetic sense remains unknown.

Behavioural experiments have shown that many animalscan sense the Earths magnetic field and use it as a cue forguiding movements over both long and short distances1.However, relatively little is known about the neural andbiophysical mechanisms that underlie this sensoryability. Whereas receptors for most other sensory sys-tems have been characterized and studied, primaryreceptors involved in detecting magnetic fields have notyet been identified with certainty in any animal.

Several factors have made locating MAGNETORECEPTORS unusually difficult. One is that magnetic fields passfreely through biological tissue. So, whereas receptorsfor sensory modalities such as vision and olfactionmust contact the external environment to detect stim-uli, this restriction does not apply to magnetoreceptors,

which might plausibly be located almost anywhere inan animals body. In addition, magnetoreceptors mightbe tiny and dispersed throughout a large volume oftissue2, or the transduction process might occur as a setof chemical reactions3, so that there is not necessarilyany obvious organ or structure devoted to magneto-reception. Finally, humans either lack magnetoreception4or are not consciously aware of it5, so our own sensoryexperiences provide little intuitive insight into wheremagnetoreceptors might be found.

So far, most of what is known about magnetorecep-tion has been inferred from behavioural experiments,theoretical considerations and a limited number of

electrophysiological and anatomical studies. This arti-cle begins by discussing the Earths magnetic field andthe basic types of information that animals can extractfrom it. We then summarize the three main hypo-theses of magnetoreception and critically evaluate theevidence for each. Finally, we suggest future directionsfor research in the field.

Information in the Earths field

To a first approximation, the Earths magnetic fieldresembles the dipole field of a giant bar magnet (FIG. 1a).Field lines leave the southern hemisphere and curvearound the globe before re-entering the planet in thenorthern hemisphere.

Animals can potentially extract at least two distinct

types of information from the Earths field. The sim-plest of these is directional or compass information,which enables an animal to maintain a consistent head-ing in a particular direction, such as north or south.Magnetic compasses are phylogenetically widespreadand exist in several invertebrate groups, includingmolluscs, crustaceans and insects, as well as in all fiveclasses of vertebrate1.

Alone, a compass is often insufficient to guide ananimal to a specific destination or to steer it reliablyalong a long and complex migratory route. For exam-ple, a sea turtle migrating through the ocean towarda distant target can be swept off course by currents,

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highly accurate position fixes forEarth-based, portable receivers.

and a migrating birds heading can be altered by wind.Navigation can therefore be enhanced by an abilityto determine position relative to a destination. Fortodays humans, this need is usually met through aGLOBAL POSITIONING SYSTEM (GPS), which provides userswith their geographical position and continuouslycomputes the direction to a goal. For some migratoryanimals, positional information inherent in the Earthsmagnetic field provides a similar, although less precise,way of assessing geographical location.

Several geomagnetic parameters, such as inclinationangle and field intensity, vary across the Earths surfacein ways that make them suitable for use in a position-finding sense6,7 (FIG. 1). Some animals, includingcertain birds810, sea turtles1114, salamanders15,16 andlobsters17, can discriminate small differences in atleast some of these magnetic features. These animalsexploit positional information in the Earths field inseveral different ways, and at least a few are able tolearn the magnetic topography of the areas in whichthey live and so acquire magnetic maps that facilitatenavigation towards specific locations (FIG. 2).

Because the parameters of the Earths field thatare useful for detecting directional and positionalinformation differ, it is possible that some animalshave two separate magnetosensory systems. Eachmight detect a different element of the Earths fieldand each might also rely on separate receptors basedon different biophysical mechanisms18,19.

Possible mechanisms of magnetoreception

During the past three decades, a number of diversemechanisms have been proposed that might providethe basis for detecting magnetic fields1,20. However, themost recent research has focused on three possibilities:ELECTROMAGNETIC INDUCTION, magnetic field-depend-ent chemical reactions and BIOGENIC MAGNETITE. Eachmechanism is discussed below.

Electromagnetic induction. A charged particle movingthrough a magnetic field experiences a force perpen-dicular to both its motion and the direction of thefield. The magnitude of this LORENTZ FORCE is equal tothe product of the magnetic field strength, the chargeand velocity of the particles, and the sine of the anglebetween the motion and field vectors21. Therefore,if an electrically conductive bar moves through amagnetic field in any direction other than parallel tothe field lines, positively and negatively charged parti-cles migrate to opposite sides of the bar, resulting in aconstant voltage that depends on the speed and direc-tion of the bars motion relative to the magnetic field.If the bar is immersed in a conductive medium thatis stationary relative to the field, an electric circuit isformed and current flows through the medium andthe bar.

This principle, known as electromagnetic induction,provides a possible explanation for how elasmobranch

fish (sharks, skates and rays) detect the Earths mag-netic field22,23. According to this hypothesis, jelly-filledcanals on the fish, known as ampullae of Lorenzini,function as the conducting bars; the surrounding seawater functions as the motionless conducting medium,and the highly resistive and sensitive electroreceptorsat the inner end of the ampullae detect the voltage dropof the induced current.

However, several factors significantly complicatethese simple models. First, the electroreceptors ofelasmobranches cannot detect the steady fields thatwere originally thought to arise24. Second, the watersurrounding marine fish is seldom motionless under

Figure 1 | Large-scale and fine-scale structure of the Earths magnetic field.

a | Diagrammatic representation of the Earths magnetic field. The general form of the Earths

field resembles the dipole field of a giant bar magnet, with field lines emerging from the southern

hemisphere, wrapping around the globe, and re-entering the Earth at the northern hemisphere.

The inclination angle (that formed between the field lines and the Earth) varies with latitude. At

the magnetic equator, the field lines are parallel to the Earths surface and the inclination angle is

0o. An animal migrating north from the magnetic equator to the magnetic pole encounters

progressively steeper inclination angles along its journey. At the magnetic pole in the northern

hemisphere, field lines are directed straight down into the Earth and the inclination angle is 90o.

This variation in the inclination angle is used by some animals to assess geographic position 11,16.

The strength or intensity of the Earths field is weakest near the equator and strongest near the

magnetic poles. Some animals can derive positional information from field intensity12. b | Merged

aeromagnetic anomaly map of the state of Virginia, USA. Although some long-distance migrants

evidently extract positional information from the general dipole field10,13 shown in (a), fine-scale

variations are more complex than the general regional patterns because concentrations of

ferromagnetic minerals in the Earths crust often generate local field anomalies. Although these

variations are typically less than 1% of the total field, their gradients (that is, thevariation per

distance) can be significantly greater than the gradients due to the main dipole field, and can

also be aligned in a different direction. The larger gradients might be easier for a short-distance

migrant or homing animal to detect, but the complexity of local magnetic contours indicates that

any navigational strategies that exploit magnetic topography over these smaller spatial scales

are likely to be site-specific, difficult to generalize and learned rather than inherited. Colour scale

shows deviations in the strength of the Earths dipole field in Virginia (dipole field is ~52,000

nanoTelsa (nT)124) in both nanoTesla and percent. Image reproduced from REF. 125.

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ELECTROMAGNETIC

INDUCTION

A current in a loop ofconducting wire that is causedby a changing magnetic field inthe circle formed by the loop.

BIOGENIC MAGNETITE

Magnetite (Fe3O

4) synthesized

by a living organism.

LORENTZ FORCE

The force exerted on a charged

particle moving through amagnetic field.

natural conditions. Third, ocean currents are also con-ductors moving through the Earths magnetic field,and so create electric fields of their own. Presumably,therefore, the animal must be able to determinewhich component of the total field that it experiencesis attributable to its own motion and which is dueto the motion of water22,25. In principle, these prob-lems might be overcome if sharks derive magneticfield information from the oscillating electric fieldsthat arise as the ampullae on their heads move backand forth during swimming25. Such fields shouldbe distinguishable from fields caused by oceaniccurrents.

Although sea water is a highly conductive medium,air is not. Therefore, birds and other terrestrial animalscannot accomplish magnetoreception by induc-tion in the same way that has been proposed forelectrosensitive marine fish. Although an induction-based system using an internal current loop (a closedcircuit inside an animal) is theoretically possible, sucha loop would need to rotate relative to the Earthsfield21 and would probably also require a specializedinternal transduction organ several millimeters indiameter26. The semicircular canals have some of thenecessary features, but at present there is no evidencethat magnetoreception occurs in the inner ear, andno likely alternative structure or site has been foundin any animal26.

Evidence for electromagnetic induction. Directevidence that animals use electromagnetic inductionto detect the Earths magnetic field has not yet beenobtained. Nevertheless, rays and sharks clearly havea highly sensitive electric sense with which they can

detect the weak electric fields generated by the tissuesof their prey27. This electrosensory system seems to besufficiently sensitive to permit detection of the Earthsmagnetic field28.

Several studies have provided experimental or cor-relative evidence that is consistent with the hypothesisthat elasmobranches do perceive magnetic stimuli2933.In some cases, however, it was impossible to determineprecisely what the animals detected. For example, in arecent experiment captive sharks learned to approachan area of the tank for a food reward when a magneticcoil surrounding the tank was turned on33. Althoughthis was interpreted as a response to the imposed mag-netic field, an equally plausible explanation is that thecrucial stimulus might have been the transient electricfield that is generated whenever the current througha coil is turned on21. Similarly, rays have been condi-tioned to move towards a specific magnetic direction inan enclosure29, but whether the rays responded to thedirection of the fieldper se, or instead to the presenceof field anomalies, is debatable1,34.

In a recent attempt to investigate the mechanismof magnetoreception in elasmobranch fish, rays wereconditioned to respond to the presence or absence ofmagnetic field anomalies31,32. The conditioned responsedisappeared when small magnets were inserted intotheir nasal cavities, whereas inserting non-magnetic

brass bars had no effect. These results have been inter-preted as evidence against the electromagnetic induc-tion hypothesis because induction should be unaffectedby attached magnets that move in concert with theanimal32. A crucial question is whether the movementsof the magnets in the nasal cavities precisely matchedmovements of the electroreceptors on the flexiblebodies of the fish, because if slight differences inmotion occurred then a magnetoreception systembased on induction might indeed have been affected.Whether elasmobranch fish rely on electromagneticinduction for magnetoreception or use an alternativemechanism remains unresolved.

Figure 2 | Evidence for a magnetic map in sea turtles. Juvenile sea turtles establish

feeding sites in coastal areas and home back to these sites if displaced126,127. To

investigate how turtles navigate to specific sites, juvenile green turtles (Chelonia mydas)

were captured in their coastal feeding areas near Melbourne Beach, Florida, USA (test

site on map). Each turtle was tethered to an electronic tracking system and placed in apool of water. The pool was surrounded by a magnetic coil system that could be used to

replicate the magnetic fields that exist at two distant sites (marked by blue dots). In the

circles, each black dot represents the mean direction of one turtle. The arrow in the centre

of each circle indicates the mean angle of the group. The dotted lines indicate the 95%

confidence interval for the mean angle. Turtles exposed to a magnetic field that exists

~330 km north of their feeding grounds oriented southward, whereas those tested in a

field that exists an equivalent distance to the south swam north. Therefore, turtles

responded to each field by swimming in the direction that would have led towards the

feeding area had they actually been in the locations at which the magnetic fields exist.

The results indicate that sea turtles have a type of magnetic map that facilitates

navigation to specific geographical areas. Modified, with permission, from REF. 14

(2004) Macmillan Magazines Ltd.


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PRECESSION

The relatively slow rotation ofthe axis of a spinning object.

BACKTRANSFER

The return of a donatedelectron to its donor.

PAULI EXCLUSION PRINCIPLE

Quantum mechanical principle

that states, among other things,that two electrons with the samespin cannot occupy the same

orbital.

RADICAL PAIR

Two charged molecules held inclose proximity in solution by acage of solvent molecules.

MICELLE

An aggregate of detergent-likemolecules in solution, withhydrophilic ends facing

outwards and hydrophobic endsfacing inwards.

Chemical magnetoreception. A second proposedmechanism of magnetoreception involves chemicalreactions that are modulated by Earth-strengthmagnetic fields. At first glance, it seems unlikelythat fields as weak as the Earths could influenceany chemical reaction, let alone those in animals.After all, such reactions involve alterations inthe energies of electrons, and the energy differ-ences between different orbitals are many orders ofmagnitude too large for the Earths field to transferelectrons directly from one orbital to another. In addi-tion, at physiological temperatures the kinetic energyof biological molecules is 2 x 1011 times greater thanthe energy of the Earths field and might, therefore, beexpected to overwhelm any slight magnetic effect35.

Nevertheless, weak magnetic fields might exertan influence on biological molecules and chemicalreactions under at least some circumstances. Severalingenious mechanisms have been proposed anddebated3639, but the only hypothesis that has so fargained widespread acceptance as physically plausible

is one that relies on chemical reactions involving pairsof radicals40,41.

The proposed mechanism is that Earth-strengthmagnetic fields influence correlated spin states ofpaired radical ions3,37,42. Electron spins are largelyunaffected by thermal noise, and so represent one ofonly a few molecular features that might plausibly beinfluenced by the Earths field35.

The putative process begins with an electron transferfrom a donor molecule, A, to an acceptor molecule, B.This leaves each with an unpaired electron, the spinsof which are either opposite (singlet state) or parallel(triplet state). Either way, the spins precess, meaningthat the axis of rotation changes slowly in much thesame way that a spinning top wobbles around a verti-cal axis as it slows down. This analogy is not precise,however, because electron spin can have only one oftwo orientations (up or down). The PRECESSION of thespins is caused by interactions with the local magneticenvironment, which, in turn, is determined by thecombined magnetic fields that are generated bythe spins and orbital motions of unpaired electrons andmagnetic nuclei, and any external field.

Because the two electrons encounter slightly dif-ferent magnetic forces, they precess at different rates.After a brief period of time, the electron that wastransferred returns to the donor. Depending on the

time that elapses before the BACKTRANSFER and the dif-ference in precession rates between the two electrons,the original singlet or triplet state of the donor mightbe preserved or altered. If electron backtransfer occursquickly, then the electron spins will have precessedlittle and are therefore likely to remain in their origi-nal opposite or parallel correlated state. As a result, Aand B remain unchanged. However, in a longer reac-tion the differences in precession rates between thetwo electrons can alter the original spin relationship;A and B are, therefore, chemically altered, which, inturn, can influence subsequent reactions. For example,a change from a singlet to a triplet state often prevents

the subsequent recombination of A and B owing tothe PAULI EXCLUSION PRINCIPLE (which states that twoelectrons with parallel spins cannot share the sameorbital)43.

For the RADICAL PAIR mechanism to operate inmagnetic fields as weak as that of the Earths, severalstringent conditions must be met40,41. First, the reactiontime must be long enough for the small differences inprecession rate to alter the spin correlation, a processthat takes at least 100 ns and that cannot occur in thetime course of most known radical pair reactions3. Onthe other hand, however, the reaction cannot occur tooslowly, or the spin correlation might be randomized byother disruptive processes3. Therefore, the mechanismcan presumably work only if the reaction time fallswithin a narrow range, although reactions of a longerthan expected duration are hypothetically possible ifthe reactants are compartmentalized in MICELLES44.

Several other factors impose considerable con-straints on the radical pair mechanism. For example,the speed of the reaction and the strength of inter-

actions between the spins of the electrons and nucleiin the molecules must be related in highly specific waysfor the orientation and strength of the Earths field tohave a significant effect41. Moreover, the moleculesinvolved must be simple and contain few hydrogenor nitrogen atoms, as otherwise internal magneticinteractions will overwhelm any effects due to theEarths field41. In addition, because the influence ofthe Earths field on the putative chemical processes isweak, the effect must presumably be summed over alarge area. Calculations indicate that ~108 radical pairsover a volume of 0.4 mm3 are required to reliably detectan anomaly with a strength of 2% of the Earths field42.Finally, the initial electron transfer must not randomizethe original parallel or opposite spin relationship of thetwo electrons. This is not true of all electron transferprocesses, but is often true when the transfer is inducedby photo-excitation (that is, by the absorption oflight)3,37. Indeed, many of the best-known radical pairreactions begin with electron transfers that are inducedby light absorption3,37,43. This consideration has led tothe suggestion that chemical magnetoreceptors, if theyexist, might also be photoreceptors3.

If magnetoreception does occur in photoreceptors,then an interesting possibility is that the processinvolves cryptochromes, a group of photosensitiveproteins that are involved in the circadian systems of

plants and animals45,46. Cryptochromes exist in the reti-nae and pineal glands of many animals47. In addition,they show marked homology to photolyases, which areknown to form radical pairs after photo-excitation48.Finally, neural activity during magnetic orientationbehaviour co-localizes with cryptochrome expressionin retinal ganglion cells in a night-active migratorybird, whereas no such co-localization occurs in non-migratory birds or during daytime45. However, itis not known whether this is due to a link betweencryptochromes and magnetoreception or simply a linkbetween cryptochromes and photoperiodic behaviourthat is associated with migration.


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Evidence for chemical magnetoreception. At present,no chemical reactions affected by Earth-strength mag-netic fields are known43. Some reactions that involvethe radical pairs mechanism are affected by fields asweak as 1 milliTesla49, but this field intensity is still ~20times the strength of the Earths field. Nevertheless,models indicate that the necessary sensitivity might bepossible under at least some conditions50,51.

Although direct evidence for chemical magneto-reception has not yet been obtained, several lines ofevidence have indicated a link between magneto-reception and the visual system. Electrophysiologicalresponses to magnetic fields have been detected in

several parts of the avian brain that receive projectionsfrom the visual system1,52. For example, the nucleus ofthe basal optic root (nBOR) in pigeons receives pro-

jections from retinal ganglion cells, and some neuronsin the nBOR and optic tectum respond to directionalchanges in the ambient magnetic field53,54. The ampli-tude of the responses in the nBOR depended on thewavelength of the light entering the eye54 and responsesto magnetic fields in both locations disappeared whenthe optic nerves were cut52.

Several studies have also indicated a link betweenmagnetoreception and the pineal gland 53,55 ,56.Electrophysiological recordings from pigeon pinealcells revealed units that were responsive to gradualchanges in Earth-strength magnetic fields57. Responseswere reduced, but not abolished, when the optic nervesand other sources of input to the pineal gland weresevered, which implies that one source of magneticsensitivity is in the pineal gland itself57. A study withnewts also revealed that the magnetic direction thatnewts orientated towards shifted when the pineal com-

plex was illuminated with light of a specific wavelength,whereas no such response was elicited when the lightilluminated the eyes alone56.

Numerous experiments have indicated that themagnetic orientation behaviour of birds, newts andflies changes when the animal is exposed to specificwavelengths of light20,5864. The finding that suchwavelength-dependent responses also vary withthe intensity of light60,65 has greatly complicated theemerging picture because absorption of light is gener-ally wavelength-dependent. So, if an animal is exposedto identical photon fluxes of two lights with differentwavelengths, it might perceive one light to be muchbrighter than the other, and receptors for vision, mag-netoreception, or both might absorb different amountsof light under the two conditions. For this reason,disentangling the effects of wavelength and intensity isalmost impossible.

No discernable pattern has yet emerged amongspecies, but a bewildering array of wavelength and/or intensity-dependent effects have been reported,including loss of orientation, shifts in orientationdirection and shifts to axial orientation59,60,6568BOX 1.Several interesting models have been proposed toexplain these complex results, most of which involveopponency between a putative dominant short-wave-length mechanism and a subordinate long-wavelength

mechanism68,69. However, so far none of the modelshave been tested rigorously.

A final line of evidence that is consistent witha radical pairs mechanism of magnetoreceptioncomes from recent studies involving radio frequencyfields. Radical pair reactions can be perturbed byradio waves of approximately the same energyas that of the interaction between the spin statesand the Earths magnetic field50,70. This allows fora potentially diagnostic test of magnetoreceptormechanism. Broadband radio noise (0.110.0 MHz)and a constant frequency signal of 7 MHz both dis-rupted magnetic orientation in European robins71.

Box 1 | Light-dependent effects: magnetoreception or motivation?

Although evidence for magnetoreception based on a radical pair mechanism is

accumulating, critics have questioned the interpretation of several key results32.

One unresolved issue involves changes in magnetic orientation behaviour that are

elicited by different wavelengths and intensities of light. These have generally been

interpreted as direct effects on magnetoreceptor function, but in some cases it is

difficult to rule out an alternative possibility: that light instead affects

physiological processes unrelated to magnetoreception, which, in turn, affectmotivation32,112.

Light-dependent effects on magnetic orientation behaviour vary greatly among

species, and some are more difficult to reconcile with motivational changes than

others. For example, it is difficult to explain in terms of motivation why a newt

would choose to shift its orientation by 90 when exposed to a specific type of

monochromatic light61. However, in contrast to such clear directional shifts, many

of the wavelength-dependent effects involve the disruption of orientation60, an

outcome that might arise for various reasons. An animal in the lab, for example,

might decide to search for shelter instead of trying to migrate when the world

around it is illuminated in a strange and perhaps alarming way.

In birds, seasonal migratory behaviour is intimately connected to light cycles and

light perception. Migratory behaviour is triggered by photoperiod and, for night

migrants, the motivation to begin the next leg of migration peaks at or near sunset.

Given the complex interplay among light-dependent processes, biological rhythms,motivation and migration, an intriguing but largely unexplored possibility is that

at least some light-dependent changes in magnetic orientation arise through effects

on a circadian pacemaker system, which, in turn, influences the expression or

timing of orientation behaviour.

The entrainment of circadian rhythms has recently been shown to depend at least

in part on the absorption of light by the photopigment melanopsin 113. In

vertebrates, melanopsin is found in the pineal gland and in the visual system,

where it has been localized to a limited number of retinal ganglion cells114,115.

The pigment is most sensitive to blue light116,117 and may have a blueyellow

opponency mechanism via cone inputs118,119. Because such opponency often results

in outcomes that vary with the spectral composition of light, these findings raise

the possibility that different combinations of wavelengths and intensities might

affect the pacemaker system in complex and unexpected ways. Finally, the apparent

lateralization of the magnetic sense, discovered in magnetic orientationexperiments in which one eye of birds was covered120, shows interesting parallels to

the lateralization of the circadian pacemaker121,122.

A first step towards investigating this possibility would be to measure melatonin

levels during and after exposure to light environments that are known to affect

magnetic orientation. Because melatonin peaks at night and provides a convenient

assay for circadian rhythmicity, a finding that melatonin levels are unaffected by

the different treatments would bolster the argument that the effects are specific to

magnetoreception. If melatonin levels do change under some light regimes, then

such changes could be replicated pharmacologically to investigate possible effects

on orientation behaviour.


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SDB = 0

SP

Ion channelsa b

Superparamagnetic clusters

these crystals inside nerve terminals and arrangedalong the cell membrane80. However, in contrast tothe single-domain magnetite detected in fish82, themagnetite crystals in the beak of the pigeon are super-paramagnetic83,85.

An interesting similarity between fish and birds

is that, in both cases, the anatomical site that con-tains the magnetite appears to be innervated by theophthalmic branch of the trigeminal nerve80,81,86. Twofurther findings are consistent with the hypothesisthat branches of the trigeminal nerve innervatemagnetoreceptors in birds. First, cutting the oph-thalmic branch permanently abolished a conditionedresponse of pigeons that had been trained to discrim-inate between the presence and absence of a smallmagnetic anomaly87. Second, electrophysiologicalrecordings in birds indicate that specific neurons inthe trigeminal ganglion, to which the ophthalmicnerve projects, respond to changes in vertical field

intensity as small as about 0.5% of the Earths field9(FIG. 4). These cells have been proposed to function ina magnetic map sense52.

Although direct evidence that magnetite functionsin magnetoreception remains limited, additionalcircumstantial evidence has been provided by pulsemagnetization experiments. A strong magnetic fieldof brief duration can be used to alter the directionof magnetization in single-domain magnetite parti-cles88. Recent analyses have also indicated that such amagnetic pulsemight also disrupt superparamagneticcrystals under at least some conditions83. Pulse mag-netization might, therefore, alter magnetite-basedmagnetoreceptors and so change the behaviour ofanimals that use such receptors to derive directionalor positional information from the Earths field.

In several studies, the application of strong mag-netic pulses to birds and turtles either randomizedthe preferred orientation direction or else deflectedit slightly relative to controls19,8992. These results havegenerally been interpreted as evidence for magnetite-

based magnetoreceptors, although other explanationscannot be ruled out entirely19, particularly given thatpulsed magnetic fields generate large transient electricfields21.

Strong magnetic pulses might hypotheticallyalter magnetite-based receptors that are part of acompass sense, a map sense or both. However, find-ings in birds indicate that the effect might be on amap sense rather than a compass sense. Pulsed fieldsinfluenced the orientation of adult birds, which arethought to rely on map information for navigation,but failed to affect young birds, which complete theirfirst migration by flying along a consistent compassheading93. At the same time, pulse magnetization alsosignificantly altered the magnetic orientation behav-iour of mole rats, which have a magnetic compass butare not thought to have a map sense94. These resultshighlight the possibility that magnetite-based recep-tors might have different functional roles in differentanimals.

Compasses, maps and mechanisms

All three mechanisms that we have described seemto be capable of providing an animal with directionalinformation that might be used in a magnetic com-pass sense. However, the information derived fromthe field is not the same in all cases. The induction

model and some single-domain magnetite mod-els are capable of detecting field polarity (that is,they can distinguish between magnetic north andsouth)28,76. By contrast, no current model based onchemical magnetoreception or superparamagnetismcan do this3,79.

Interestingly, there are two functionally differenttypes of magnetic compass in animals. Polarity com-passes, which are present in lobsters95, salmon96 andmole rats94, determine north using the polarity of thehorizontal field component. By contrast, the inclina-tion compasses of birds1,97 and sea turtles98 evidentlydo not detect the polarity of the field (that is, north

Figure 3 | The different magnetic properties of single-domain and superparamagneticcrystals. a | Single-domain (SD) and superparamagnetic (SP) magnetite crystals have

different magnetic properties. Single-domain crystals have permanent magnetic moments

(indicated by red arrows) even in the absence of an external magnetic field (B = 0). If an

external field is present (black arrow) and the crystals are free to rotate, they will align with the

external field. By contrast, superparamagnetic crystals have no magnetic moment in the

absence of an external field. If an external field is present, however, the crystals develop a

magnetic moment that tracks it, even though the crystal itself does not rotate. b | A

hypothetical transduction mechanism based on interacting clusters of superparamagnetic

crystals located in the membranes of neurons. Depending on the orientation of the external

field, the clusters will either attract or repel each other, deforming the membrane and possibly

opening or closing ion channels. For example, when the external field is parallel to the cell

membrane, the fields in each crystal (red arrows) align in such a way that adjacent clusters

attract each other like a row of bar magnets aligned end to end (middle panel). The membrane

might, therefore, be slightly compressed. By contrast, a 90-degree change in the orientationof the external field (bottom panel) results in different interactions between clusters, because

adjacent clusters now behave like a row of bar magnets aligned side by side. The resulting

interactions might stretch the membrane and open ion channels. This model was inspired by

the discovery of superparamagnetic crystals in pigeon nerve terminals79. Modified, with

permission, from REF. 79 (2003) Elsevier Science.


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versus south). Instead, they define poleward as thedirection along the Earths surface in which the angleformed between the magnetic field vector and thegravity vector is smallest. Some salamanders haveboth types of compasses and use each in differentbehavioural tasks99.

Because some of the proposed magnetoreception

mechanisms can detect field polarity whereas otherscannot, it is tempting to conclude that polarity andinclination compasses have different underlyingmechanisms. However, this inference might be pre-mature. For example, single-domain magnetite crystalscan potentially yield receptors that are either capableor incapable of detecting field polarity76,100. In addi-tion, higher-order neural processing often gives riseto behavioural outputs that do not closely mirror theproperties of receptors. For now, the only safe con-clusion seems to be that chemical magnetoreceptionand superparamagnetic magnetite cannot account forpolarity compasses.

All three mechanisms seem to be capable ofdetecting at least some elements of the Earths fieldthat might be used in assessing geographical loca-tion. To detect the inclination of field lines, an animalwould presumably need to integrate informationfrom its magnetoreception system with informationfrom a gravity-sensing system. However, no theoreti-cal barrier seems to preclude detection of magneticinclination by a receptor system based on any of themechanisms.

By contrast, the different mechanisms are likelyto have differing sensitivities to field intensity.Receptors based on single-domain or superpara-magnetic magnetite might be able to detect verysmall changes in field intensity10 0, whereas thechemical and induction mechanisms probably can-not3,26. In the chemical models, the limitation is dueto the small effect of field strength on the proposedreactions3,101. In induction models, difficulties arisebecause the animal would need to precisely deter-mine both its own velocity and the magnitude of the

background (passive) electrical fields in its environ-ment. So, given the relatively small field changes thatan animal using a magnetic map would probablyneed to detect102104, a map sense based on intensityis unlikely to be mediated by a chemical or inductionmechanism.

Concluding remarks

Three physically plausible mechanisms have beenproposed that might underlie magnetoreception inanimals. Recent advances are consistent with thehypothesis that a magnetic compass based on chemicalmagnetoreception exists in birds, and candidatemagnetite-based receptors, possibly functioningin a magnetic map sense, have now been reported inboth birds and fish. However, these findings shouldbe viewed as tentative. Despite recent progress, pri-mary magnetoreceptors have not been identified withcertainty in any animal, and the mode or modes oftransduction for the magnetic sense therefore remainunknown.

Future progress might be expedited by two real-izations. First, although magnetoreception researchbegan with behavioural studies, such studies cannot,by themselves, elucidate transduction processes thatoccur at or below the cellular level. Sustained effortsto incorporate a wider range of modern neuro-

science techniques into magnetoreception researchare now needed an undertaking that has perhaps

just recently begun45,46,80,105109. In parallel with thisis the need to identify new model systems in whichmagnetoreception can be investigated. Migratory

vertebrates, such as birds and sea turtles, have provedfavourable for behavioural experiments, but they arenot ideal for work in the realms of neurobiology,microscopy and genetics. The discovery that magneticsensitivity exists in zebrafish110, the fruitflyDrosophilamelanogaster62,111 and in Tritonia diomedea, a molluscwith a simple nervous system107109 might representpromising first steps in this direction.

Figure 4 | Results of electrophysiological experiments with the bobolink bird. a | The

trigeminal ganglion of the bobolink (Dolichonyx oryzivorus), showing the nerves and the

locations of neurons (marked by crosses) that responded to changes in the ambient magnetic

field with altered electrical activity. b | Recordings from one such ganglion cell during different

changes in vertical magnetic field intensity (these changes also altered the inclination and total

intensity of the field). (1) Spontaneous activity. (2) Response to 200 nanoTelsa (nT) change.

(3) Response to 5,000 nT change. (4) Response to 15,000 nT change. (5) Response to 25,000

nT change. (6) Response to 100,000 nT change. The Earths field is ~50,000 nT. Stimulus

onset is indicated by the bar below each series. Modified, with permission, from REF. 9

(2003) Elsevier Science.


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AcknowledgementsWe thank P. Hore, J. Canfield and C. Lohmann for comments ondrafts of the manuscript. The authors research was supported by

a grant from the National Science Foundation.

Competing interests statementThe authors declare no competing financial interests.


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