FEATURES on June 23, 2016 http://science.sciencemag.org/ Downloaded from

Joe Kirschvink, sporting an EEG sensor cap, was the first subject in his magnetic-sensing tests.

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Published by AAAS NEWS POLAR EXPLORER Joe Kirschvink thinks he has found a magnetic sixth in humans

By Eric Hand on June 23, 2016 irds do it. Bees do it. But the human array of electrical coils, while an electro- subject, standing here in a hoodie— encephalogram (EEG) machine records his can he do it? Joe Kirschvink is de- waves. termined to find out. For decades, For much of the 20th century, magneto- he has shown how critters across reception research seemed as unsavory as the the kingdom navigate us- study of dowsing or telepathy. Yet it is now ing magnetoreception, or a sense an accepted fact that many sense the of Earth’s . Now, the always-on, barely-there magnetic field of geophysicist at the California Insti- Earth. Birds, fish, and other migratory ani- tute of Technology (Caltech) in Pasadena is mals dominate the list; it makes sense for Btesting humans to see if they too have this them to have a built-in compass for their subconscious sixth sense. Kirschvink is pretty globetrotting journeys. In recent years, re- http://science.sciencemag.org/ sure they do. But he has to prove it. searchers have found that less speedy crea- He takes out his iPhone and waves it over tures—lobsters, worms, snails, frogs, newts Keisuke Matsuda, a neuroengineering gradu- —possess the sense. Mammals, too, seem ate student from the University of Tokyo. On to respond to Earth’s field: In experiments, this day in October, he is Kirschvink’s guinea wood mice and mole rats use magnetic field pig. A magnetometer app on the phone lines in siting their nests; and deer ori-

would detect magnetic dust on Matsuda— ent their bodies along them when grazing; Downloaded from or any hidden magnets that might foil the and point themselves north or south experiment. “I want to make sure we don’t when they urinate or defecate. have a cheater,” Kirschvink jokes. The mounting scientific evidence for They are two floors underground at magnetoreception has largely been behav- Caltech, in a clean room with magnetically ioral, based on patterns of movement, for ex- shielded walls. In a corner, a liquid helium ample, or on tests showing that disrupting or pump throbs and hisses, cooling a super- changing magnetic fields can alter animals’ conducting instrument that Kirschvink has habits. Scientists know that animals can used to measure tiny magnetic fields in every- sense the fields, but they do not know how thing from bird beaks to martian meteorites. at the cellular and neural level. “The frontier On a lab bench lie knives—made of ceramic is in the biology—how the brain actually uses and soaked in acid to eliminate magnetic this information,” says David Dickman, a contamination—with which he has sliced neurobiologist at the Baylor College of Medi- up human in search of magnetic par- cine in Houston, Texas, who in a 2012 Science ticles. Matsuda looks a little nervous, but he paper showed that specific neurons in the will not be going under the knife. With a sy- inner ears of pigeons are somehow involved, ringe, a technician injects electrolyte gel onto firing in response to the direction, polarity, Matsuda’s scalp through a skullcap studded and intensity of magnetic fields. with electrodes. He is about to be exposed Finding the magnetoreceptors responsible

PHOTO: SPENCER LOWELL PHOTO: to custom magnetic fields generated by an for triggering these neurons has been like

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Published by AAAS NEWS | FEATURES looking for a magnetic needle in a haystack. things and not right about other things.” There’s no obvious sense organ to dissect; In support of his hypotheses, Kirschvink magnetic fields sweep invisibly through the has gathered rocks from all over the world: entire body, all the time. “The receptors could South Africa, China, Morocco, and Australia. What and where be in your left toe,” Kirschvink says. But looking for magnets in animals—and Scientists have come up with two ri- humans—in his windowless subbasement are the body’s val ideas about what they might be (see lab has remained an abiding obsession. Just sidebar, right). One is that magnetic fields ask his first-born son, who arrived in 1984, as magnetometers? trigger quantum chemical reactions in Kirschvink and his wife—Atsuko Kobayashi, called . Crypto- a Japanese structural biologist—published By Eric Hand chromes have been found in the retina, but the discovery of in the sinus tis- no one has determined how they might con- sue of yellowfin tuna. At Kirschvink’s sugges- hat many animals sense and trol neural pathways. The other theory, which tion, they named him Jiseki: magnet stone, respond to Earth’s magnetic field Kirschvink favors, proposes that miniature or magnetite. is no longer in doubt, and people, compass needles sit within receptor cells, Kirschvink, 62, could never decide be- too, may have a magnetic sense either near the behind ani- tween geology and biology. He remembers (see main story, p. 1508). But how mals’ noses or in the inner ear. The needles, the day in 1972 when, as an undergraduate at Tthis sixth sense might work remains presumed to be made up of a strongly mag- Caltech, he realized that the two were inter- a mystery. Some researchers say it netic mineral called magnetite, would twined. A professor held the tongue plate relies on an iron mineral, magnetite; somehow open or close neural pathways. of a , a type of mollusk, and dragged others invoke a in the retina The same candidate magnetoreceptors it around with a bar magnet. Its teeth were called . are found in humans. So do we have a mag- capped with magnetite. “That blew me Magnetite has turned up in bird netic sense as well? “Perhaps we lost it with away,” recalls Kirschvink, who still keeps beaks and fish noses and even in the our civilization,” says Michael Winklhofer, a the tongue plate on his desk. “Magnetite is human brain, as Joe Kirschvink of the biophysicist at the University of Oldenburg typically something that geologists expect in California Institute for Technology in on June 23, 2016 in Germany. Or, as Kirschvink thinks, per- igneous rocks. To find it in an animal is a bio- Pasadena reported in 1992, and it is haps we retain a vestige of it, like the wings chemical anomaly.” extremely sensitive to magnetic fields. of an ostrich. For many years, scientists thought As a result, Kirschvink and other fans had evolved a way to synthesize magnetite say, it can tell an animal not only which KIRSCHVINK SPECIALIZES in measuring simply because the hard mineral makes for way it is heading (compass sense) but remanent magnetic fields in rock, which a good, strong tooth. But in 1975, Richard also where it is. “A compass cannot can indicate the latitude at which the rock Blakemore at the Woods Hole Oceanographic explain how a sea can migrate all formed, millions or billions of years ago, Institution in Massachusetts suggested that the way around the ocean and return to and can trace its tectonic wanderings. The in certain , magnetite is a magnetic the same specific stretch of beach where technique has led him to powerful, influen- sensor. Studying bacteria from Cape Cod it started out,” says neurobiologist tial ideas. In 1992, he marshaled evidence marsh muds, Blakemore found that when Kenneth Lohmann of the University of http://science.sciencemag.org/ that glaciers nearly covered the globe more he moved a small magnet around his glass North Carolina, Chapel Hill. A compass than 650 million years ago, and suggested slides, the bacteria would rush toward the sense is enough for an animal to figure that their subsequent retreat from “Snow- magnet. Looking closer, he found that the mi- out latitude, based on changes in the ball Earth” (a term he coined) triggered an crobes harbored chains of magnetite crystals inclination of magnetic field lines (flat evolutionary sweepstakes that would become that forced the cells to align with the lines of at the equator, plunging into the earth the Cambrian explosion 540 million years Earth’s own magnetic field, which in Mas- at the poles). But longitude requires ago. In 1997, he worked out a provocative sachusetts dip down into the ground at 70°, detecting subtle variations in field explanation for the abnormally speedy drift toward the North Pole. Many bacteria search strength from place to place—an extra Downloaded from of continental plates about the same time as randomly for the right balance of oxygen and map or signpost sense that magnetite the Cambrian explosion: Earth’s rotational nutrients, utilizing a motion called “tumble could supply, Lohmann says. axis had tipped over by as much as 90°, and run.” But as swimming compass needles, Except in bacteria, however, no one Kirschvink proposed. The climatic havoc Blakemore’s bacteria knew up-mud from has seen magnetite crystals serving as a from this geologically sudden event also down-mud. They could surf this gradient magnetic sensor. The crystals could be would have spurred the biological innova- more efficiently and would swim downward something else—say, waste products of tions seen in the Cambrian. And he was along it whenever the mud was disturbed. iron metabolism, or a way for the body prominent among a group of scientists who These bacterial magnetoreceptors are still to sequester carcinogenic heavy metals. in the 1990s and 2000s argued that magnetic the only ones scientists have definitively In the early 2000s, scientists found crystals in a famous martian meteorite, Allan located and studied. To Kirschvink, their magnetite-bearing cells in the beaks of Hills 84001, were fossilized signs of life on presence indicates that magnetoreception pigeons. But a follow-up study found the Red Planet. Although the significance of is ancient, perhaps predating Earth’s first that the supposed magnetoreceptors Allan Hills 84001 remains controversial, the eukaryotic cells, which are thought to have were in fact scavenger immune cells idea that life leaves behind magnetofossils is evolved nearly 2 billion years ago after a host that had nothing to do with the neural an active area of research on Earth. cell captured free-living bacteria that became system. And because there is no unique “He’s not afraid to go out on a limb,” says the cell’s energy-producing mitochondria. stain or marker for magnetite, false Kenneth Lohmann, a neurobiologist who “I’m suggesting that the original mitochon- sightings are easy to make. studies magnetoreception in lobsters and dria were magnetic bacteria,” Kirschvink Cryptochrome, too, offers much sea at the University of North Caro- says, which could mean that all eukaryotes lina, Chapel Hill. “He’s been right about some have a potential magnetic sense.

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Published by AAAS Making sense of it all Scientists studying magnetoreception are zooming in on two possible mechanisms: a mechanical sensor based on the magnetic mineral magnetite and a biochemical sensor based on the protein cryptochrome.

Magnetite model Magnetite has been found in many Cell membrane Positive ion animal tissues, but in fsh, some + evidence points to the nose as the home Ion channel for magnetoreceptors. They could sit opens between ciliated olfactory sensory cells. Salmon Cilia

Cytoplasm

Ion channel Magnetite, tugged by Earth’s Eeld, would mechanically control neural circuits by opening ion Olfactory bulb channels in cell membranes. Magnetoreceptor cell Magnetite

Cryptochrome model Cryptochromes may lie in mysterious double Opsin Cryptochrome Light turns the cryptochrome into a cone cells. The ratio of chemical products radical pair molecule, with two unpaired from each cone could determine magnetic electrons that fip between parallel and on June 23, 2016 orientation, which the brain might process antiparallel states. as light and dark patches on the visual Eeld. Same spin

0 Radical Pigeon Cone Light pairs Rod DiLerent Disk membranes Fields Retina spin

90 shift http://science.sciencemag.org/ Bipolar cell

Ganglion cell Cryptochromes in neighboring cones could be oriented 90 from Magnetic Eelds can boost the tendency Eye each other and held in place by for antiparallel states, altering chemical

membrane stacks. reaction outputs. Downloaded from

to like. When short-wavelength light focused on cryptochrome’s control over magnetite, however, scientists haven’t strikes it, it becomes what chemists call circadian clocks, but Schulten knew that yet seen the molecule in action and don’t a “radical pair”: a molecule containing the molecule could form a radical pair. know exactly how it might alter neural two unpaired electrons whose spins can “This was my day,” Schulten says. “Finally circuitry. Worse, laboratory experiments be either aligned or not. A magnetic field now I had a really good candidate.” In show that it takes magnetic fields orders can flip the spins back and forth between 2000, he published a study showing how of magnitude stronger than Earth’s to trip aligned and nonaligned states, changing magnetic fields could influence crypto- a cryptochrome sensor. the chemical behavior of the molecule. In chrome reactions to create light and dark So who’s right? It doesn’t have to be 1978, , a physicist at the patches in the visual fields of birds. either-or, says Peter Hore, a physical University of Illinois, Urbana-Champaign, A retinal cryptochrome sensor could chemist at the University of Oxford in the had suggested that animals could use explain why blue or green light appears United Kingdom who likes the idea that radical-pair reactions for magnetorecep- to activate birds’ compasses but red light nature evolved two different magneto- tion. But he didn’t have a molecule that jams them, or why birds seem to tell reception systems. “The map sense could could support those reactions until the north from south by measuring changes be magnetite, the compass sense could late 1990s, when researchers discovered in the field’s inclination instead of reading be radical pairs,” he says. It would be the cryptochrome serving as a light sensor the magnetic field directly. (Cryptochrome best of both worlds—or at least the best

DIAGRAM: C. BICKEL/ SCIENCE C. DIAGRAM: in mammalian retinas. Most researchers can’t “feel” magnetic polarity.) As with way to navigate this one. j

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Published by AAAS NEWS | FEATURES

Reading about Blakemore’s work, had what appeared to be a magnetic sense. Now, with a $900,000 grant from Kirschvink wondered which way magnetic In later variations, Baker claimed to find the Human Frontier Science Program, bacteria swim in the Southern Hemisphere: a human compass sense in “walkabout” ex- Kirschvink; Shinsuke Shimojo, a Caltech northward like the Massachusetts microbes, periments, in which subjects pointed home psychophysicist and EEG expert; and or southward toward their own pole, or in after being led on a twisty route; and “chair” Ayumu Matani, a neuroengineer at the Uni- some other direction? He flew to Australia experiments, in which they were asked for versity of Tokyo, are making their best ef- to search stream beds for Blakemore’s anti- cardinal directions after being spun around. fort ever to test Baker’s claims. podal counterparts. They were most abun- Baker performed some of his experiments Baker finds it ironic that his onetime an- dant in a sewage treatment pond near Can- for live television, and he announced some tagonist is now leading the charge for human magnetoreception. “Joe is probably in a bet- ter position to do this than most,” he writes. As for whether he thinks his results still indi- Playing the field Earth’s magnetic field, generated by its liquid outer core, is similar to that of a giant off-axis bar magnet. Its strength ranges from 25 microtesla (µT) near the equator to 60 µT at the poles. cate something real, Baker says there is “not That is weak: An MRI’s field is more than 100,000 times stronger. a shadow of doubt in my mind: Humans can detect and use the Earth’s magnetic field.”

NEXT DOOR to Kirschvink’s magnetics lab Geographic North Polepole Magnetic North Pole is the room where he tests his human sub- jects. In it is a box of thin aluminum siding, known as a Faraday cage, just big enough to hold the test subject. Its role is to screen out electromagnetic noise—from computers, Liquid elevators, even radio broadcasts—that might outer core confound the experiment. “The Faraday cage Equator

is key,” Kirschvink says. “It wasn’t until the on June 23, 2016 last few years, after we put the damned Fara- day shield in, that we went, ‘Wait a minute.’” Kirschvink added it after an experiment led by one of Winklhofer’s Oldenburg col- leagues, Henrik Mouritsen, showed that elec- Magnetic Geographic tromagnetic noise prevents European robins South Polepole South Polepole Other animals, such as sea turtles, possess from orienting magnetically. The stray fields a full map sense, and seem to sense even would probably affect any human compass, Some animals, such as birds, gain a compass by fner variations in strength due to magnetic Kirschvink says, and the noise is most disrup- sensing the feld lines and their inclination. rocks in the crust. tive in a band that overlaps with AM radio broadcasts. That could explain why Baker’s berra. “I just went with a magnet and hand of his results prior to peer review in books experiments succeeded in Manchester, which http://science.sciencemag.org/ lens,” he says. “They’re all over the place.” and popular science magazines—a flair for at the time did not have strong AM radio Sure enough, they swam down toward the the dramatic that rubbed other academics stations. The U.S. Northeast, however, did, South Pole. They had evolved south-seeking the wrong way. which could explain why scientists there magnetite chains. In an email, Baker says there was a “base couldn’t replicate the findings. By then, Kirschvink was a postdoc at hostility” among his U.S. counterparts. In the current setup, the Faraday cage Princeton University, working with biolo- Kirschvink and Gould were among the skep- is lined with squares of wire coils, called gist James Gould. He had also graduated up tics. In 1981, they invited Baker to Princeton Merritt coils. Electricity pulsed through the Downloaded from the food chain of animals. In 1978, he and for a chance to perform the experiments, coils induces a uniform magnetic field run- Gould found magnetite in the abdomen of one whistle stop on a reproducibility tour ning through the center of the box. Because honey bees. Then, in 1979, in the heads of of several U.S. campuses in the Northeast. the coils are arranged in three perpendicular pigeons. Unbeknownst to Kirschvink, across At Princeton and elsewhere, the replica- directions, the experimenters can control the the Atlantic Ocean a young, charismatic tion efforts failed. After Baker claimed in a orientation of the field. A fluxgate magneto- University of Manchester, U.K., biologist 1983 Nature paper that human sinus bones meter to check field strength dangles above named Robin Baker was setting his sights were magnetic, Kirschvink showed that the a wooden chair that has had all of its iron- on the magnetic capabilities of larger, more results were due to contamination. In 1985, containing parts replaced with nonmagnetic WDMAM/CIRES ; (IMAGE) sophisticated animals: British students. In Kirschvink failed to replicate a version of the brass screws and aluminum brackets. a series of experiments, he gathered blind- chair experiment. Kirschvink, Shimojo, and Matani’s idea is SCIENCE folded students from a “home” point onto Although the Manchester experiments to apply a rotating magnetic field, similar a Sherpa mini-bus, took them on a tortu- cast a pall over human magnetoreception, in strength to Earth’s, and to check EEG re- ous route into the countryside, and asked Kirschvink quietly took up Baker’s mantle, cordings for a response in the brain. Finding them the compass direction of home. In pursuing human experiments on the side for one would not reveal the magnetoreceptors Science in 1980, Baker reported something 30 years. He never gave up running students themselves, but it would prove that such a uncanny: The students could almost always through a gauntlet of magnetic coils and ex- sense exists, with no need to interpret often- point in the quadrant of home. When they perimental protocols. “The irritating thing ambiguous human behavior. “It’s a really fan- wore a bar magnet in the elastic of their was, [our] experiments were not negative,” tastic idea,” Winklhofer says. “I’m wondering blindfolds, that pointing skill was thwarted, he says. “But from day to day, we couldn’t re- why nobody has tried it before.”

whereas controls who wore a brass bar still produce them.” The experiments began at the end of 2014. GRULLÓN/ G. BY ADAPTED (DIAGRAM) CREDITS:

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Published by AAAS Kirschvink was human subject No. 1. No. 19 ery researcher in the field of animal naviga- the equivalent of the subject looking to the is Matsuda, on loan from Matani’s lab, which tion. Conferences from years past have dwelt right—there was sharp drop in a waves. The is replicating the experiment in Tokyo with a on navigation by the sun, moon, or stars—or suppression of a waves, in the EEG world, similar setup. Matsuda signs a consent form by sound and smell. But at this year’s meet- is associated with brain processing: A set of and is led into the box by the technician, who ing, in April at Royal Holloway, University neurons were firing in response to the mag- carries the EEG wires like the train of a wed- of London, magnetoreception dominated netic field, the only changing variable. The ding veil. “Are we ready to start?” the tech- the agenda. Evidence was presented for neural response was delayed by a few hun- nician asks, after plugging in the electrodes. magnetoreception in cockroaches and poi- dred milliseconds, and Kirschvink says the Matsuda nods grimly. “All right, I’ll shut the son frogs. Peter Hore, a physical chemist lag suggests an active brain response. A mag- box.” He lowers the flap of aluminum, turns at the University of Oxford in the United netic field can induce electric currents in the off the lights, and shuts the door. Piped into Kingdom, presented work showing how brain that could mimic an EEG signal—but the box is Kirschvink’s nasal, raspy voice. the quantum behavior of the cryptochrome they would show up immediately. “Don’t fall asleep,” he says. system could make it more precise than Kirschvink also found a signal when the ap- Matsuda will sit in the box for an hour in laboratory experiments had suggested. Can plied field yawed into the floor, as if the sub- total blackness while an automated program Xie, a biophysicist from Peking University, ject had looked up. He does not understand runs through eight different tests. In half of pressed his controversial claim that, in the why the a wave signal occurred with up- them, a magnetic field roughly as strong as retina of fruit flies, he had found a complex down and counterclockwise changes, but not Earth’s rotates slowly around the subject’s of magnetic iron structures, surrounded by the opposite, although he takes it as a sign of head. In the others, the Merritt coils are set cryptochrome proteins, that was the long- the polarity of the human magnetic compass. to cancel out the induced field so that only sought magnetoreceptor. “My talk went *really* well,” he wrote jubi- Earth’s natural is at work. These Then, in the last talk of the first day, lantly in an email afterwards. “Nailed it. Hu- tests are randomized so that neither experi- Kirschvink took the podium to deliver his po- mans have functioning magnetoreceptors.” menter nor subject knows which is which. tentially groundbreaking news. It was a small Others at the talk had a guarded response: sample—just two dozen human subjects— amazing, if true. “It’s the kind of thing that’s EVERY FEW YEARS,

the Royal Institute of but his basement apparatus had yielded a hard to evaluate from a 12-minute talk,” on June 23, 2016 Navigation (RIN) in the United Kingdom consistent, repeatable effect. When the mag- Lohmann says. “The devil’s always in the holds a conference that draws just about ev- netic field was rotated counterclockwise— details.” Hore says: “Joe’s a very smart man and a very careful experimenter. He wouldn’t have talked about this at the RIN if he wasn’t pretty convinced he was right. And you can’t Center of attraction Researchers are testing humans for a subconscious magnetic sense by putting them in a dark metal box and applying magnetic fields. say that about every scientist in this area.” Two months later, in June, Kirschvink is in Japan, crunching data and hammering out experimental differences with Matani’s Faraday cage group. “Alice in Wonderland, down the rab- Thin sheets of aluminum prevent bit hole, that’s what it feels like,” he says. outside electromagnetic interference. Matani is using a similarly shielded setup, http://science.sciencemag.org/ except his cage and coils are smaller—just Merritt coils big enough to encompass the heads of sub- When supplied with electricity, coils jects, who must lie on their backs. Yet this create uniform magnetic felds in team, too, is starting to see repeatable EEG the center of the box. effects. “It’s absolutely reproducible, even in Tokyo,” Kirschvink says. “The doors are

opening.” Downloaded from Nonmagnetic chair A wooden chair’s iron-containing Kirschvink’s lifelong quest seems to be on screws are replaced with brass. Wire core the cusp of resolution, but it also feels like a beginning. A colleague in New Zealand says he is ready to replicate the experiment in the EEG machine Southern Hemisphere, and Kirschvink wants Electrodes pick up brain waves, money for a traveling Faraday cage that he which could signal magnetoreception. could take to the magnetic equator. There are papers to write, and new subjects to recruit. Just as Baker’s results ricocheted through the One direction Any direction Active sham research community for years, Kirschvink Applied knows that the path toward getting his idea feld accepted is long, and uphill. But he relishes the thought of showing, once and for all, that there is something Earth’s that connects the iPhone in his pocket—the

SCIENCE feld electromagnetic laws that drive devices and define modernity—to something deep inside Current him, and the tree of life. “It’s part of our evo- One set of Merritt coils produces Using all three sets of coils, a feld Alternating currents cancel out lutionary history. Magnetoreception may be

DIAGRAM: C. BICKEL/ C. DIAGRAM: a feld along the axis of the coils. can be created in any direction. applied feld, leaving only Earth’s. the primal sense.” j

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Published by AAAS Polar explorer Eric Hand (June 23, 2016) Science 352 (6293), 1508-1513. [doi: 10.1126/science.352.6293.1508]

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