After implantation, the tissue developed blood vessels and became integrated into neuronal networks in the animals’ brains.
Researchers from various disciplines are homing in on the mechanics of magnetoreception, an enigmatic sense that some animals use to navigate the globe.
August 1, 2013|
© INGO ARNDT/GETTY IMAGES
In a small, pitch-dark room at Baylor College of Medicine in Houston, Texas, a homing pigeon stands on a metal platform, its wings restrained in a leather harness and its head held in place by a plastic arm. The platform sits in the center of a 2-foot cubic frame containing electricity-conducting coils—one on every face of the cube. The coils are programmed to precisely deliver magnetic fields from any direction in three-dimensional space.
In an adjacent room cluttered with racks of whirring, bleeping equipment, neuroscientists David Dickman and Le-Qing Wu stare at their computer screens. The pigeon is stock still as it is subjected to a magnetic stimulus directed from hundreds of different positions: the surrounding coils generate a field that incrementally moves through 360° across 4 different “great circle” planes intersecting the center of the bird’s head. Meanwhile, electrodes implanted in the bird’s brain relay the spiking patterns of individual neurons. It takes an hour to record a single neuron’s response to all the differently directed stimuli, and the pigeon gets tired after a few hours, so the researchers can record from no more than 4 neurons per day.
Magnetoreception is a huge mystery. That’s what makes this such an exciting field. We simply don’t know how they do this, so it’s wide open to discovery.
This was Dickman’s and Wu’s daily routine throughout the summer of 2009, as they studied the activity of 329 neurons in the brains of seven different homing pigeons. The researchers were hoping to catch the brain cells in the act of responding to magnetic fields, and thus to better understand how homing pigeons, like many other creatures, use the Earth’s magnetic field for navigation. For months they observed nothing unfamiliar; neurons fired at normal rates, seemingly unaffected by changes in magnetic field. Then, one day, the screen displayed an unusual spiking pattern. “I remember that moment,” says Dickman, who realized then that they’d captured for the first time a neuron responding to information about the bird’s magnetic surroundings. “We were jumping up and down; we broke out the champagne.”
Over the coming weeks and months, Dickman and Wu identified 53 different neurons in the vestibular nuclei, brain regions linked to the inner ear, that are strongly modulated by magnetic stimuli at a range of intensities equivalent to those of the Earth’s magnetic field. Each cell is finely tuned to a field coming from one particular direction. “Let’s say you have a field pointing up from below the bird’s nose to the top of its head at an angle of 45 degrees,” says Dickman. “There is a neuron that is most active in response to that, and least active to a field from the opposite direction, while there is another neuron that responds best to [a field pointing from] the opposite direction.”
They also discovered that the neurons are sensitive to three different aspects of the geomagnetic field: direction, intensity, and polarity. “These are the three components you need to determine your position within the three-dimensional magnetic field,” says Dickman. It is information derived from this tripartite sensitivity, the researchers hypothesize, that homing pigeons might use to pinpoint their position—much as humans use a GPS unit—in addition to using it like a compass, to determine which way they’re heading. “We don’t know that for sure yet,” Dickman adds, “but that’s our guess.”
Although it is a sizable achievement, Dickman and Wu’s discovery does not solve the mystery of magnetoreception. In fact, in at least one way their findings complicate the quest to understand this elusive sixth sense: the study, which was published last year,1 indicates that receptors sensing magnetic information and passing it on to the brain might be found in the inner ear, whereas most researchers have been looking in beaks, snouts, and eyes. A definitive sensor has yet to be found.
Indeed, the question of how animals can detect magnetic fields has proven maddeningly difficult to answer, and scientists are only just beginning to elucidate the physiological mechanisms behind this mysterious extra sense.
“This is a sense that doesn’t exist in humans, so we don’t have any intuitive feeling for what it would be like to perceive magnetic fields,” says Ken Lohmann, a neurobiologist at the University of North Carolina at Chapel Hill, who studies the navigational abilities of sea turtles and other marine animals. “In addition, unlike most other stimuli, magnetic fields go right through biological tissue, so in principle the receptors could be anywhere in the body, and they may not be clustered in one place.”
“[Magnetoreception] is a huge mystery,” says Dickman. “That’s what makes this such an exciting field. We simply don’t know how they do this, so it’s wide open to discovery.”
COURTESY OF MARIANNE HANZLIKFifty years ago, the very idea of magnetoreception was the subject of ridicule. In 1968, Wolfgang Wiltschko, a graduating zoology student at Goethe University in Frankfurt, Germany, demonstrated that the direction in which caged European robins tried to flee in the fall could be changed from its typical southern bearing by using coil systems to simulate magnetic “north” around their enclosure. It was the first real evidence of birds’ internal magnetic compass, but most researchers were skeptical. All previous attempts to prove the existence of such a sense had failed, and many people simply did not believe that it was possible for animals to sense magnetic fields as weak as those generated by the Earth.
Today, it is well known that dozens of species, from migratory birds and sea turtles to spiny lobsters and monarch butterflies, have the ability to sense direction and navigate using the Earth’s magnetic field. Not only does the field provide a compass, allowing animals to orient themselves with regard to north and south; it seems that the Earth’s magnetism can also serve as a kind of map.
© CATHERINE DELPHIAIn the years following his experiments with European robins, Wiltschko teamed up with his wife, Roswitha, also a zoologist at Goethe University, to demonstrate that the birds’ compass sense is based not on the polarity of the Earth’s magnetic field, but on the angles at which the field lines intersect the planet’s surface, known as the inclination. Depending on how the inclination of the field lines change as they fly, the birds perceive whether they are heading poleward or “equator-ward” and gauge their approximate distance between the magnetic equator and the nearest magnetic pole.
More recently, scientists have found that animals also use the Earth’s field lines as magnetic “signposts”—positional information created by unique combinations of field inclination and intensity at specific geographic locations. “What had been overlooked is that those two parameters don’t vary in the exact same direction across the surface of the Earth,” Lohmann says. For example, loggerhead turtles returning to the US coast as juveniles after navigating the North Atlantic gyre—a swirling ocean current—need to adjust their swimming direction at key locations to avoid being swept off course, and Lohmann hypothesized that they might be using the inclination and intensity anomalies to determine where and when to turn.
In 2011 Lohmann and colleagues tested the hypothesis by placing hatchlings in a tank surrounded by magnetic coils and tethering the animals to a swinging metal arm to track their orientation. When hatchlings were exposed to magnetic fields mimicking those found near Puerto Rico or near the Cape Verde Islands, 400 miles off the coast of West Africa—two locations on roughly the same latitude but on opposite sides of the Atlantic—they swam in the appropriate direction to remain within the gyre.2 This was the first evidence that animals can encode information about longitude as well as latitude, and it suggests that the two can be combined in an animal’s brain to pinpoint its specific geographic location.
“We think different areas along the migratory pathway are marked by unique magnetic signatures, and the turtles have evolved responses that are coupled to these signatures,” says Lohmann.
The existence of the signpost sense and the internal compass are now generally accepted, and a number of scientists think that some animals may have both. The sensory and neural mechanisms underlying these senses, however, are more controversial.
In the mid-1970s researchers discovered that bacteria living at the bottom of the ocean contain microscopic magnetite particles arranged in linear chains inside the cells. (See image on right.) These strings of magnetite—an iron-based substance that is sensitive to magnetic fields—align with the direction and inclination of the Earth’s magnetic field lines, pointing the bacteria toward their preferred habitat in the seafloor sediment.
Nearly 3 decades later, researchers used dyes that bind to iron-based minerals to identify similar-looking iron-rich particles in the upper-beak skin of homing pigeons. By 2010, the particles had also been spotted in the upper beaks of chickens, European robins, and garden warblers. These putative magnetite clusters were located in the dendrites of sensory nerve cells, seemingly integrating them with the central nervous system. What’s more, several studies have suggested that the ophthalmic branch of the trigeminal nerve, which in birds carries signals exclusively from the beak, transmits magnetic information to the brain—so all signs pointed to the iron-based particles in the beak being the magnetic sensors.
But that hypothesis was dealt a severe blow last year, with the publication of a study revealing that the particles in question are in fact contained in immune cells called macrophages,3 rather than in sensory neurons, meaning they are not linked to the brain and are therefore unlikely to be magnetic receptors. “That was quite a big upheaval,” says Michael Winklhofer, a geophysicist at Ludwig-Maximilians University in Munich, Germany, “particularly for people looking for magnetite-based receptors in birds, who have to start all over again.”
A few months later, however, Winklhofer and colleagues identified magnetite-containing cells in the snouts of rainbow trout. The researchers suspended olfactory epithelial cells in liquid and placed them under a microscope around which an artificial magnetic field was rotated—a novel method for testing cellular responses to magnetism. Sure enough, some cells actually rotated with the field. Although these magnetic cells were few and far between—roughly 1 in every 10,000 cells in the olfactory epithelium—their sensitivity to magnetic fields was much greater than expected, suggesting that such cells may be capable of detecting small variations in the geomagnetic field.
Studying these rotating cells one by one under a confocal reflectance microscope, Winklhofer and his team noticed that each one contained a structure of iron-rich crystals, most likely magnetite, attached to the cell membrane.4 Magnetite clusters aligning to the magnetic field in nonmotile cells in the olfactory epithelium of trout might put physical pressure on the cell membrane, he proposes. “When the membrane is stretched, mechanosensitive ion channels may open and change the electric potential across the membrane, which then might trigger a nerve impulse.” (See illustration.) For the moment, though, “the missing link in our story is whether these cells are neurons or not,” says Winklhofer.
Nevertheless, he adds, “the new method is a game changer in that it should allow us to get at these cells more easily and study them in more detail.”
And thanks to Dickman and Wu’s 2012 study, which identified magnetically sensitive neurons in the vestibular nuclei, researchers have expanded the search for magnetism receptors beyond the beak and snout to the inner ear. Indeed, earlier this year another group reported the discovery of a membrane-bound, iron-rich organelle in the cochlear and vestibular hair cells of pigeons and other bird species.5
© CATHERINE DELPHIABut some scientists have an alternative explanation for the biophysical mechanism behind magnetic sensing. In the late 1970s biophysicist Klaus Schulten, then a postdoc at the Max Planck Institute for Biophysical Chemistry in Göttingen, Germany, had an inkling that some bizarre chemical reactions he was studying might form the basis of magnetoreception.
Schulten, now at the University of Illinois at Urbana-Champaign, was looking at reactions involving radical pairs. Electrons normally whirl around their atomic nuclei in even numbers and in set orbits, with pairs of electrons spinning on their axes in opposite directions. But light can disrupt this routine by causing electrons to jump to different regions within the same molecule or to neighboring molecules, resulting in pairs of radicals—molecules with unpaired electrons. In this transient state, the unpaired electrons can spin in one of two ways: in the same direction, known as parallel, or in opposite directions, known as antiparallel—and the amount of time they spend in each state can be influenced by magnetic fields.
These two spin states are chemically different—certain reactions can only take place when unpaired electron spins are parallel and others only when they are antiparallel. Magnetic fields can influence the outcome or speed of chemical reactions involving radical pairs by causing flips between the two spin states and by controlling the relative amount of time the molecular players spend in each. Such fluctuations in reactions could in turn provide a chemical cue about the magnetic field, which could be picked up by a sensory neuron, Schulten thought.
“I had this wonderful proof of a biochemical reaction . . . that was affected in very weak fields, so I thought, well, maybe that’s the internal compass the biologists were looking for,” he says.
© ANDREW_HOWE/ISTOCKPHOTO.COMIn 1978, Schulten submitted a paper detailing his theory to Science—and promptly received a rejection note that read, “A less bold scientist would have designated this piece of work for the waste paper basket.” Undeterred, Schulten published in an obscure German journal. Since the formation of radical pairs in vitro required light, he thought the most likely site for the interaction in a living creature would be the eye. But at the time, there was no known photoreceptor in the eye capable of forming radical pairs.
That changed in 1998, with the discovery of a blue-light photoreceptor protein that generates radical pairs when exposed to light. Known as a cryptochrome, the protein has since been identified in the retinal tissue of several migratory birds and of other animals, including humans. Assuming that the products of radical-pair reactions in cryptochromes could in some way affect the sensitivity of light receptors in the retina, Schulten and Thorsten Ritz, a biophysicist now at the University of California, Irvine, argued in a theoretical paper published in 2000 that the modulation of these reactions by magnetic fields would affect the visual system of birds to provide compass cues.6 (See illustration.)
In the intervening years, researchers have produced reams of circumstantial evidence in support of this idea. In 2004, for example, Ritz and the Wiltschkos showed that high-frequency radio waves, known to disrupt the spin behavior of radical pairs in vitro, stopped robins from navigating.7 Three years later, Henrik Mouritsen, a neurobiologist at the University of Oldenburg in Germany, and colleagues showed that a cryptochrome isolated from the garden warbler produces long-lived radical pairs.8 And in 2011, the Wiltschkos showed that one of the four known bird cryptochromes is found in all ultraviolet/violet cone cells in the retinas of both European robins and chickens—specifically, in the stacked membrane discs of the photosensitive outer segment of the cone cell, which also contains the visual pigments.9
“What we have is a lot of evidence that the necessary conditions for this hypothesis to be true are in place,” says Ritz. “But then you need to connect these findings with the behavior of the animals, and that’s where we’re faced with a big gap.”
Some of the most compelling evidence for the importance of cryptochromes came in 2008, when Steven Reppert, a neurobiologist at the University of Massachusetts Medical School in Worcester, and colleagues showed that wild-type fruit flies responded to magnetic fields under full-spectrum light—they could even be trained to follow artificial magnetic cues to find food—but when the team blocked the particular wavelengths of light to which cryptochromes are sensitive, the same flies could no longer detect magnetic stimuli. Furthermore, mutant flies lacking the gene for cryptochrome did not respond to magnetic fields even under full-spectrum light,10 and in 2010, Reppert rescued the magnetosensory ability in mutant flies by transfecting them with two different cryptochrome genes from monarch butterflies.11 “The deletion and replacement experiments really said that the cryptochrome is an essential feature of the light-dependent magnetic sensing system in Drosophila,” he says.
But the case is far from closed. First of all, Reppert’s flies were exposed to magnetic fields 8 to 10 times stronger than the one emanating from the Earth. Moreover, Reppert says that knockout experiments on migratory animals would provide more compelling evidence—and it’s important that the results are replicated with individual animals that routinely reproduce magnetic orientation behavior in the lab rather than the population-based studies his group performed with fruit flies. Unfortunately, that’s unlikely to be achieved with birds or turtles in the near future because of the difficulties associated with creating gene knockouts and transgenic lines in such animals, but Reppert says his group is “making tremendous progress” with monarch butterflies, whose genomes can be manipulated.
Proponents of the cryptochrome theory also have yet to show that retinal neurons respond to variations in Earth-strength magnetic fields; to elucidate the signaling pathways that connect cryptochromes to the nervous system; or to explain how animals that possess this visually mediated compass perceive the information it provides—though some have speculated that the magnetic field might appear as patterns of light and shade superimposed on the animals’ vision.
© CATHERINE DELPHIADespite recent progress, the field of magnetoreception has been hindered by the fact that many findings have proven very difficult to replicate, says Mouritsen. “The field has been slowed down by a number of claims that have turned out not to be right,” he says. One reason for this irreproducibility is that humans lack the magnetic sense, so researchers are susceptible to misinterpreting artifacts as real results. “It will be helped a lot if everybody would start doing double-blind experiments with very carefully controlled and measured stimuli,” adds Mouritsen. “If that happens we would move forward much faster.”
As it stands, there are several hypotheses supported by strong, albeit not yet conclusive, data. Most researchers in the field agree that the compass sense is likely seated in cryptochromes within the eye, and many are convinced that there is another sense, most likely a signpost sense, passed through the trigeminal nerve and probably based on some sort of iron-containing, magnetism-sensing cells in beaks or snouts. Then there is Dickman and Wu’s idea: that both of these abilities may rely on receptors in the inner ear.
Moreover, Dickman points out, these mechanisms may not be mutually exclusive. “It could be that there are multiple [receptor] sites that may be providing different sorts of information about different aspects of the magnetic field, which then converge in the brain,” he says.
Although the researchers who have come together from a diverse range of disciplines to unravel the secrets of magnetoreception are still some way from their final destination, there is a palpable sense of momentum. “It’s really tough work, but it’s also exciting,” says Winklhofer, “because everybody wants to be the first to demonstrate how this extra sense works.”
August 1, 2013
In the absence of any theoretical reasons or definitive empirical data, one would be well advised to be extremely skeptical about the existence of "magnetoreceptors" in any organism.
August 6, 2013
This is a very interesting article for me!
I found here on The Scientist a set of articles about the capacity of the living organisms orientation trough bio-magnetic sensors.
Even spatial communication affects people every day, we can break the barriers in spatial interactions and bio-communications understanding only by introducing interdisciplinary studies. The fluidity of space constraints is an integral part of spatial magnetic communication, but they are rigid in accordance with the signal frequency.
Because it's very low frequency, the magnetic mental signal may radiate as far as 200 feet around the living body and it hasn't got the capacity to penetrate the space at long distances.
To really penetrate the space at long distance we need very high frequency equipments as exist in telecommunications.
Have you looked at the mitochondria physical structure through the eyes of the engineer specialized in spatial communications?
I am sure you have not and, please, do not :"be extremely skeptical about the existence of magnetoreceptors in any organism" (T S Raman comment)
"The field of magnetoreception has been hindered by the fact that many findings have proven very difficult to replicate" (Mouritsen), because the bio-magnetoreceptors are controled by the brain. I am sure that there is an internal communication channel between the brain and the bio-antennas as exist in the satellite telecommunications systems (LMSC - learning management system control). Please, read the result of my research about mitochondrial DNA similitude with "magnetoreceptors":
Abstract: Brain and soul storming - The necessary and sufficient processes to a well function of the human body are meticulous arranged by specific organizational cells, so called process bio-managers, using interconditioned procedures, transmitted through three ways of communication: chemical or “protein channel”, electrical or “ion channel” and mitochondrial or “EMF wireless channel”. The third type is out of the visible and measurable spectrum and raises a new challenge to the scientist. For this type of bio communication we bring a new theoretical hypothesis, based on the managerial multidisciplinary analysis of a cybernetic model proposed by us, by simulating the human body function with the virtual computerized system based on the management of its total knowledge and its perfect quality way of function. The main bricks used for this virtual construction are: the brain, as main bio-processor, and Eve mtDNA and Adam mtDNA, as bio-antennas. This assembly of the total knowledge, build with “brain reasoning, biological feeling, and unlimited soul feeling”, is called by us “main decision triangle, IQ-EQ-CQ”. The main principle of the management of the total knowledge imposes us to not neglect the information produced by man during the time, even if it seems creasy at the beginning (see brainstorming definition). Because in the natural fertilisation the spermatozoids are naturally equipped with the paternal mtDNA (it looks like reflex klystron power amplifier, KPA = a veritable main bio-GPS), we consider that the paternal mitochondria DNA have a very important role in the evolution of the human being life quality and we have developed a new hypothesis, “Adam mtDNA theory”, in addition to “Eve mtDNA theory”. Keywords: brain, mitochondria, maternal, paternal.
August 6, 2013
No living organisms have animate nagnetosensors, and none except humans, can navigate by using the earth's magnetic field, which humans can do only provided they fashion purchace, brrow, or steal an inanimate magnetic compass; which they can do only because they alone have human "brains"!
Those still chasing after the phantom of animate magnetosensors have only managed to innundate science with a huge amount of worthless garbage
August 7, 2013
This is an excellent article and helps explain why so many birds are having problems in navigating near sources of manmade electromagnetic radiation and fields.
Another article looking at magnetoreception in plants would be interesting. Thigmonastic movements in response to environmental stimulus, foliar spiral direction and influences on electro-signalling are topics which spring to mind.
August 13, 2013
Why are scientists so sure that humans have no magnetic sensing capabilities?
August 26, 2013
How do various sub-human animals use the earth's magnetic-field to navigate? They don't!
August 29, 2013
Re Rosenbio and Roy Niles comments:
One can postulate a negative, but last time I checked, proving a negative is not what we do in science.
Also, each scientist speaks for her/him-self. Not for all of us.
There was a time when most people thought the world was flat and that nothing as small as a microbe could harm a human.
May 10, 2014
This year there is more substantial evidence emerging of quantum effects in the biological processes of photosynthesis and magnetoreception e.g
Perhaps rather than just rejecting the idea of magnetoreception as a quantum process, we should be looking at whether there is any potential cross fertilisation of data and theory across the two processes.
For example it is increasingly being recognised that photosynthesis was evolved in plants through endosymbiosis involving photosynthetic bacteria.
So is it also possible that various species have evolved to be magnetoreceptive or magnetosenstive due to a form of endosymbisosis with magnetotactic bacteria?
"The widespread distribution of organisms (bacteria through higher vertebrates) that are magnetoreceptive argues that this sensory modality evolved prior to the radiation of the animal phyla and shares a common origin. In microorganisms, magnetoreception solves the problem of the random walk induced by Brownian motion, as magnetic orientation energy is typically a factor of 10 or more than background trend energy KT. Swimming along the magnetic field lines allow them to stay at the oxygen gradient near the mud/water transition. As the early stage metazoans also lived in an aqueous environment, navigation abilities ought to have been selected for strongly. Thus it is proposed that the biophysical mechanisms for magnetoreceptive transduction in the nervous system have evolved as ancestral traits common to all animals and not as separate entities between groups" see JL Kirschvink
It has already been suggested that Cry 1 and 2 may have originated from an endosymobiotic ancester of modern day alphaproteobacteria.
What if the same was true of the production of structures and processes supporting biomagnetite based magnetoreception.
If there was an endosymobiotic connection, I would suggest that mitrochrondria might play a role.
It may also be of interest to know that a recent scientific paper has found evidence of alphaproteobacteria in the brain (across humans, primates, and non primates), so that endosymbiotic process may still be taking place.