Physics of the Senses 101: Magnetoreception or a Sense without a Receptor?

Foreword

Human beings are provided with a variety of senses that help them navigate the world around them, including five basic ones: sight, hearing, touch, smell, and taste. The organs associated with each of the latter report on certain sensations to the brain, which then translates them into understandable information, via a complex, yet fascinating process. Bright colours, a loud thud, an acute pain, a familiar flavour on the tongue or a sweet smell that tickles the nose – all these stimuli are put together into one big picture for us to identify our surroundings. However, while these systems are remarkably sophisticated ones in humans, some animals have super sensors. Felines are well-known for their nocturnal vision, elephants have the most powerful nose of the animal world, while bats rely on sound waves to hunt. Magnetoreception – the ability to detect the Earth’s magnetic field, is even considered a sixth sense that birds, along with certain mammals, reptiles, and fish, are gifted with.

The Physics of the Senses 101 series offers to explore the physical processes that make up each sense, including the so-called sixth sense, and to explain the extent to which they grant certain species 'super-capacities'.

1. Physics of the Senses 101: Visual Perception or Sight

2. Physics of the Senses 101: Auditory Perception or Hearing

3. Physics of the Senses 101: Haptic Perception or Touch

4. Physics of the Senses 101: Olfaction or Smell

5. Physics of the Senses 101: Gustatory Perception or Taste

6. Physics of the Senses 101: Magnetoreception or a Sense without a Receptor?

Magnetoreception, described as ‘perhaps the least understood’ sense that evolution equipped life with by researchers Nordmann, Hochstoeger and Keays (Nordmann et al., 2017, p.1), is the faculty to derive information from the Earth’s magnetic field and use it for biologically relevant purposes (Winklhofer, 2010). While an array of evidence supports the fact that animals, insects or even bacteria rely on magnetoreception for orientation and navigation, the hypothesis that humans possess the same ability is still open to debate: ‘[f]or decades, there’s been a back-and-forth between positive reports and failures to demonstrate the trait in people, with seemingly endless controversy’ (Shimojo et al., 2019, p.1). Recent research, however, has established that the human brain is able to pick up on Earth’s magnetic fields (Wang et al., 2019). The extent of it, its use, or even the exact cells, molecules and mechanisms mediating sensory transduction of magnetoreception remain unclear (Nordmann et al., 2017). The final article of this series will therefore start by outlining the current knowledge of this intriguing sense, before exploring its existence in humans and other species such as birds, dogs, bees, and sharks.

Figure 1: Magnetic Sense of Robins Illustration (Pollack, 2012)

To start with, the stimulus involved in magnetoreception is the geomagnetic field, which is believed to arise from the motion of the Earth’s conducting fluid core. It is a vector quantity made up of three distinct geophysical components: an inclination – the angle between the field lines emerging from the planet with respect to the Earth’s surface, a declination – the angle of the field lines with respect to the true geographic North, and an intensity – the density of the field lines (Nordmann et al., 2017). Drawing on existing precepts in sensory biology which were detailed in previous articles, Nordmann, Hochstoeger and Keays attempt to address the mystery of magnetoreception using three different theories.

The first one is the existence of a mechanically sensitive magnetoreceptor. Indeed, ‘[i]n many sensory systems, the receptor proteins involved in transducing the signal are directly influenced by the incoming stimulus and undergo structural rearrangements upon activation’ (Nordmann et al., 2017, p.3). The issue is that proteins exhibit very low magnetic susceptibility to due their composition (primarily carbon, nitrogen and oxygen). Therefore, for a membrane protein to undergo a conformation change, a ferromagnetic structure made of an iron oxide would be required. In theory, this is possible since numerous species can form biogenic magnetite. For instance, the Mam proteins in magnetotactic bacteria synthesize magnetite crystals, which serve as an internal compass needle guiding their ‘swimming along the incline of the magnetic field vector to deeper waters’ (Nordmann et al., 2017, p.4). However, research has so far failed to detect the presence of magnetite in vertebrates, and ‘the available sequence data suggest there are no genuine homologues of the Mam proteins in eukaryotic magnetosensitive species’ (Nordmann et al., 2017. p.4).

Figure 2: The Earth's Magnetic Field (Gruillon, 2016)

The second theory is that the geomagnetic field modulates biochemical reactions in receptor cells that are analogous to the visual pigments detecting light. Indeed, behavioural data demonstrated that European robins require light in the blue-green spectrum for magnetic orientation, suggesting that the geomagnetic field influences the spin state of light-induced radical pairs, and thus the reactivity of certain molecules (Nordmann et al., 2017). As Nordmann and his colleagues further explain, a number of studies support this concept by showing that ‘low-intensity broadband electromagnetic fields (which influence electron spins) disrupt magnetic orientation’ (Nordmann et al., 2017, p.7) in vertebrates. Nevertheless, it is still unclear which cells would be involved in a light-dependent chemical compass.

Lastly, the detection of magnetic fields could rely on accessory structures converting it into another stimulus, similar to those associated with the auditory system to convert airborne sound waves into spring tension in hair cells.

‘As magnetism and electricity are inseparable, it is conceivable that a secondary structure might convert information about the Earth's magnetic field into an electric stimulus. This proposition, which reflects Faraday’s law of electromagnetic induction, predicts that movement of an animal in a fixed magnetic field would induce an electromotive force in a conductor’ (Nordmann et al., 2017, p.9).

This idea is based on the existence of electroreceptors in ocean animals, as well as on the possibility that electromagnetic induction could also occur in the ear canals of birds. The limitation of this theory lies in the relatively small amount of ‘behavioral, anatomical, physiological, or experimental data that directly supports it’ (Nordmann et al., 2017, p.10).

Figure 3: Three Mechanisms Proposed (A) Mechanically sensitive magnetite-based magnetoreceptor. (B) Light-sensitive chemical-based magnetoreceptor. (C) Based on electromagnetic induction. (Nordmann et al., 2017)

Nordmann’s paper outlines multiple reasons why the current understanding of magnetoreception remains rudimentary. For example, the weakness of the Earth’s magnetic field was a long-lasting argument to dismiss the possibility of detecting it altogether. Also, magnetoreceptors, if they exist, would be very challenging to locate in an animal’s body because magnetic fields can freely penetrate biological tissue. Moreover, the usual electrophysiological methods applied in sensory neurobiology make the interpretation of data challenging in the case of the magnetic sense due to the risk of induction in recording electrodes. Finally, unlike for other senses, experimental approaches can’t be based on instinctive concepts due to the lack of active perception of the Earth’s magnetic field in humans (Nordmann et al., 2017). Professor Kirschvink from the California Institute of Technology indeed explains that there is evidence for magnetic sensation in our animal ancestors, and that this ability is currently taking place in the subconscious human mind (Shimojo et al., 2019). Besides, strong, artificial magnetic fields are found throughout the modern world, and exposure to them when, for example, using a headset, sitting in an airplane cabin or having an MRI scan could further affect magnetoreception (Human Frontier Science Program, n.d.).

The question of the human magnetic sense has been controversial for decades, despite positive results dating back to the 1980s. Indeed, Baker points out that experiments at Manchester University demonstrated the existence of a ‘non-visual ability to orient and navigate based, at least in part, on magnetoreception’, yet many others continued to not offer support of this view, in what he calls an ‘unexplained feature of the literature of human magnetoreception’ (Baker, 1987, p.1). Nevertheless, there have been recent breakthroughs in this field of research. Kirschvink and his team discovered that transduction of the geomagnetic field was evidenced from alpha-band activity in the human brain (Wang et al., 2019). By placing thirty-four volunteers in a six-sided electromagnetic cage, using aluminium walls to avoid interference and an electroencephalogram machine to measure brain waves, the team discovered that certain scenarios triggered a drop in the alpha-band, which is linked to information processing. Although the strength of the responses varied hugely among participants, such result suggest that the brain is able to detect changes in the magnetic environment. The scientists found no sign that the magnetoreceptive system could be linked to human consciousness, however, their tests rule out electrical induction, free-radical quantum compass mechanisms, or the presence of artefacts as explanations (Wang et al., 2019). Instead, they state that ‘[f]erromagnetism remains a viable biophysical mechanism for sensory transduction and provides a basis to start the behavioral exploration of human magnetoreception’ (Wang et al., 2019, p.1).

Figure 4: Electromagnetic Cage used to Search for a Subconscious Magnetic Sense (Nordmann et al., 2017)

On the other hand, a 2022 study established for the first time that the human magnetic sense is mediated by a light-dependent and magnetic field resonance-dependent mechanism. Researchers found, by combining the rotary chair method with a two-alternative forced choice paradigm, that magnetic orientation of subjects was sensitive to the incident light’s wavelengths and ‘critically dependent on blue light reaching the eyes’ (Chae et al., 2022, p.1). ‘The magnetic response to blue light approximately matches the absorption spectrum of fully oxidised FAD [Flavid Adenine Dinucleotide] in cryptochrome […] suggesting that cryptochromes might be a promising magnetoreceptor in humans’ (Chae et al., 2022, p.5). The researchers explain that at first sight, their principal result is difficult to reconcile with Kirschvink’s study, which pointed towards a light-independent magnetite-based mechanism (Wang et al., 2019). However, the two, very different experimental methods could be probing different receptors, compared to the magnetoreceptive system in birds, ‘which are thought to have radical pairs in the eyes (for direction sensing) and magnetite elsewhere (for intensity sensing)’ (Chae et al., 2022, p.5).

Regarding the rest of the animal kingdom, evidence accumulated suggests that a tremendous number of species exploit the Earth’s field to guide their movements, of which migratory birds are the most famous example. These birds can use two kinds of information from the geomagnetic field for navigation: the direction of the field lines as a compass and magnetic intensity as a component of the navigational ‘map’’ (Wiltschko, 2019, p.1). As explained earlier, they sense direction via radical pair processes formed by cryptochromes in the eyes, which is then transmitted by the optic nerve to the brain. The intensity appears to be perceived by magnetite-based receptors in the beak, which is transported by the ophthalmic branch of the trigeminal nerve to the trigeminal ganglion. The visual and haptic systems therefore seem to oversee the interpretation the signals (Wiltschko, 2019). Proof was lacking that the cryptochromes truly possess magnetic sensitivity until Xu’s 2021 study, which provided in vitro evidence that the protein ErCRY4, located in the eyes of European robins, exhibits the right physical properties to be the elusive magnetosensor (Warrant, 2021). In vivo experiments will need to be carried out to definitely establish the pivotal importance of this cryptochrome (Warrant, 2021), behind the migratory birds’ ability to sense the compass direction of the magnetic field, which allows them to travel long distances, determine their position on the Earth, and also gain weight when necessary (Mouritsen, 2015).

Figure 5: Magnetoreception in Animals (Delphia, 2013)

Other behaviours linked to magnetoreception include excremental habits in dogs as well as foraging in bees. Firstly, a team of German and Czech scientists observed seventy dogs of thirty-seven different breeds and found that they prefer to defecate with their bodies aligned along the north-south axis (Hart et al., 2013). Magnetic alignment, ‘i.e., spontaneous alignment of the body with respect to the magnetic field lines, when other determinants (e.g. wind direction, sun position, curiosity) of the body position are negligible’ (Hart et al., 2013, p.1), has been found in other mammals such as resting cattle when grazing, roe deer, red deer, and hunting red foxes (Hart et al., 2013). To continue, in the case of bees, their suspected magnetoreceptors are the iron granules in their abdomens (Liang et al., 2016). They navigate thanks to an array of visual clues as well as directional information from the sky compass, to which they add geomagnetic cues for orientation. Cryptochromes are also present in the bees’ brains, as it has been confirmed to be the magnetoreception in most other insects such as fruit flies, blowflies, cockroaches and butterflies. However, experiments show that bees also respond to changes in the magnetic azimuth in totally dark environments, while cryptochromes cannot function without blue light excitation, which ‘may be the reason for the development of the magnetite-based magnetoreception in the honey bee’ (Liang et al., 2016, p.4). These superparamagnetic particles are thought to expand or contract in an orientation-specific manner and to relay the signal via the cytoskeleton (Hsu et al., 2007). Other studies have linked the honey bees’ magnetosensitivy to comb building and homing orientation as well as foraging (Lambinet et al., 2017). This ability, which seems essential to their survival, could be the subject of future experiments since researchers believe bees could become the model organisms for studying magnetoreception (Johnston, 2017).

Lastly, new evidence suggest that sharks use their magnetic sense to navigate, especially for homeward orientation, and possibly to maintain population structure. Indeed, ‘[m]igration is common in marine animals and use of the map-like information of the Earth’s magnetic field appears to play an important role’ (Keller et al., 2021, p.2881). Wild-caught bonnetheads were subjected to magnetic displacement experiments. Specifically, they were placed in tanks, around which a structure was built to produce vertically and horizontally manipulable electromagnetic fields with variable poles and intensity. The geomagnetic conditions of three different places were mimicked using this set up: the control location of their capture, a location 370 miles north and another 370 miles south. In similar intensity and arrangement conditions to their home range, the bonnetheads didn’t exhibit any apparent preferred swimming direction, whereas in the tweaked magnetic conditions of the southern location, they tended to orient themselves towards home. In the scenario of the northern location, which the sharks would never experience in the wild for it corresponded to the magnetic conditions of Tennessee, they exhibited no statistically significant heading. These tests not only demonstrated the sharks’ ability to orient themselves according to the magnetic field, but it also suggests that they also must have a magnetic map sense to point towards home (Keller et al., 2021). The study also looked at the bonnetheads’ mitochondrial DNA, which is female-inherited, to compare genetic variation among various subpopulations with their different living conditions. Instead, the researchers found a greater correlation between divergence in DNA and the sharks’ home areas’ magnetic signature than the physical distance or differences in temperature. This supports the idea the female sharks’ perception of home may be at least partly defined by local magnetic fields (Keller et al., 2021). Expanding the knowledge of marine species’ perception of their environment could therefore be key in building more responsible offshore infrastructures.

Figure 6: Moral Compass Illustration (Pink Polish Design, n.d.)

To summarize, magnetoreception remains a puzzling sense whose study was refuted for decades because of the weak nature of the Earth’s magnetic field, and still suffers from scepticism in academic literature despite mounting evidence of its existence. Studies have indeed emerged in the recent years, proving that humans have not completely lost the ancestral system that detects magnetic information. Narrowing down the exact biophysical concepts involved in magnetoreception is an ongoing challenge, however, two theories are currently debated: the presence of a magnetite-based receptor or a light-sensitive, magnetic resonance-dependent mechanism. It is important to note that both concepts are not incompatible and are found combined in multiple migratory bird species. While it is unclear whether modern humans could consciously hone this sense and use it for navigation, orientation, or food location, these are abilities common to an array of species from invertebrates, insects, mammals and even microorganisms. Future studies could provide valuable insight into their lives in the wild or even bring to light new possibilities for humankind. Magnetoreception is therefore a fascinating, growing field of research, and as Nordmann pointed out: ‘solving this scientific mystery will require the development of new genetic tools in magnetosensitive species, coupled with an interdisciplinary approach that bridges physics, behavior, anatomy, physiology, molecular biology, and genetics’ (2017, p.11).

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