Magnetic sensing is a type of sensory perception that has long been studied. Over the past 50 years, scientific studies have shown that a wide variety of living organisms have the ability to perceive magnetic fields and can use information from the Earth’s magnetic field in orientation behavior. Examples abound: salmon, sea turtles, spotted newts, lobsters, honeybees and perhaps us humans can all perceive and utilize geomagnetic field information.
But perhaps the most well-studied example of animal magnetoreception is the case of migratory birds (e.g. European robins (Erithacus rubecula), silvereyes (Zosterops l. lateralis), garden warblers (Sylvia borin)), who use the Earth’s magnetic field, as well as a variety of other environmental cues, to find their way during migration.
The avian magnetic compass is a complex entity with many surprising properties. The basis for the magnetic sense is located in the eye of the bird, and furthermore, it is light-dependent, i.e., a bird can only sense the magnetic field if certain wavelengths of light are available. Specifically, many studies have shown that birds can only orient if blue light is present. The avian compass is also an inclination-only compass, meaning that it can sense changes in the inclination of magnetic field lines but is not sensitive to the polarity of the field lines. Under normal conditions, birds are sensitive to only a narrow band of magnetic field strengths around the geomagnetic field strength, but can orient at higher or lower magnetic field strengths given accommodation time.
A Radical-Pair-Based Avian Compass
Despite decades of study, the physical basis of the avian magnetic sense remains elusive. The two main models for avian magnetoreception are a magnetite-based model and a radical-pair-based model (for review see, e.g., Solov’yov, Schulten, Greiner, 2010). The former suggests that the compass has its foundation in small particles of magnetite located in the head of the bird. The latter idea is that the avian compass may be produced in a chemical reaction in the eye of the bird, involving the production of a radical pair. A radical pair, most generally, is a pair of molecules, each of which have an unpaired electron. If the radical pair is formed so that the spins on the two unpaired electrons in the system are entangled (i.e. they begin in a singlet or triplet state), and the reaction products are spin-dependent (i.e., there are distinct products for the cases where the radical pair system is in an overall singlet vs. triplet state), then there is an opportunity for an external magnetic field to affect the reaction by modulating the relative orientation of the electron spins.
How could a radical pair reaction lead to a magnetic compass sense? Suppose that the products of a radical pair reaction in the retina of a bird could in some way affect the sensitivity of light receptors in the eye, so that modulation of the reaction products by a magnetic field would lead to modulation of the bird’s visual sense, producing brighter or darker regions in the bird’s field of view. (The last supposition must be understood to be speculative; the particular way in which the radical pair mechanism interfaces with the bird’s perception is not well understood.)
When the bird moves its head, changing the angle between its head and the Earth’s magnetic field, the pattern of dark spots would move across its field of vision and it could use that pattern to orient itself with respect to the magnetic field. This idea is explored in detail by Ritz et al (see below). Interestingly, studies have shown that migratory birds exhibit a head-scanning behavior when using the magnetic field to orient that would be consistent with such a picture. Such a vision-based radical-pair-based model would explain several of the unique characteristics of the avian compass, e.g., that it is light-dependent, inclination-only, and linked with the eye of the bird. It is also consistent with experiments involving the effects of low-intensity radio frequency radiation on bird orientation, as suggested by Canfield et al.
The question remains as to where, physically, this radical pair reaction would take place. It has been suggested that the radical pair reaction linked to the avian compass arises in the protein cryptochrome. Cryptochrome is a signaling protein found in a wide variety of plants and animals, and is highly homologous to DNA photolyase. There is some evidence that retinal cryptochromes may be involved in the avian magnetic sense. Detailed analysis of cryptochrome as a transducer for the avian compass would require an atomic-resolution structure of the protein, and unfortunately, no structure of avian cryptochrome is currently available.
However, the structure of cryptochrome from a plant (Arabidopsis thaliana) is available, and the cryptochromes of plants and birds are structurally very similar. Recent experiments by Ahmad et al. (Ahmad, Galland, Ritz, Wiltschko and Wiltschko. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225, 615-624 (2007)) have shown that Arabidopsis seedlings exhibit a magnetic field effect. Processes involved with cryptochrome signaling (such as hypocotyl growth inhibition) are enhanced under a magnetic field of 5 G (as compared with an Earth-strength 0.5 G magnetic field).
Both photolyase and cryptochrome internally bind the chromophore flavin adenine dinucleotide (FAD). In photolyase, the protein is brought to its active state via a light-induced photoreduction pathway involving a chain of three tryptophans. Studies suggest that cryptochrome also is activated by a similar photoreduction pathway.
However cryptochrome’s signalling state has a limited lifetime. Under aerobic conditions, the stable FADH molecule slowly reverts back to the initial FAD state as illustrated in Fig. 3. This process is not well understood and occurs on the millisecond time scale. The cryptochrome back-reaction attracted considerable attention recently due to indications that it may be the key link to avian magnetoreception. In the course of the back-reaction a radical pair is formed between flavin and an oxygen molecule.
