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A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception?
John B. Phillips, Rachel Muheim, Paulo E. Jorge


In terrestrial organisms, sensitivity to the Earth's magnetic field is mediated by at least two different magnetoreception mechanisms, one involving biogenic ferromagnetic crystals (magnetite/maghemite) and the second involving a photo-induced biochemical reaction that forms long-lasting, spin-coordinated, radical pair intermediates. In some vertebrate groups (amphibians and birds), both mechanisms are present; a light-dependent mechanism provides a directional sense or ‘compass’, and a non-light-dependent mechanism underlies a geographical-position sense or ‘map’. Evidence that both magnetite- and radical pair-based mechanisms are present in the same organisms raises a number of interesting questions. Why has natural selection produced magnetic sensors utilizing two distinct biophysical mechanisms? And, in particular, why has natural selection produced a compass mechanism based on a light-dependent radical pair mechanism (RPM) when a magnetite-based receptor is well suited to perform this function? Answers to these questions depend, to a large degree, on how the properties of the RPM, viewed from a neuroethological rather than a biophysical perspective, differ from those of a magnetite-based magnetic compass. The RPM is expected to produce a light-dependent, 3-D pattern of response that is axially symmetrical and, in some groups of animals, may be perceived as a pattern of light intensity and/or color superimposed on the visual surroundings. We suggest that the light-dependent magnetic compass may serve not only as a source of directional information but also provide a spherical coordinate system that helps to interface metrics of distance, direction and spatial position.


  • J.B.P. was supported by grant IOB 06-47188, and P.E.J. by grant IOB 07-48175, from the National Science Foundation, USA. R.M. was supported by a junior research position by the Swedish Research Council.

  • Supplementary material available online at http://jeb.biologists.org/cgi/content/full/213/19/3247/DC1

  • Glossary

    Light-dependent magnetic compass (LDMC)
    A sensory mechanism that derives directional (i.e. compass) information from the Earth's magnetic field that is altered by certain wavelengths and intensities of light, and/or abolished in total darkness.
    Radical pair mechanism (RPM)
    A biophysical mechanism proposed to explain the properties of the light-dependent magnetic compass in which the alignment of an Earth-strength magnetic field influences a photo-induced electron transfer (redox) reaction that forms radical intermediates (‘radical pair’).
    Light-sensitive flavoproteins that serve as photopigments in a variety of non-visual light responses in both plants and animals, affecting growth and development, entrainment of circadian rhythms and pupillary responses. Crytochromes also function as non-light-sensitive components of the mammalian circadian clock.
    A class of flavoproteins in the same gene family as the cryptochromes that carry out light-dependent DNA repair.
    Flavin adenine dinucleotide (FAD)
    Cofactor that absorbs light and participates in light-dependent redox reactions in a variety of flavoproteins, including cryptochromes and photolyases.
    Singlet state
    A quantum state (S) in which the electron spins are antiparallel so the dipoles cancel out and the total spin moment is zero. In photo-excited electron transfer (redox) reactions, the radical pair is generally formed in an overall singlet state in which the spins of the unpaired electrons are antiparallel. When the radical pair is in an overall singlet state, an unpaired electron can back transfer to the original donor molecule, decreasing the persistence of the radical pair.
    Triplet state
    A set of quantum states each of which sums to S=1. In a radical pair, this occurs when the spins of the unpaired electrons are parallel and, thus, cannot occupy the same orbital, preventing back transfer of one electron to the original donor molecule, increasing the persistence of the radical pair. The triplet state is generally lower in energy than the singlet state.
    Magnetite-based magnetic compass (MBMC)
    A magnetoreception mechanism containing particles of the mineral magnetite that provides directional (i.e. compass) information.
    Pulse remagnetization
    Exposure to a brief, high-intensity magnetic pulse that can remagnetize particles of magnetite with stable magnetic moments, used to test for certain types of magnetite-based magnetoreception mechanisms. This treatment has no lasting effect on a light-dependent magnetic compass mediated by a radical pair mechanism.
    Redox partner
    Atom or molecule forming one member of a redox pair that undergoes an electron transfer reaction. As a consequence of electron transfer, one partner is oxidized (loses an electron) and the other is reduced (receives an electron).
    Head direction cells (HDCs)
    Neurons found in many parts of the brain that fire when the animal's head points in a specific direction, regardless of location. HDCs tend to be narrowly tuned, with firing rates approaching zero at approximately 45 deg on either side of the preferred direction.
    Subicular place cells (SPCs)
    Neurons in the subiculum of rats that fire when the animal occupies a specific spatial location or locations (‘firing fields’) relative to its surroundings. Properties of SPCs differ from the better known hippocampal place cells, which generally have a single firing field that changes unpredictably when the animal moves to new surroundings and is independent of the direction the animal is facing. By contrast, firing fields of SPCs show some variation in firing depending on the animal's compass heading, may consist of two or more subfields, retain the same general shape(s) and alignment(s) in different surroundings, and expand or contract to fill the animal's field of view.
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