A New Type of Radical-Pair-Based Model for Magnetoreception

Stoneham, A. M.; Gauger, Erik M.; Porfyrakis, Kyriakos; Benjamin, Simon C.; Lovett, Brendon W.

doi:10.1016/j.bpj.2012.01.007

Cited by 39 publications

(40 citation statements)

References 48 publications

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“…Spin relaxation much slower that 1 μs has been invoked before to explain the apparent sensitivity of birds to weak (nanotesla) monochromatic radiofrequency fields (21,26,53,54). The problem with this proposal is that if there is no possibility of a spike, a coherence time of 1-2 μs is sufficient to achieve the optimum compass performance so that there would be no evolutionary pressure to prolong relaxation times beyond this point (55,56). Because the spike only emerges when the coherence time exceeds 1 μs, its presence could explain why slow relaxation might have evolved.…”

Section: Discussionmentioning

confidence: 99%

The quantum needle of the avian magnetic compass

Hiscock

Worster

Kattnig

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

168

223

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Migratory birds have a light-dependent magnetic compass, the mechanism of which is thought to involve radical pairs formed photochemically in cryptochrome proteins in the retina. Theoretical descriptions of this compass have thus far been unable to account for the high precision with which birds are able to detect the direction of the Earth's magnetic field. Here we use coherent spin dynamics simulations to explore the behavior of realistic models of cryptochrome-based radical pairs. We show that when the spin coherence persists for longer than a few microseconds, the output of the sensor contains a sharp feature, referred to as a spike. The spike arises from avoided crossings of the quantum mechanical spin energy-levels of radicals formed in cryptochromes. Such a feature could deliver a heading precision sufficient to explain the navigational behavior of migratory birds in the wild. Our results (i) afford new insights into radical pair magnetoreception, (ii) suggest ways in which the performance of the compass could have been optimized by evolution, (iii) may provide the beginnings of an explanation for the magnetic disorientation of migratory birds exposed to anthropogenic electromagnetic noise, and (iv) suggest that radical pair magnetoreception may be more of a quantum biology phenomenon than previously realized. magnetic compass | magnetoreception | migratory birds | quantum biology | radical pair mechanism M igratory birds have a light-dependent magnetic compass (1-4). The primary sensory receptors are located in the eyes (2, 3, 5-7), and directional information is processed bilaterally in a small part of the forebrain accessed via the thalamofugal visual pathway. The evidence currently points to a chemical sensing mechanism based on photo-induced radical pairs in cryptochrome flavoproteins in the retina (8-18). Anisotropic magnetic interactions within the radicals are thought to give rise to intracellular levels of a cryptochrome signaling state that depend on the orientation of the bird's head in the Earth's magnetic field (8,9,19). In support of this proposal, the photochemistry of isolated cryptochromes in vitro has been found to respond to applied magnetic fields in a manner that is quantitatively consistent with the radical pair mechanism (15). Aspects of the radical pair hypothesis have also been explored in a number of theoretical studies, the majority of which have concentrated on the magnitude of the anisotropic magnetic field effect (9,10,16,17,(19)(20)(21)(22)(23)(24)(25)(26)(27). Very little attention has been devoted to the matter we address here: the precision of the compass bearing available from a radical pair sensor (28).To migrate successfully over large distances, it is not sufficient simply to distinguish north from south (or poleward from equatorward) (29). A bar-tailed godwit (Limosa lapponica baueri), for example, was tracked by satellite flying from Alaska to New Zealand in a single 11,000-km nonstop flight across the Pacific Ocean (30). A directional error of more than a few degre...

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Section: Discussionmentioning

confidence: 99%

The quantum needle of the avian magnetic compass

Hiscock

Worster

Kattnig

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

168

223

View full text Add to dashboard Cite

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“…The isoalloxazine ring of the light-responsive chromophore in cryptochromes, the flavin adenine dinucleotide, preferentially absorbs light polarized parallel to the ring formation (13,28). Consequently, the population of cryptochrome receptors with their transition dipoles aligned parallel to the e-vector of light will be preferentially excited, i.e., polarization selected (13,23,24). Recent models suggest that partially or fully polarized light enhances the photoselection effects on the radical-pair magnetoreceptors described above (13).…”

Section: Significancementioning

confidence: 99%

“…Recent models suggest that partially or fully polarized light enhances the photoselection effects on the radical-pair magnetoreceptors described above (13). Assuming that the lens, ocular media, or retinal tissue in the avian eye do not significantly depolarize the incoming light before reaching the magnetoreceptor molecules, the light-dependent magnetic compass is therefore expected to be based on a photo-and polarization-selected population of magnetoreceptors whose signaling state depends on the relative alignment of the receptor molecules with polarized light and the magnetic field (13,23,24). Magnetic compass orientation in birds and other animals is, therefore, expected to be influenced by polarized light aligned at different angles to the magnetic field.…”

Section: Significancementioning

confidence: 99%

“…As recently pointed out by Lau et al (13), traditional radical-pair models thus do not take into consideration that natural skylight always enters the eyes directionally through the cornea and lens and that the magnetoreceptor molecules absorb light anisotropically, i.e., they preferentially absorb light of a specific direction and polarization. The probability of photoexcitation and, thereby, formation of radical pairs will therefore differ between magnetoreceptors across the retina and result in a photoselected population of magnetoreceptors that the magnetic field can act upon (13,23,24). The ratio of singlet and triplet states and, thereby, the magnetic field effect, will in turn depend on the relative alignment of the radical pair to the magnetic field (8,10).…”

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Polarized light modulates light-dependent magnetic compass orientation in birds

Muheim

Sjöberg

Pinzon-Rodriguez

2016

Proc. Natl. Acad. Sci. U.S.A.

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Magnetoreception of the light-dependent magnetic compass in birds is suggested to be mediated by a radical-pair mechanism taking place in the avian retina. Biophysical models on magnetic field effects on radical pairs generally assume that the light activating the magnetoreceptor molecules is nondirectional and unpolarized, and that light absorption is isotropic. However, natural skylight enters the avian retina unidirectionally, through the cornea and the lens, and is often partially polarized. In addition, cryptochromes, the putative magnetoreceptor molecules, absorb light anisotropically, i.e., they preferentially absorb light of a specific direction and polarization, implying that the light-dependent magnetic compass is intrinsically polarization sensitive. To test putative interactions between the avian magnetic compass and polarized light, we developed a spatial orientation assay and trained zebra finches to magnetic and/or overhead polarized light cues in a four-arm “plus” maze. The birds did not use overhead polarized light near the zenith for sky compass orientation. Instead, overhead polarized light modulated light-dependent magnetic compass orientation, i.e., how the birds perceive the magnetic field. Birds were well oriented when tested with the polarized light axis aligned parallel to the magnetic field. When the polarized light axis was aligned perpendicular to the magnetic field, the birds became disoriented. These findings are the first behavioral evidence to our knowledge for a direct interaction between polarized light and the light-dependent magnetic compass in an animal. They reveal a fundamentally new property of the radical pair-based magnetoreceptor with key implications for how birds and other animals perceive the Earth’s magnetic field.

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“…We believe that this question is unanswerable at present. So little is known about the signal transduction mechanisms that the primary detection sensitivity is currently a matter of speculation [53]. It is true that one can estimate the number of cryptochrome molecules needed in the eye to achieve a given angular resolution for the compass [20,32,39,54], but the results are heavily model-dependent, requiring many simplifying assumptions.…”

Section: Discussionmentioning

confidence: 99%

Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes

Lau

Rodgers

Hore

2012

J. R. Soc. Interface.

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According to the radical pair model, the magnetic compass sense of migratory birds relies on photochemical transformations in the eye to detect the direction of the geomagnetic field. Magnetically sensitive radical pairs are thought to be generated in cryptochrome proteins contained in magnetoreceptor cells in the retina. A prerequisite of the current model is for some degree of rotational ordering of both the cryptochromes within the cells and of the cells within the retina so that the directional responses of individual molecules do not average to zero. Here, it is argued that anisotropic distributions of radical pairs can be generated by the photoselection effects that arise from the directionality of the light entering the eye. Light-induced rotational order among the transient radical pairs rather than intrinsic ordering of their molecular precursors is seen as the fundamental condition for a magnetoreceptor cell to exhibit an anisotropic response. A theoretical analysis shows that a viable compass magnetoreceptor could result from randomly oriented cryptochromes contained in randomly oriented cells distributed around the retina.

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A New Type of Radical-Pair-Based Model for Magnetoreception

Cited by 39 publications

References 48 publications

The quantum needle of the avian magnetic compass

The quantum needle of the avian magnetic compass

Polarized light modulates light-dependent magnetic compass orientation in birds

Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes

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