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A Model for Photoreceptor-Based Magnetoreception in Birds
Open accessAbstract
A large variety of animals has the ability to sense the geomagnetic field and utilize it as a source of directional (compass) information. It is not known by which biophysical mechanism this magnetoreception is achieved. We investigate the possibility that magnetoreception involves radical-pair processes that are governed by anisotropic hyperfine coupling between (unpaired) electron and nuclear spins. We will show theoretically that fields of geomagnetic field strength and weaker can produce significantly different reaction yields for different alignments of the radical pairs with the magnetic field. As a model for a magnetic sensory organ we propose a system of radical pairs being 1) orientationally ordered in a molecular substrate and 2) exhibiting changes in the reaction yields that affect the visual transduction pathway. We evaluate three-dimensional visual modulation patterns that can arise from the influence of the geomagnetic field on radical-pair systems. The variations of these patterns with orientation and field strength can furnish the magnetic compass ability of birds with the same characteristics as observed in behavioral experiments. We propose that the recently discovered photoreceptor cryptochrome is part of the magnetoreception system and suggest further studies to prove or disprove this hypothesis.
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“In recent years, quantum biology too has been benefitting considerably from the refinement of experimental tools that are beginning to provide direct access to the observation of quantum dynamics in biological systems [11-14]”
From Vibrations, quanta and biology (2013) · cites this paper as [11]
In the citing paper
“environment assisted excitation energy transport in photosynthesis [11, 15, 16], magneto-reception of birds [17-19] and the mechanism underlying olfaction [20, 21], for which there is some compelling theoretical and/or experimental evidence that quantum phenomena are essential for their understanding.”
From Vibrations, quanta and biology (2013) · cites this paper as [11]
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“Cryptochromes were also proposed to act as sensors for the geomagnetic field and assists many animals in long-range navigation 5,10,11,13,14,16,28,31 .”
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“Several conditions need to be satisfied for a radical pair to be suitable as a geomagnetic compass sensor5: (1) the electron spin in at least one of the radicals must interact anisotropically with nuclear spins, (2) the mutual interaction of the two electron spins should be small, (3) the radical pair must react spin…”
BackgroundExtremely low-frequency electromagnetic fields disrupt magnetic alignment of ruminants
Burda, H., Begall, S., Červený, J., Neef, J., & Němec, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811194106 · Cited by 114
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An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway
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“MFmodulates interconversion of the singlet and triplet states of RP, hence changing the proportions of two competing pathways yielding different reaction products (5).”
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Are biochemical reactions affected by weak magnetic fields?
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“The most likely candidate magnetoreceptor for this compass is the photoactive protein, cryptochrome, in which apparently suitable flavin-tryptophan radical pairs are formed in vitro after excitation by blue light (19).”
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Nießner, C., Denzau, S., Stapput, K., Ahmad, M., Peichl, L., Wiltschko, W., & Wiltschko, R. (2013) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.0638 · Cited by 109
“[4] had suggested cryptochromes, blue-light absorbing flavoproteins, because they were the only known photoreceptor molecules in animals that form radical pairs [11].”
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“The magnetic sensitivity is also influenced by the radical-pair lifetime (Ritz et al., 2000; Efimova and Hore, 2008; Solov’yov et al., 2014); it has been assumed that lifetimes of ∼1 µs are realistic for biological systems and that ∼1 µs might be close to optimum for sensing the direction of the…”
BackgroundInfluentialMagnetoreception in birds: two receptors for two different tasks
Wiltschko, W., & Wiltschko, R. (2007) · Journal für Ornithologie · doi:10.1007/s10336-007-0233-2 · Cited by 107
“The required conditions could be met by the more or less spherical arrangement of receptors in the eyes—radical pair processes would generate characteristic patterns of activation across the retina (Ritz et al. 2000).”
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Magnetic Maps in Animals: A Theory Comes of Age?
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“The two predominant theoretical mechanisms believed to mediate sensitivity to the geomagnetic field involve either excited states of macromolecules (Schulten and Windemuth 1986; Ritz et al. 2000) or biogenic magnetite (Kirschvink and Walker 1985; Winklhofer et al.”
BackgroundCryptochrome 1 mediates light-dependent inclination magnetosensing in monarch butterflies
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“It predicts that the spin state of light-induced radical pairs is influenced by local magnetic fields, altering the photochemical properties of a receptor protein (2, 3).”
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Begall, S., Malkemper, E. P., Červený, J., Němec, P., & Burda, H. (2012) · Mammalian Biology · doi:10.1016/j.mambio.2012.05.005 · Cited by 105
“Provided that MA in foxes is based on a radical-pairmechanism (Schulten et al., 1978; Ritz et al., 2000), i.”
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Öztürk, N., Song, S.-H., Özgür, S., Selby, C. P., Morrison, L., Partch, C. L., Zhong, D., & Sancar, A. (2007) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2007.72.015 · Cited by 104
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“This model allows two testable predictions, namely (1) magnetoreception should be light dependent and (2) oscillating fields in the MHz range that interfere with radical pair processes should disrupt magnetoreception (Ritz et al., 2000).”
BackgroundSelf-citationThe magnetic compass mechanisms of birds and rodents are based on different physical principles
Thalau, P., Ritz, T., Burda, H., Wegner, R., & Wiltschko, R. (2006) · Journal of The Royal Society Interface · doi:10.1098/rsif.2006.0130 · Cited by 99
“Assuming that the radical pairs within a cell are sufficiently ordered, the sensitivity of radical reactions on the direction of an external magnetic field can provide the basis for a magnetic compass sense (for details of the model see Ritz et al. 2000).”
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“The first, known as the radical pair hypothesis, argues that the spin state of a light-induced radical pair is influenced by the Earth’s magnetic field, which, in turn, affects the biochemical properties of a signaling protein (8).”
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“In order to achieve a compass, it is necessary that the blue-light-sensitive pigment molecules (possibly CCs) are aligned physically within each receptor cell so that their net interaction with the geomagnetic field at the cellular level can be detected, which is a condition for an axial magnetic compass (Schulten 198…”
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Electron spin relaxation can enhance the performance of a cryptochrome-based magnetic compass sensor
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“in birds and mammals), it may be perceived as a visual image superimposed on the animal’s surroundings (Ritz et al., 2000; Ritz et al., 2010).”
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Quantum Computing for Molecular Biology**
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BackgroundPhotocycle and signaling mechanisms of plant cryptochromes
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Spin-selective reactions of radical pairs act as quantum measurements
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Robins have a magnetic compass in both eyes
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“Our results showing that European Robins have a magnetic compass in both eyes are in line with other recent findings, which otherwise would be difficult to explain: (1) garden warblers have a magnetic compass in both eyes(11); (2) the putative magnetoreceptive cryptochromes are located in both eyes(6); (3) Cluster N(7…”
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MethodInfluentialSelf-citationEffect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana
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“…(circles). field strength because of the competition between two different physical mechanisms underlying magnetic field effects on radical pairs (Ritz et al., 2000). from these studies in the present context is the evidence By far, the most common mechanism to generate a for an 90 shift in the…”
BackgroundSelf-citationLight-dependent magnetoreception in birds: the crucial step occurs in the dark
Wiltschko, R., Ahmad, M., Nießner, C., Gehring, D., & Wiltschko, W. (2016) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.1010 · Cited by 86
“In this study, we use a behavioural response, with the time birds require for obtaining magnetic directional information for this response yet unknown—it not only depends on the time course of the FAD cycle, but mainly on the biological processes transmitting and processing the respective information, involving, for e…”
InfluentialMigratory Birds Use Head Scans to Detect the Direction of the Earth's Magnetic Field
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“…mechanisms (e.g., using knockout strains lacking functional copies of genes that have been implicated in magnetoreception [e.g., cryptochromes; Ritz et al., 2000]); and (3) biophysical mechanisms (e.g., observing effects of low-level radio frequency fields that have been shown to disrupt…”
Overall energy conversion efficiency of a photosynthetic vesicle
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“Carotenoids transfer excitation within less than a picosecond to a nearby BChl (Damjanović et al., 1999; Berera et al., 2009) and also play a role in quenching triplet states of BChls through reverse excitation transfer (Ritz et al., 2000a).”
BackgroundSelf-citationModulation of Hydrogen Peroxide Production in Cellular Systems by Low Level Magnetic Fields
Martino, C. F., & Castello, P. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022753 · Cited by 88
“In order to observe changes in reaction yields in the presence of the Earth’s magnetic field, the hyperfine interaction between radical pairs should be in the same order of magnitude as the Zeeman interaction [25,26,28], thus making the possibility for the magnetic field effect.”
BackgroundCellular autofluorescence is magnetic field sensitive
Ikeya, N., & Woodward, J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2018043118 · Cited by 79
“It is quite widely believed that blue light photoreceptors called cryptochromes, which contain flavin adenine dinucleotide (FAD) as a noncovalently bound cofactor, are responsible for RPM-based magnetoreception (12).”
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“(2) as an additional, time‐dependent Zeeman term.”
BackgroundRadio frequency magnetic fields disrupt magnetoreception in American cockroach
Vácha, M., Půžová, T., & Kvíčalová, M. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.028670 · Cited by 79
“The so-called magnetite-based mechanism assumes the presence of ferrimagnetic, iron oxide particles in tissues (Fleissner et al., 2003; Fleissner et al., 2007; Kirschvink et al., 2001), and the other principle postulates the radical pair-based mechanism (Ritz et al., 2000).”
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Prior, H., Wiltschko, R., Stapput, K., Güntürkün, O., & Wiltschko, W. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.02.018 · Cited by 80
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An overview of biomimetic sensor technology
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“A theoretical concept for a vision-based magnetic compass that relies on radical-pair processes directly mimics the sensitivity modulation of the light receptors in the eye ( Ritz et al. , 2000”
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Magnetic Strategies for Nervous System Control
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“Some organisms exhibit magnetoreception, the ability to perceive magnetic fields (Ritz et al. 2000, Wiltschko & Wiltschko 2005).”
BackgroundInteractions between electromagnetic radiation and biological systems
Liu, L., Huang, B., Lu, Y., Zhao, Y., Tang, X., & Shi, Y. (2024) · iScience · doi:10.1016/j.isci.2024.109201 · Cited by 80
“The external magnetic field affects the interconversion between the singlet and triplet states of the radical pair (adapted from 207,208 ).”
BackgroundA multi-site variational master equation approach to dissipative energy transfer
Pollock, F. A., McCutcheon, D. P. S., Lovett, B. W., Gauger, E. M., & Nazir, A. (2013) · New Journal of Physics · doi:10.1088/1367-2630/15/7/075018 · Cited by 73
Orientation of Birds in Total Darkness
Stapput, K., Thalau, P., Wiltschko, R., & Wiltschko, W. (2008) · Current Biology · doi:10.1016/j.cub.2008.03.046 · Cited by 76
Sensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome
Wiltschko, R., & Wiltschko, W. (2014) · Biosensors · doi:10.3390/bios4030221 · Cited by 76
Diamond-based single-molecule magnetic resonance spectroscopy
Cai, J., Jelezko, F., Plenio, M. B., & Retzker, A. (2013) · New Journal of Physics · doi:10.1088/1367-2630/15/1/013020 · Cited by 75
Cryptochrome magnetoreception: four tryptophans could be better than three
Wong, S. Y., Wei, Y., Mouritsen, H., Solov’yov, I. A., & Hore, P. J. (2021) · Journal of The Royal Society Interface · doi:10.1098/rsif.2021.0601 · Cited by 76
Pinzon-Rodriguez, A., Bensch, S., & Muheim, R. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2018.0058 · Cited by 75
Reaction Kinetics and Mechanism of Magnetic Field Effects in Cryptochrome
Solov’yov, I. A., & Schulten, K. (2011) · The Journal of Physical Chemistry B · doi:10.1021/jp209508y · Cited by 75
Self-citationEntanglement and Sources of Magnetic Anisotropy in Radical Pair-Based Avian Magnetoreceptors
Hogben, H. J., Biskup, T., & Hore, P. J. (2012) · Physical Review Letters · doi:10.1103/physrevlett.109.220501 · Cited by 73
Dreuw, A. (2006) · ChemPhysChem · doi:10.1002/cphc.200600064 · Cited by 73
Photolyases and cryptochromes: common mechanisms of DNA repair and light-driven signaling?
Essen, L. (2006) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2006.01.004 · Cited by 73
Cain, S. D. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.539 · Cited by 73
“In parallel with behavioral experiments, several theoretical models of magnetoreception have been proposed to explain how animals might detect magnetic fields (Kalmijn, 1978; Kirschvink and Gould, 1981; Schulten and Windemuth, 1986; Ritz et al., 2000, 2002).”
BackgroundMagnetoreception in birds: the effect of radio-frequency fields
Wiltschko, R., Thalau, P., Gehring, D., Nießner, C., Ritz, T., & Wiltschko, W. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.1103 · Cited by 72
“The eye was suggested as site of magnetoreception [3,4] and cryptochrome, a blue light receptor (for review, see e.”
BackgroundInfluentialSelf-citationMagnetic field effects in flavoproteins and related systems
Evans, E. W., Dodson, C. A., Maeda, K., Biskup, T., Wedge, C. J., & Timmel, C. R. (2013) · Interface Focus · doi:10.1098/rsfs.2013.0037 · Cited by 69
Phillips, J. B., Deutschlander, M. E., Freake, M. J., & Borland, S. C. (2001) · Journal of Experimental Biology · doi:10.1242/jeb.204.14.2543 · Cited by 72
Quantum Coherence and Sensitivity of Avian Magnetoreception
Bandyopadhyay, J. N., Paterek, T., & Kaszlikowski, D. (2012) · Physical Review Letters · doi:10.1103/physrevlett.109.110502 · Cited by 74
Bolte, P., Bleibaum, F., Einwich, A., Günther, A., Liedvogel, M., Heyers, D., Depping, A., Wöhlbrand, L., Rabus, R., Janssen‐Bienhold, U., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147819 · Cited by 74
“The immuno-labelled cells detected with our diagnostic antibody were evenly distributed across the entire retina, which is in accordance with the radical-pair model [13].”
BackgroundResultVariable Electron Transfer Pathways in an Amphibian Cryptochrome
Biskup, T., Paulus, B., Okafuji, A., Hitomi, K., Getzoff, E. D., Weber, S., & Schleicher, E. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.417725 · Cited by 72
“Such RP states in Crys – if spincorrelated – have been proposed to form the basis of a photochemical magnetoreceptor (40).”
BackgroundCoherent Spin Manipulation in Molecular Semiconductors: Getting a Handle on Organic Spintronics
Lupton, J. M., McCamey, D. R., & Boehme, C. (2010) · ChemPhysChem · doi:10.1002/cphc.201000186 · Cited by 70
Natal imprinting to the Earth’s magnetic field in a pelagic seabird
Wynn, J., Padget, O., Mouritsen, H., Perrins, C. M., & Guilford, T. (2020) · Current Biology · doi:10.1016/j.cub.2020.05.039 · Cited by 71
Light-dependent Structural Change of Chicken Retinal Cryptochrome4
Watari, R., Chiaki, Y., Zemba, W., Kubo, Y., Okano, K., & Okano, T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.395731 · Cited by 68
Lateralized activation of Cluster N in the brains of migratory songbirds
Liedvogel, M., Feenders, G., Wada, K., Troje, N. F., Jarvis, E. D., & Mouritsen, H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05350.x · Cited by 70
“In a NMF, there are expected to be small modulations of the singlet–triplet proportions (probably a few per cent) in different parts of the retina (Ritz et al., 2000).”
BackgroundResultInfluentialViability of superoxide-containing radical pairs as magnetoreceptors
Player, T. C., & Hore, P. J. (2019) · The Journal of Chemical Physics · doi:10.1063/1.5129608 · Cited by 69
Unraveling navigational strategies in migratory insects
Merlin, C., Heinze, S., & Reppert, S. M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.11.009 · Cited by 71
“Using genetic and behavioral approaches in Drosophila, the UV/blue light photoreceptor CRYPTOCHROME (CRY), proposed previously as a candidate magnetoreceptor [43], has recently been shown to mediate lightdependent magnetosensitivity in flies [44 ].”
Kattnig, D. R., & Hore, P. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-09914-7 · Cited by 73
“It is clear from equations (8) and (9) that the scavenging reaction has converted a portion of the surviving radical pairs into the triplet state.”
BackgroundThamarath, S. S., Heberle, J., Hore, P. J., Kottke, T., & Matysik, J. (2010) · Journal of the American Chemical Society · doi:10.1021/ja1082969 · Cited by 69
Xu, C., Yin, X., Lv, Y., Wu, C., Zhang, Y., & Song, T. (2011) · Advances in Space Research · doi:10.1016/j.asr.2011.12.004 · Cited by 69
Origin of Light-Induced Spin-Correlated Radical Pairs in Cryptochrome
Weber, S., Biskup, T., Okafuji, A., Marino, A. R., Berthold, T., Link, G., Hitomi, K., Getzoff, E. D., Schleicher, E., & Norris, J. R. (2010) · The Journal of Physical Chemistry B · doi:10.1021/jp103401u · Cited by 70
Quantum effects in biology: Bird navigation
Ritz, T. (2011) · Procedia Chemistry · doi:10.1016/j.proche.2011.08.034 · Cited by 67
Self-citationNanomagnetic Control of Intersystem Crossing
Cohen, A. E. (2009) · The Journal of Physical Chemistry A · doi:10.1021/jp907113p · Cited by 64
Metadata
- Authors
- Ritz, T., Adem, S., & Schulten, K.
- Affiliations
- University of Illinois Urbana-Champaign (US)
- Corresponding author
- Schulten, Klaus
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2000-02
- Volume
- 78
- Issue
- 2
- Pages
- 707-718
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1300674
- OpenAlex
- W2138668594
- Cited by
- 1,176
- References
- 62
- Citations by year
- 2026: 68 · 2025: 63 · 2024: 49 · 2023: 66 · 2022: 62 · 2021: 71 · 2020: 59 · 2019: 40 · 2018: 58 · 2017: 71 · 2016: 59 · 2015: 46 · 2014: 73 · 2013: 36 · 2012: 42
- FWCI
- 8.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Center for Research Resources (P41RR005969)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electromagnetic Fields and Biological Effects
- Physical Sciences › Earth and Planetary Sciences › Geophysics › Geomagnetism and Paleomagnetism Studies
- Physical Sciences › Chemistry › Spectroscopy › Electron Spin Resonance Studies
- Keywords
- magnetoreception, birds, geomagnetic field, radical pairs, cryptochrome, photoreceptors, hyperfine interaction, magnetic compass, phototransduction, reaction yield
- MeSH terms
- Animals, Birds, Eye Proteins, Flavoproteins, Homing Behavior, Magnetics, Models, Biological, Visual Perception, Anisotropy, Photoreceptor Cells, Invertebrate, Photoreceptor Cells, Vertebrate, Drosophila Proteins, Receptors, G-Protein-Coupled, Cryptochromes
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