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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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Self-citationThe Radical-Pair Mechanism of Magnetoreception
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“Triplet products are chemically different from the singlet products and thus may play a role in magnetoreception (modified from Ritz et al. 2000) Hence the radical pair model can only apply to the magnetic compass of birds, amphibians and marine turtles (see Table 1).”
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“It was the suggestion, in 2000, that cryptochromes could host magnetically sensitive radical pairs that set in motion the work reviewed in this Perspective (2).”
BackgroundInfluentialLong-distance navigation and magnetoreception in migratory animals
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“Although the first two are essentially classical effects, there is growing body of evidence in certain species (including birds[4], fruit flies[13] and even plants[14]) for the RP mechanism — which relies on the quantum evolution of a spatially-separated interacting pair of electron spins.”
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“The animal magnetoreception is often dependent on light, and it was proposed that the magnetic information is transmitted to the nervous system through the light-induced product of magnetically sensitive radical-pair reaction in photoreceptors (Ritz et al., 2000; Liedvogel and Mouritsen, 2009).”
Quantum coherence in biological systems
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“In 2000, it was hypothesized that CRYs contain magnetosensitive radical pairs (Ritz et al., 2000).”
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Ritz, T., Wiltschko, R., Hore, P. J., Rodgers, C. T., Stapput, K., Thalau, P., Timmel, C. R., & Wiltschko, W. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2008.11.072 · Cited by 305
“The radical-pair model ( 7 ,8) assumes that these properties of the avian magnetic compass—light-dependence and insensitivity to polarity—directly reflect characteristics of the primary processes of magnetoreception.”
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“(A radical pair process is started by the absorption of a photon by an acceptor molecule resulting in an electron transfer; the donor and acceptor molecules then each have one unpaired electron that holds a magnetic moment; Ritz et al. 2000.)”
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Zapka, M., Heyers, D., Hein, C. M., Engels, S., Schneider, N.-L., Hans, J. B., Weiler, S., Dreyer, D., Kishkinev, D., Wild, J. M., et al. (2009) · Nature · doi:10.1038/nature08528 · Cited by 296
Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism
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Fleissner, G., Holtkamp‐Rötzler, E., Hanzlik, M., Michael Winklhofer, A., Fleissner, G., Petersen, N., & Wiltschko, W. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10579 · Cited by 289
“Biochemical processes in the photoreceptive cascade are sensitive to direction changes in the surrounding magnetic field (whereby excited macromolecules form biradicals; Schulten and Windemuth, 1986; Ritz et al., 2000).”
BackgroundGalland, P., & Pazur, A. (2005) · Journal of Plant Research · doi:10.1007/s10265-005-0246-y · Cited by 285
“Recent studies imply a light-driven biradical mechanism underlying the magnetoreception of birds (Ritz et al. 2000) that could be mediated by cryptochromes (Möller et al.”
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Bostick, C. D., Mukhopadhyay, S., Pecht, I., Sheves, M., Cahen, D., & Lederman, D. (2018) · Reports on Progress in Physics · doi:10.1088/1361-6633/aa85f2 · Cited by 254
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BackgroundInfluentialCryptochromes—a potential magnetoreceptor: what do we know and what do we want to know?
Liedvogel, M., & Mouritsen, H. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0411.focus · Cited by 231
“This proposal has been revived by Ritz et al. (2000), who proposed that the retina with its almost perfect half-ball shape is well suited as an ordered structure , and that the radical pair intermediate is involved in some kind of visual reception system.”
BackgroundInfluentialCryptochrome Mediates Light-Dependent Magnetosensitivity of Drosophila's Circadian Clock
Yoshii, T., Ahmad, M., & Helfrich-Förster, C. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000086 · Cited by 232
“[10] calculated the yield of the triplet products in relation to the strength of the magnetic field and the angle of the field with respect to the alignment of the radical pair in space.”
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“Cryptochromes, which involve the photopigment flavin dehydrogenase (FAD), are blue-green light photoreceptors [37,38] and have been suggested as magneto-sensory candidate molecules [17].”
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“We furthermore suggested that Cluster N is likely to process such light-mediated magnetic compass responses, based on the fact that Cluster N is the only known forebrain area that is highly active during magnetic compass orientation, and on the theoretical model [7] on magnetic field modulation of the light sensitivit…”
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“Magnetic orientation is probably based on specific light receptors in the eye and shown not only to be light dependent (Ritz et al. 2000), but also wavelength dependent: migratory birds require light from the blue-green part of the spectrum for magnetic compass orientation (Wiltschko and Wiltschko…”
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BackgroundInfluentialHuman cryptochrome exhibits light-dependent magnetosensitivity
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“In many animals, magnetoreception is thought to depend on light-sensitive chemical reactions involving the flavoprotein cryptochrome (CRY”
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Directional orientation of birds by the magnetic field under different light conditions
Wiltschko, R., Stapput, K., Thalau, P., & Wiltschko, W. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0367.focus · Cited by 205
“The other hypothesis, the ‘radical-pair’ model, first forwarded by Schulten (1982) and later detailed by Ritz et al. (2000), suggests that magnetoreception in birds is based on spin-chemical processes in specialized photopigments.”
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Magnetic Field Effects in Arabidopsis thaliana Cryptochrome-1
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“(22), permitting the bird to visually discern the magnetic field.”
InfluentialSelf-citationMagnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana
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“The sensitivity to magnetic fields as weak as the geomagnetic field of 25-60 |iT is linked to the effect of magnetic fields on electron transfer reac tions of photoreceptors through radical-pair processes (Schulten 1982; Ritz et al. 2000), with the blue-light receptor cryptochrome suggested as a promising candi date f…”
BackgroundInfluentialSelf-citationThe origins of quantum biology
McFadden, J., & Al-Khalili, J. (2018) · Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rspa.2018.0674 · Cited by 192
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Role of Exchange and Dipolar Interactions in the Radical Pair Model of the Avian Magnetic Compass
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“have proposed that a radical pair magnetoreceptor is formed by photoinduced intramolecular electron transfers in a cryptochrome (8).”
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“favored is the Radical Pair Model by Ritz and colleagues [4]: it proposes that photon absorption in specialized receptor molecules leads to an electron transfer and the formation of radical pairs.”
BackgroundMethodResultInfluentialQuantum Control and Entanglement in a Chemical Compass
Cai, J., Guerreschi, G. G., & Briegel, H. J. (2010) · Physical Review Letters · doi:10.1103/physrevlett.104.220502 · Cited by 182
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“This led to the suggestion that photochemical reactions in the birds’ eyes could produce spin-correlated radical pairs as the primary sensor in a magnetic field-dependent signalling cascade [7,8], based on the fact that the recombination reactions of spin-correlated radical pairs are known to be magnetic field-sensiti…”
BackgroundInfluentialWoodward, J. R. (2002) · Progress in Reaction Kinetics and Mechanism · doi:10.3184/007967402103165388 · Cited by 181
Night-vision brain area in migratory songbirds.
Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K., & Jarvis, E. (2005) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0409575102 · Cited by 159
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“…activated by light (Griffin et al. 1999; Van Gelder et al. 2003), and not all ‘radical-pair’ processes in flavoproteins have immediate physiological functions, the fact that cryptochromes are found in the robin’s retina is very intriguing in view of the ‘radical-pair’ model (Ritz et al. 2000).”
BackgroundInfluentialLight at night as an environmental endocrine disruptor
Russart, K. L. G., & Nelson, R. J. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.08.029 · Cited by 174
“Retinal neurons that express cryptochromes have high activity when nightmigratory birds perform magnetic compass orientation [122].”
BackgroundMagnetic compass orientation of migratory birds in the presence of a 1.315�MHz oscillating field
Thalau, P., Ritz, T., Stapput, K., Wiltschko, R., & Wiltschko, W. (2005) · Naturwissenschaften · doi:10.1007/s00114-004-0595-8 · Cited by 165
“A model proposed by Schulten (1982) and detailed by Ritz et al. (2000) suggests that certain chemical reactions such as radical-pair processes are sensitive to the direction of the ambient magnetic field and thus can provide the basis for a compass sense.”
BackgroundMethodInfluentialSelf-citationMuheim, R., Moore, F. R., & Phillips, J. B. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01960 · Cited by 168
“For example, a recent theoretical model by Ritz et al. (2000) suggests that the biophysical process that underlies the lightdependent magnetic compass will cause a decrease in sensitivity to light in magnetically sensitive photoreceptors aligned either parallel or antiparallel to the axis of the…”
BackgroundInfluentialA magnetic compass aids monarch butterfly migration
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Magnetoreception through Cryptochrome May Involve Superoxide
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“Such a magnetic field-sensing mechanism can explain many long-observed properties of avian magnetoreception (1,2, 18 ,23,24).”
BackgroundMethodResultInfluentialSelf-citationWiltschko, R., & Wiltschko, W. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0295 · Cited by 157
“The radical pair model These properties of the avian magnetic compass caused Ritz and colleagues [15] to propose the radical pair model: upon absorption of a photon, radical pairs are formed, either as singlets with antiparallel spin or as triplets with parallel spin.”
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“Recently, cryptochromes have been proposed as candidate genes involved in magnetoreception and orientation (Ritz et al. 2000; Liedvogel et al. 2007), but no other genes have been identified that can explain the often prominent variation in migratory behaviour exhibited within many species (Pulido…”
BackgroundThe magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds
Mouritsen, H., & Hore, P. J. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.01.005 · Cited by 154
Hunt, R. W., Zavalin, A. I., Bhatnagar, A., Chinnasamy, S., & Das, K. C. (2009) · International Journal of Molecular Sciences · doi:10.3390/ijms10104515 · Cited by 154
“order of 1 mT inducing an increase in the signaling activity of the protein by ~10% [79,80].”
BackgroundTransduction of the Geomagnetic Field as Evidenced from alpha-Band Activity in the Human Brain
Wang, C. X., Hilburn, I. A., Wu, D.-A. J., Mizuhara, Y., Cousté, C. P., Abrahams, J. N. H., Bernstein, S. E., Matani, A., Shinsuke Shimojo, A., & Kirschvink, J. L. (2019) · eNeuro · doi:10.1523/eneuro.0483-18.2019 · Cited by 154
“The asymmetric declination response provided a starting point for evaluating potential mechanisms of magnetosensory transduction, particularly the quantum compass hypothesis, which has received much attention in recent years (Ritz et al., 2000; Hore and Mouritsen, 2016).”
BackgroundInfluentialDirect Observation of a Photoinduced Radical Pair in a Cryptochrome Blue‐Light Photoreceptor
Biskup, T., Schleicher, E., Okafuji, A., Link, G., Hitomi, K., Getzoff, E. D., & Weber, S. (2008) · Angewandte Chemie International Edition · doi:10.1002/anie.200803102 · Cited by 153
Muheim, R., Bäckman, J., & Åkesson, S. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.24.3845 · Cited by 151
Quantum effects in biology: golden rule in enzymes, olfaction, photosynthesis and magnetodetection
Brookes, J. C. (2017) · Proceedings of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rspa.2016.0822 · Cited by 168
“The RPM was first introduced by Schulten and colleagues [83] and developed further by Ritz and colleagues [84–88], his idea is that the ‘chemical compass’ in the bird is a light-initiated RPM, where a disruption to the pair recombination due to magnetic field effects results in interpretation and recognition in the bi…”
BackgroundMagnetoreception—A sense without a receptor
Nordmann, G. C., Hochstoeger, T., & Keays, D. A. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2003234 · Cited by 149
Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G., & Fleiṡsner, G. (2007) · Die Naturwissenschaften · doi:10.1007/s00114-007-0236-0 · Cited by 149
“Three theories currently dominate the scientific discussion: electrical induction processes (Kalmijn 1978), photopigment-based magnetoreception (Ritz et al. 2000), and iron-mineral-based magnetoreception (Kirschvink et al.”
BackgroundCintolesi, F., Ritz, T., Kay, C. W. M., Timmel, C. R., & Hore, P. J. (2003) · Chemical Physics · doi:10.1016/s0301-0104(03)00320-3 · Cited by 146
Self-citationAlternative radical pairs for cryptochrome-based magnetoreception
Lee, A. A., Lau, J. C. S., Hogben, H. J., Biskup, T., Kattnig, D. R., & Hore, P. J. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.1063 · Cited by 140
“In 2000, Ritz and Schulten proposed the protein cryptochrome as the primary sensor in birds [5].”
BackgroundResultInfluentialA study of spin chemistry in weak magnetic fields
Timmel, C. R., & Henbest, K. B. (2004) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2004.1459 · Cited by 138
The Neural Basis of Long-Distance Navigation in Birds
Mouritsen, H., Heyers, D., & Güntürkün, O. (2015) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105054 · Cited by 142
Henbest, K. B., Kukura, P., Rodgers, C. T., Hore, P. J., & Timmel, C. R. (2004) · Journal of the American Chemical Society · doi:10.1021/ja048220q · Cited by 136
Ritz, T., Ahmad, M., Mouritsen, H., Wiltschko, R., & Wiltschko, W. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0456.focus · Cited by 135
“…responses of birds, but only the regular compass, is affected by oscillating magnetic fields (e.g. Wiltschko et al. 2005, 2007b) and that the disruptive effect occurs only at certain frequencies and alignments, matching general expectations from a radical pair model (Ritz et al. 2000, 2009).”
BackgroundInfluentialSelf-citationAlgal photoreceptors: in vivo functions and potential applications
Kianianmomeni, A., & Hallmann, A. (2013) · Planta · doi:10.1007/s00425-013-1962-5 · Cited by 138
“1999; Lin and Shalitin 2003) and are also known to mediate magnetoreception (Ceriani et al. 1999; Gegear et al. 2010; Kume et al. 1999; Ritz et al. 2000); (3) DASH (Drosophila, Arabidopsis, Synechocystis and Human) cryptochromes: DASH cryptochromes were identified first in cyanobacteria (Brudler et al.”
BackgroundThe neurobiology of magnetoreception in vertebrate animals
Lohmann, K. J., & Johnsen, S. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01542-8 · Cited by 132
The Quantum Biology of Reactive Oxygen Species Partitioning Impacts Cellular Bioenergetics
Usselman, R. J., Chavarriaga, C., Castello, P. R., Procopio, M., Ritz, T., Dratz, E. A., Singel, D. J., & Martino, C. F. (2016) · Scientific Reports · doi:10.1038/srep38543 · Cited by 133
Self-citationMagnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase
Henbest, K. B., Maeda, K., Hore, P. J., Joshi, M., Bacher, A., Bittl, R., Weber, S., Timmel, C. R., & Schleicher, E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803620105 · Cited by 130
“Two competing hypothetical models for the primary detection mechanism of this magnetic compass have been proposed: one involving magnetic iron-containing particles (18–20), the other based on magneticfield-sensitive radical pair chemistry (17, 21, 22).”
BackgroundMagnetic field changes activate the trigeminal brainstem complex in a migratory bird
Heyers, D., Zapka, M., Hoffmeister, M., Wild, J. M., & Mouritsen, H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907068107 · Cited by 130
Gehring, W. J. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.96 · Cited by 134
Magnetic particle-mediated magnetoreception
Shaw, J., Boyd, A., House, M. J., Woodward, R. C., Mathes, F., Cowin, G., Saunders, M., & Baer, B. (2015) · Journal of The Royal Society Interface · doi:10.1098/rsif.2015.0499 · Cited by 130
Partch, C. L., & Sancar, A. (2005) · Photochemistry and Photobiology · doi:10.1562/2005-07-08-ir-607 · Cited by 130
Effects of static magnetic fields in biology: role of free radicals
Okano, H. (2008) · Frontiers in bioscience · doi:10.2741/3141 · Cited by 129
“The recent data related to the mechanisms of action of SMF on FRR are diverse and multifold but elusive.”
BackgroundInfluentialElectron spin relaxation in cryptochrome-based magnetoreception
Kattnig, D. R., Solov’yov, I. A., & Hore, P. J. (2016) · Physical Chemistry Chemical Physics · doi:10.1039/c5cp06731f · Cited by 129
A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception
Dodson, C. A., Hore, P. J., & Wallace, M. I. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.07.002 · Cited by 129
Spectroscopy in sculpted fields
Yang, N., Tang, Y., & Cohen, A. E. (2009) · Nano Today · doi:10.1016/j.nantod.2009.05.001 · Cited by 127
Usselman, R. J., Hill, I., Singel, D. J., & Martino, C. F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093065 · Cited by 126
“The Schulten lab have taken the fundamental ideas developed in prior work [16,17,23] and applied its significance to an example of biological function in vivo, specifically the role of cryptochrome as a magnetoreceptor in the case of avian magnetic sensing [15].”
BackgroundStructural biology of DNA photolyases and cryptochromes
Müller, M., & Carell, T. (2009) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2009.05.003 · Cited by 125
Extended Electron-Transfer in Animal Cryptochromes Mediated by a Tetrad of Aromatic Amino Acids
Nohr, D., Franz, S., Rodriguez, R., Paulus, B., Essen, L., Weber, S., & Schleicher, E. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2016.06.009 · Cited by 124
Physiological, behavioral, and ecological aspects of migration in reptiles
Southwood, A. L., & Avens, L. (2009) · Journal of Comparative Physiology B · doi:10.1007/s00360-009-0415-8 · Cited by 123
Possible existence of optical communication channels in the brain
Kumar, S., Boone, K., Tuszyński, J. A., Barclay, P. E., & Simon, C. (2016) · Scientific Reports · doi:10.1038/srep36508 · Cited by 124
“A well-known biological example is provided by cryptochrome proteins, which can be activated by light to produce a pair of radicals with correlated electronic spins, which are suspected to be involved in bird magnetoreception (the ability to perceive magnetic fields) 34 .”
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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