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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Quantum biology has been benefitting from refinement of experimental tools that are beginning to provide direct access to observation of quantum dynamics in biological systems.
“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]
There is compelling theoretical and/or experimental evidence that quantum phenomena are essential for understanding environment assisted excitation energy transport in photosynthesis.
“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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“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…”
BackgroundLateralization of magnetic compass orientation in a migratory bird
Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H., & Wiltschko, R. (2002) · Nature · doi:10.1038/nature00958 · Cited by 217 · see citing works
Avian navigation: from historical to modern concepts
Wiltschko, R., & Wiltschko, W. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2054 · Cited by 215 · see citing works
Magnetic field effects in chemical systems
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Green Light for Nocturnally Migrating Birds
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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…”
BackgroundMagnetic fields and radical reactions: recent developments and their role in nature
Brocklehurst, B. (2002) · Chemical Society Reviews · doi:10.1039/b107250c · Cited by 213 · see citing works
The quantum needle of the avian magnetic compass
Hiscock, H. G., Worster, S., Kattnig, D. R., Steers, C., Jin, Y., Manolopoulos, D. E., Mouritsen, H., & Hore, P. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600341113 · Cited by 215 · see citing works
“Theoretical treatments of radical pair-based magnetoreception typically involve simulations of the quantum spin dynamics of short-lived radicals in Earth strength (∼50 μT) magnetic fields (9, 10, 17).”
BackgroundInfluentialHuman cryptochrome exhibits light-dependent magnetosensitivity
Foley, L. E., Gegear, R. J., & Reppert, S. M. (2011) · Nature Communications · doi:10.1038/ncomms1364 · Cited by 214 · see citing works
“In many animals, magnetoreception is thought to depend on light-sensitive chemical reactions involving the flavoprotein cryptochrome (CRY”
BackgroundJohnsen, S., & Lohmann, K. J. (2008) · Physics Today · doi:10.1063/1.2897947 · Cited by 209 · see citing works
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 · see citing works
“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.”
BackgroundInfluentialGünther, A., Einwich, A., Sjulstok, E., Feederle, R., Bolte, P., Koch, K.-W., Solov’yov, I. A., & Mouritsen, H. (2018) · Current Biology · doi:10.1016/j.cub.2017.12.003 · Cited by 204 · see citing works
Magnetic Field Effects in Arabidopsis thaliana Cryptochrome-1
Solov’yov, I. A., Chandler, D. E., & Schulten, K. (2007) · Biophysical Journal · doi:10.1529/biophysj.106.097139 · Cited by 196 · see citing works
“(22), permitting the bird to visually discern the magnetic field.”
InfluentialSelf-citationMagnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana
Ahmad, M., Galland, P., Ritz, T., Wiltschko, R., & Wiltschko, W. (2006) · Planta · doi:10.1007/s00425-006-0383-0 · Cited by 194 · see citing works
“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 · see citing works
“1929 [24], 1932 [25], 1941 [20], 1944 [19], 1953 [42], 1963 [32], 1966 [43], 1974 [44], 1976 [45–48], 1989 [49], 2000 [50], 2007 [4].”
Role of Exchange and Dipolar Interactions in the Radical Pair Model of the Avian Magnetic Compass
Efimova, O., & Hore, P. J. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.119362 · Cited by 189 · see citing works
“have proposed that a radical pair magnetoreceptor is formed by photoinduced intramolecular electron transfers in a cryptochrome (8).”
BackgroundMagnetic field effects in biology from the perspective of the radical pair mechanism
Zadeh-Haghighi, H., & Simon, C. (2022) · Journal of The Royal Society Interface · doi:10.1098/rsif.2022.0325 · Cited by 197 · see citing works
Müller, P., & Ahmad, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.228940 · Cited by 190 · see citing works
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Avian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors
Nießner, C., Denzau, S., Gross, J. C., Peichl, L., Bischof, H., Fleissner, G., Wiltschko, W., & Wiltschko, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020091 · Cited by 184 · see citing works
“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 · see citing works
Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C. R., Hore, P. J., & Mouritsen, H. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001106 · Cited by 183 · see citing works
“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 · see citing works
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 · see citing works
Möller, A., Sagasser, S., Wiltschko, W., & Schierwater, B. (2004) · Naturwissenschaften · doi:10.1007/s00114-004-0578-9 · Cited by 173 · see citing works
“…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 169 · see citing works
“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 · see citing works
“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 · see citing works
“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
Guerra, P. A., Gegear, R. J., & Reppert, S. M. (2014) · Nature Communications · doi:10.1038/ncomms5164 · Cited by 168 · see citing works
Magnetoreception through Cryptochrome May Involve Superoxide
Solov’yov, I. A., & Schulten, K. J. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.03.048 · Cited by 157 · see citing works
“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 · see citing works
“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.”
BackgroundBensch, S., Grahn, M., MÜLLER, N., Gay, L., & Åkesson, S. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04210.x · Cited by 156 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
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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 161 · see citing works
“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 · see citing works
Fleissner, G., Stahl, B., Thalau, P., Falkenberg, G., & Fleiṡsner, G. (2007) · Die Naturwissenschaften · doi:10.1007/s00114-007-0236-0 · Cited by 149 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 137 · see citing works
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“…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 131 · see citing works
“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 · see citing works
The Quantum Biology of Reactive Oxygen Species Partitioning Impacts Cellular Bioenergetics
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Self-citationMagnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase
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“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
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Magnetic particle-mediated magnetoreception
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“The recent data related to the mechanisms of action of SMF on FRR are diverse and multifold but elusive.”
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A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception
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“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
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Extended Electron-Transfer in Animal Cryptochromes Mediated by a Tetrad of Aromatic Amino Acids
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“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 .”
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Geomagnetism and Paleomagnetism Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › 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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