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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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Mechanisms of Magnetic Orientation in Birds
Beason, R. C. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.565 · Cited by 67
“Magnetic compass reception in birds appears to be a light dependent process based on antagonistically interacting spectral mechanisms with at least one shortwavelength and one long-wavelength mechanism (Deutschlander et al., 1999b) or multiple states of a short-wavelength sensitive mechanism (Ritz et al., 2000, 2004).”
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Cadiou, H., & McNaughton, P. A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0423.focus · Cited by 71
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“This property of the avian magnetic compass remained unexplained until Ritz et al. (2000) forwarded the ‘Radical Pair’ model of magnetoreception.”
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“2008; Solov’yov & Schulten 2009), that cryptochrome molecules may be the primary sensory molecules behind this mechanism (Ritz et al. 2000; Möller et al. 2004; Mouritsen et al. 2004; Liedvogel et al. 2007a; Maeda et al. 2008), that cluster N is involved in the magnetic compass information processing circuit (Mouritsen…”
BackgroundInfluentialTwo Different Types of Light-Dependent Responses to Magnetic Fields in Birds
Wiltschko, R., Ritz, T., Stapput, K., Thalau, P., & Wiltschko, W. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.037 · Cited by 66
“triplets depending on the alignment of the respective molecules in the ambient magnetic field (for details, see [ 1 ]).”
InfluentialSelf-citationThe Magnetic Compass of Birds: The Role of Cryptochrome
Wiltschko, R., Nießner, C., & Wiltschko, W. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.667000 · Cited by 65
How the Geomagnetic Field Influences Life on Earth – An Integrated Approach to Geomagnetobiology
Erdmann, W., Kmita, H., Kosicki, J. Z., & Kaczmarek, L. D. (2021) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-021-09612-5 · Cited by 66
Essential elements of radical pair magnetosensitivity in Drosophila
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Magnetoreception in microorganisms and fungi
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Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata
Keary, N., Ruploh, T., Voss, J., Thalau, P., Wiltschko, R., Wiltschko, W., & Bischof, H. (2009) · Frontiers in Zoology · doi:10.1186/1742-9994-6-25 · Cited by 65
“Cryptochrome, a photopigment with a flavin as photoactive chromophore [27], has been suggested by Ritz et al. [21] as a candidate.”
BackgroundInfluentialAnt antennae: are they sites for magnetoreception?
de Oliveira, J. F., Wajnberg, E., Esquivel, D. M. S., Weinkauf, S., Michael Winklhofer, A., & Hanzlik, M. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2009.0102 · Cited by 65
“The radical-pair hypothesis assumes a special class of molecules that undergo magnetically anisotropic chemical reactions as the basis for the magnetic compass sense (Ritz et al. 2000, 2004; Maeda et al. 2008).”
BackgroundCryptochrome 1 in Retinal Cone Photoreceptors Suggests a Novel Functional Role in Mammals
Nießner, C., Denzau, S., Malkemper, E. P., Gross, J. C., Burda, H., Winklhofer, M., & Peichl, L. (2016) · Scientific Reports · doi:10.1038/srep21848 · Cited by 65
Quantum limits for the magnetic sensitivity of a chemical compass
Cai, J., Caruso, F., & Plenio, M. B. (2012) · Physical Review A · doi:10.1103/physreva.85.040304 · Cited by 63
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Levitt, B. B., Lai, H. C., & Manville, A. M. (2021) · Reviews on Environmental Health · doi:10.1515/reveh-2021-0050 · Cited by 68
Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields
Irwin, W. P., & Lohmann, K. J. (2005) · Journal of Comparative Physiology A · doi:10.1007/s00359-005-0609-9 · Cited by 63
“A second hypothesis is that magnetoreception involves chemical reactions that are modulated by earthstrength magnetic fields (Leask 1977; Schulten and Windemuth 1996; Deutschlander et al. 1999; Ritz et al. 2000, 2002).”
BackgroundSpin relaxation of radicals in cryptochrome and its role in avian magnetoreception
Worster, S. B., Kattnig, D. R., & Hore, P. J. (2016) · The Journal of Chemical Physics · doi:10.1063/1.4958624 · Cited by 63
Thöing, C., Oldemeyer, S., & Kottke, T. (2015) · Journal of the American Chemical Society · doi:10.1021/jacs.5b01404 · Cited by 62
Effects of disorder and motion in a radical pair magnetoreceptor
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“Ritz et al. (2000) proposed that magnetically sensitive radical pairs are produced photochemically in cryptochrome proteins (Sancar 2003; Lin & Todo 2005; Partch & Sancar 2005) in the retina.”
BackgroundInfluentialStatic magnetic field regulates Arabidopsis root growth via auxin signaling
Jin, Y., Guo, W., Hu, X., Liu, M., Xu, X., Hu, F., Lan, Y., Lv, C., Fang, Y., Liu, M., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-50970-y · Cited by 62
Avian Navigation: A Combination of Innate and Learned Mechanisms
Wiltschko, R., & Wiltschko, W. (2015) · Advances in the study of behavior · doi:10.1016/bs.asb.2014.12.002 · Cited by 62
Radio Frequency Magnetic Field Effects on Electron-Hole Recombination
Woodward, J. R., Timmel, C. R., McLauchlan, K. A., & Hore, P. J. (2001) · Physical Review Letters · doi:10.1103/physrevlett.87.077602 · Cited by 62
Запорожан, В. М., & Ponomarenko, A. (2010) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph7030938 · Cited by 63
“However, convincing hypotheses and explanations of pertinent mechanisms have been presented in [19,28,32-34], among others.”
BackgroundThe threat of global mercury pollution to bird migration: potential mechanisms and current evidence
Seewagen, C. L. (2018) · Ecotoxicology · doi:10.1007/s10646-018-1971-z · Cited by 61
“In contrast, photoexcitation of cryptochrome molecules in the eyes of night-migrants creates a radical pair process (see Ritz et al. 2000) through which birds are believed to visually perceive the inclination of magnetic fields and thereby distinguish north from south (Mouritsen et al. 2005;…”
BackgroundLeberecht, B., Kobylkov, D., Karwinkel, T., Döge, S., Burnus, L., Wong, S. Y., Apte, S., Haase, K., Musielak, I., Chetverikova, R., et al. (2022) · Journal of Comparative Physiology A · doi:10.1007/s00359-021-01537-8 · Cited by 61
Waved albatrosses can navigate with strong magnets attached to their head
Mouritsen, H., Huyvaert, K. P., Frost, B. J., & Anderson, D. J. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00650 · Cited by 61
“However, it could be argued that if birds use a radical-pair, light-mediated, magnetoreception mechanism (Ritz et al., 2000), they may be able to use the geomagnetic field as a compass even in the presence of a strong stationary magnet, since the ghost images hypothesised by Ritz et al. (2000) may…”
BackgroundNight‐time neuronal activation of Cluster N in a day‐ and night‐migrating songbird
Zapka, M., Heyers, D., Liedvogel, M., Jarvis, E. D., & Mouritsen, H. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07311.x · Cited by 61
“If a cryptochrome is the primary magnetoreceptor (Ritz et al., 2000; Möller et al., 2004; Mouritsen et al., 2004a; Liedvogel et al., 2007b; Maeda et al., 2008), then cryptochromes located in the ganglion cells and ⁄ or in the photoreceptor cells of the eye are good candidates (Mouritsen et al.”
BackgroundInfluentialMagnetic Sensing through the Abdomen of the Honey bee
Liang, C.-H., Chuang, C.-L., Jiang, J., & Yang, E. (2016) · Scientific Reports · doi:10.1038/srep23657 · Cited by 60
Magnetocarcinogenesis: is there a mechanism for carcinogenic effects of weak magnetic fields?
Juutilainen, J., Herrala, M., Luukkonen, J., Naarala, J., & Hore, P. J. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0590 · Cited by 62
Kerpal, C., Richert, S., Storey, J. G., Pillai, S., Liddell, P. A., Gust, D., Mackenzie, S. R., Hore, P. J., & Timmel, C. R. (2019) · Nature Communications · doi:10.1038/s41467-019-11655-2 · Cited by 60
Albert, L., Deschamps, F., Jolivet, A., Olivier, F., Laurent Chauvaud, A., & Chauvaud, S. (2020) · Marine Environmental Research · doi:10.1016/j.marenvres.2020.104958 · Cited by 59
“(Ritz et al., 2000; Schulten et al., 1978) involving chemical reactions within the visual system , 24”
BackgroundRastogi, A., Kumari, Y., Rani, S., & Kumar, V. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07737.x · Cited by 59
“In contrast, it seems that night-migratory songbirds use a vision-mediated pathway acting via cryptochromes in the retinal ganglion cells (RGCs) and ⁄ or photoreceptors to find their direction (Ritz et al., 2000; Möller et al., 2004; Mouritsen et al., 2004; Mouritsen & Ritz, 2005).”
BackgroundPhillips, J. B., Borland, S. C., Freake, M. J., Brassart, J., & Kirschvink, J. L. (2002) · Journal of Experimental Biology · doi:10.1242/jeb.205.24.3903 · Cited by 59
Insight into shark magnetic field perception from empirical observations
Anderson, J. M., Clegg, T. M., de Queiroz-Véras, L. V. M. V., & Holland, K. N. (2017) · Scientific Reports · doi:10.1038/s41598-017-11459-8 · Cited by 59
Timmel, C. R., Cintolesi, F., Brocklehurst, B., & Hore, P. J. (2001) · Chemical Physics Letters · doi:10.1016/s0009-2614(00)01436-6 · Cited by 59
Chirality-Induced Spin Coherence in Electron Transfer Reactions
Fay, T. P. (2021) · The Journal of Physical Chemistry Letters · doi:10.1021/acs.jpclett.1c00009 · Cited by 61
Gagliardo, A., Ioalè, P., Savini, M., & Wild, M. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.031864 · Cited by 58
“Although it is a common opinion that geomagnetic compass orientation is mediated by the cryptochromes of the retina (Ritz et al., 2000; Wiltschko and Wiltschko, 2005), a possible involvement of the trigeminal system in determining a magnetic directional reference has not been experimentally…”
BackgroundEffects of weak static magnetic fields on the gene expression of seedlings of Arabidopsis thaliana
Dhiman, S. K., & Galland, P. (2018) · Journal of Plant Physiology · doi:10.1016/j.jplph.2018.08.016 · Cited by 58
Holland, R. A., & Helm, B. (2013) · Journal of The Royal Society Interface · doi:10.1098/rsif.2012.1047 · Cited by 57
The neural mechanisms of long distance animal navigation
Frost, B. J., & Mouritsen, H. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.06.005 · Cited by 60
“Chemical magnetoreception requiring light and being mediated by radical-pair processes (a radical-pair involves two spatially-separated, unpaired electrons) [70] has received strong experimental support as the basis of the magnetic compass of night-migratory songbirds.”
BackgroundBabcock, N. S., & Kattnig, D. R. (2020) · The Journal of Physical Chemistry Letters · doi:10.1021/acs.jpclett.0c00370 · Cited by 59
Theoretical Analysis of an Iron Mineral-Based Magnetoreceptor Model in Birds
Solov’yov, I. A., & Greiner, W. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.105098 · Cited by 57
“The two most likely candidates are a chemical reaction mechanism involving a specialized photoreceptor molecule called the radical pair model (21,22) and an iron-mineralbased model (23–33).”
BackgroundMagnetoreception of Directional Information in Birds Requires Nondegraded Vision
Stapput, K., Güntürkün, O., Hoffmann, K., Wiltschko, R., & Wiltschko, W. (2010) · Current Biology · doi:10.1016/j.cub.2010.05.070 · Cited by 56
Photoactivation of the cryptochrome/photolyase superfamily
Wang, J., Du, X., Pan, W., Wang, X., & Wu, W. (2014) · Journal of Photochemistry and Photobiology C Photochemistry Reviews · doi:10.1016/j.jphotochemrev.2014.12.001 · Cited by 60
Migratory bats respond to artificial green light with positive phototaxis
Voigt, C. C., Roeleke, M., Marggraf, L. C., Pētersons, G., & Voigt‐Heucke, S. L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177748 · Cited by 56
Variation in morphology and performance of predator-sensing system in wild cricket populations
Dangles, O. J., Magal, C., Pierre, D., Olivier, A., & Casas, J. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01369 · Cited by 56
“To our knowledge, none of the numerous models built to understand animal perception (Neumann, 2002; Ritz et al., 2000; Svensen and Kiorboel, 2000; Erwin et al., 2001), has ever incorporated the potential structural variability of a sensor to predict consequences on the performance of animals.”
BackgroundLateralized response of chicks to magnetic cues
Rogers, L. J., Munro, U. H., Freire, R., Wiltschko, R., & Wiltschko, W. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.029 · Cited by 55
“Given the hypothesis of light-dependent magnetoreception in birds (Ritz et al, 2000), this distinction is particularly important because inability to detect magnetic cues when using one eye would indicate that the photo-pigment involved is not present in that eye.”
Magnetic compass in the cornea: local anaesthesia impairs orientation in a mammal
Wegner, R., Begall, S., & Burda, H. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02573 · Cited by 55
“The first is based on retinal chemo-physical radical-pair reactions (Ritz et al., 2000), a system suggested as the primary signal transduction process for migratory birds (Ritz et al., 2004).”
BackgroundLight Reflection Control in Biogenic Micro-Mirror by Diamagnetic Orientation
Iwasaka, M., & Mizukawa, Y. (2013) · Langmuir · doi:10.1021/la400046a · Cited by 55
Xu, Y., & Mi, W. (2023) · Materials Horizons · doi:10.1039/d3mh00024a · Cited by 56
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Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle
Nießner, C., Denzau, S., Peichl, L., Wiltschko, W., & Wiltschko, R. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.110965 · Cited by 54
“The Radical Pair Model (Ritz et al., 2000) proposes that the sensing of magnetic direction in birds is based on radical pair processes, with cryptochrome as receptor molecule.”
BackgroundInfluentialIdentifying Cellular and Molecular Mechanisms for Magnetosensation
Clites, B. L., & Pierce-Shimomura, J. T. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031312 · Cited by 53
Hafeez, M. B., Zahra, N., Ahmad, N., Shi, Z., Raza, A., Wang, X., & Li, J. (2022) · Plant Biology · doi:10.1111/plb.13459 · Cited by 53
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“…the geomagnetic field of 25–60 lT is linked to the effect of magnetic fields on electron transfer reactions of photoreceptors through radical-pair processes (Ritz et al. 2000), with the blue-light receptor cryptochrome suggested as a promising candidate for the receptor molecule (Ritz et al. 2000).”
BackgroundLau, J. C. S., Rodgers, C. T., & Hore, P. J. (2012) · Journal of The Royal Society Interface · doi:10.1098/rsif.2012.0374 · Cited by 52
Müller, P., Ignatz, E., Kiontke, S., Brettel, K., & Essen, L. (2017) · Chemical Science · doi:10.1039/c7sc03969g · Cited by 53
Diamond-based single-molecule magnetic resonance spectroscopy
Cai, J., Jelezko, F., Plenio, M. B., & Retzker, A. (2013) · OPen Access Repositorium der Universität Ulm (OPARU) (Ulm University) · doi:10.18725/oparu-46884 · Cited by 53
Fuelling decisions in migratory birds: geomagnetic cues override the seasonal effect
Kullberg, C., Henshaw, I., Jakobsson, S., Johansson, P., & Fransson, T. (2007) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2007.0554 · Cited by 53
“We used juvenile European robins (Erithacus rubecula) to study whether geomagnetic cues affect fuel deposition in a medium-distance migrant by simulating a migratory journey from southeast Sweden to the wintering area in southern Spain.”
MethodInfluentialAdvances in Electromagnetic Fields in Living Systems
Lin, J. C. (2009) · Advances in electromagnetic fields in living systems · doi:10.1007/978-0-387-92736-7 · Cited by 53
Night-Migratory Songbirds Possess a Magnetic Compass in Both Eyes
Engels, S., Hein, C. M., Lefeldt, N., Prior, H., & Mouritsen, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043271 · Cited by 52
“The direction of the Earth’s magnetic field is supposedly sensed by radical pair-forming, light-dependent photopigments in the birds eyes [4,11–20] and then processed in Cluster N, a specialized, night-time active, light-processing forebrain region [9,21–24] which is required for magnetic compass orientation [10].”
BackgroundNo evidence for magnetic field effects on the behaviour of Drosophila
Bassetto, M., Reichl, T., Kobylkov, D., Kattnig, D. R., Michael Winklhofer, A., Hore, P. J., & Mouritsen, H. (2023) · Nature · doi:10.1038/s41586-023-06397-7 · Cited by 53
Magnetic orientation of garden warblers ( Sylvia borin ) under 1.4 MHz radiofrequency magnetic field
Kavokin, K. V., Chernetsov, N., Pakhomov, A. Y., Bojarinova, J., Kobylkov, D., & Namozov, B. R. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0451 · Cited by 52
“Based, again, mainly on laboratory experiments with birds, two theoretical models of magnetoreception in terrestrial animals were singled out as the most viable: one involving magnetic nanocrystals of iron oxides [11] and the other based on magneto-sensitive photochemical reactions in the eye [12,13] (the radical-pair…”
BackgroundNohr, D., Paulus, B., Rodriguez, R., Okafuji, A., Bittl, R., Schleicher, E., & Weber, S. (2017) · Angewandte Chemie International Edition · doi:10.1002/anie.201700389 · Cited by 52
Bird navigation: what type of information does the magnetite-based receptor provide?
Wiltschko, W., Munro, U. H., FORD, H. A., & Wiltschko, R. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3651 · Cited by 52
“…by particles of magnetite (Yorke 1979; Kirschvink & Gould 1981; and others), whereas the radical pair model suggests that magnetic input is mediated by magnetically sensitive chemical processes involving specialized photo pigments (Schulten & Windemuth 1986, later detailed in Ritz et al. 2000).”
BackgroundDifferential effects of magnetic pulses on the orientation of naturally migrating birds
Holland, R. A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2010.0159 · Cited by 52
Cellular metabolites modulate in vivo signaling of Arabidopsis cryptochrome-1
El-Esawi, M. A., Glascoe, A., Engle, D., Ritz, T., Link, J. J., & Ahmad, M. (2015) · Plant Signaling & Behavior · doi:10.1080/15592324.2015.1063758 · Cited by 51
Self-citationCailliez, F., Müller, P., Firmino, T. D. R., Pernot, P., & de la Lande, A. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.5b10938 · Cited by 51
Nießner, C., Gross, J. C., Denzau, S., Peichl, L., Fleissner, G., Wiltschko, W., & Wiltschko, R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150377 · Cited by 50
“Because of this, they were proposed as potential receptor molecules for sensing magnetic directions in the Radical Pair Model of magnetoreception [3].”
BackgroundInfluentialATP Binding and Aspartate Protonation Enhance Photoinduced Electron Transfer in Plant Cryptochrome
Cailliez, F., Müller, P., Gallois, M., & de la Lande, A. (2014) · Journal of the American Chemical Society · doi:10.1021/ja506084f · Cited by 51
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O'Dea, A. R., Curtis, A. F., Green, N. J. B., Timmel, C. R., & Hore, P. J. (2005) · The Journal of Physical Chemistry A · doi:10.1021/jp0456943 · Cited by 51
Are stress responses to geomagnetic storms mediated by the cryptochrome compass system?
Close, J. (2012) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2012.0324 · Cited by 49
Polarized light modulates light-dependent magnetic compass orientation in birds
Muheim, R., Sjöberg, S., & Pinzon-Rodriguez, A. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513391113 · Cited by 50
“Cryptochromes have been proposed as putative candidate receptor molecules (8, 14) and found to be expressed in the retinas of birds exhibiting magnetic orientation behavior (15–17).”
BackgroundInfluentialBiological effects related to geomagnetic activity and possible mechanisms
Крылов, В. В. (2017) · Bioelectromagnetics · doi:10.1002/bem.22062 · Cited by 50
“Representatives of several taxa developed this tool over the course of evolution, producing a magnetic sense useful for spatial orientation [Ritz et al., 2000; Wiltschko et al., 2007; Zapka et al., 2009; Mouritsen and Hore, 2012].”
BackgroundMethodMagnetoreception in birds: Different physical processes for two types of directional responses
Wiltschko, R., Stapput, K., Ritz, T., Thalau, P., & Wiltschko, W. (2007) · HFSP journal · doi:10.2976/1.2714294 · Cited by 50
Self-citationTracking the Electron Transfer Cascade in European Robin Cryptochrome 4 Mutants
Timmer, D., Frederiksen, A., Lünemann, D. C., Thomas, A. R., Xu, J., Bartölke, R., Schmidt, J., Kubař, T., Sio, A. D., Solov’yov, I. A., et al. (2023) · Journal of the American Chemical Society · doi:10.1021/jacs.3c00442 · Cited by 49
Zebra finches have a light-dependent magnetic compass similar to migratory birds
Pinzon-Rodriguez, A., & Muheim, R. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.148098 · Cited by 49
“how the birds perceive and interpret the magnetic modulation pattern proposed to be produced by a radical-pair-based magnetic compass (Ritz et al., 2000; Phillips et al., 2010b).”
BackgroundInfluentialMichael Winklhofer, A. (2010) · Journal of The Royal Society Interface · doi:10.1098/rsif.2010.0010.focus · Cited by 49
Nontrivial quantum and quantum-like effects in biosystems: Unsolved questions and paradoxes
Melkikh, A. V., & Khrennikov, A. Y. (2015) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2015.07.001 · Cited by 49
A light-dependent magnetoreception mechanism insensitive to light intensity and polarization
Worster, S. B., Mouritsen, H., & Hore, P. J. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0405 · Cited by 46
“Previous studies have recognized that a high degree of immobilization and some degree of alignment among the magnetoreceptors is likely to be required for direction sensing [2,34,48,66].”
BackgroundBerntsson, O., Rodriguez, R., Henry, L., Panman, M. R., Hughes, A. J., Einholz, C., Weber, S., Ihalainen, J. A., Henning, R. W., Kosheleva, I., et al. (2019) · Science Advances · doi:10.1126/sciadv.aaw1531 · Cited by 46
Bolte, P., Einwich, A., Seth, P. K., Chetverikova, R., Heyers, D., Wojahn, I., Janssen‐Bienhold, U., Feederle, R., Hore, P. J., Dedek, K., et al. (2021) · Ethology Ecology & Evolution · doi:10.1080/03949370.2020.1870571 · Cited by 48
“This so-called radical pair theory suggests that photon absorption in specialised magnetoreceptor molecules leads to electron transfer reactions and the subsequent formation of a long-lived radical pair (Schulten et al. 1978; Ritz et al. 2000; Maeda et al. 2008; Hore & Mouritsen 2016).”
BackgroundInfluentialLeberecht, B., Wong, S. Y., Satish, B., Döge, S., Hindman, J., Venkatraman, L., Apte, S., Haase, K., Musielak, I., Dautaj, G., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301153120 · Cited by 47
The puzzle of magnetic resonance effect on the magnetic compass of migratory birds
Kavokin, K. V. (2009) · Bioelectromagnetics · doi:10.1002/bem.20485 · Cited by 47
“…the magnetic field is attributed to the anisotropy of the hyperfine interaction with respect to structural axes of the molecule: the molecules are assumed to be spatially fixed and oriented uniformly, in order to make the overall reaction yield a function of the field direction [Ritz et al 2000].”
BackgroundMethodInfluentialThe use of the geomagnetic field for short distance orientation in zebra finches
Voss, J., Keary, N., & Bischof, H. (2007) · Neuroreport · doi:10.1097/wnr.0b013e32818b2a21 · Cited by 47
“The Earth’s magnetic field may be perceived using a ‘radical pair’ mechanism acting in pigments (probably cryptochrome) located in the photoreceptors of the visual system [15,16].”
BackgroundBreus, T. K., Binhi, V. N., & Petrukovich, A. A. (2016) · Physics-Uspekhi · doi:10.3367/ufne.2015.12.037693 · Cited by 47
Kobylkov, D., Wynn, J., Michael Winklhofer, A., Chetverikova, R., Xu, J., Hiscock, H. G., Hore, P. J., & Mouritsen, H. (2019) · Journal of The Royal Society Interface · doi:10.1098/rsif.2019.0716 · Cited by 47
Iron-mineral-based magnetoreception in birds: the stimulus conducting system
Fleissner, G., Fleissner, G., Stahl, B., & Falkenberg, G. (2007) · Journal für Ornithologie · doi:10.1007/s10336-007-0229-y · Cited by 46
“Experiments performed for example with birds (Wiltschko et al. 2006) and newts (Phillips et al. 2002) have provided evidence for such a composite magnetosensory system with two mechanisms, based on a blue photopigment (cryptochrome: Ritz et al. 2000 ), as well as on magnetite (Kirschvink and Gould 1981).”
BackgroundAnimal navigation: how animals use environmental factors to find their way
Wiltschko, R., & Wiltschko, W. (2022) · The European Physical Journal Special Topics · doi:10.1140/epjs/s11734-022-00610-w · Cited by 46
Landler, L., Painter, M. S., Youmans, P. W., Hopkins, W. A., & Phillips, J. B. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124728 · Cited by 46
“, cryptochromes) has been suggested to play a central role in the RPM [10–13] with the alignment of the magnetic field modulating the response of these photopigments to light [14].”
BackgroundRapid Learning of Magnetic Compass Direction by C57BL/6 Mice in a 4-Armed ‘Plus’ Water Maze
Phillips, J. B., Youmans, P. W., Muheim, R., Sloan, K. A., Landler, L., Painter, M. S., & Anderson, C. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073112 · Cited by 46
“As a consequence, the response of photoreceptors containing an ordered array of light-activated cryptochrome molecules may show a complex dependence on magnetic field alignment [34,41,42].”
BackgroundInfluentialMagnetic field-driven induction of ZENK in the trigeminal system of pigeons ( Columba livia )
Lefeldt, N., Heyers, D., Schneider, N.-L., Engels, S., Elbers, D., & Mouritsen, H. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0777 · Cited by 46
“Currently, three main magnetoreception hypotheses are discussed: a light-dependent chemical compass sense associated with the visual system [3–10], a recently suggested involvement of the vestibular system [11–15] but see [16], and an iron-mineral-based sense located in the upper beak [17–20].”
BackgroundQuantum coherence in photosynthesis
Engel, G. S. (2011) · Procedia Chemistry · doi:10.1016/j.proche.2011.08.029 · Cited by 49
Xu, C., Lv, Y., Chen, C., Zhang, Y., & Wei, S. (2014) · Advances in Space Research · doi:10.1016/j.asr.2014.01.033 · Cited by 46
Murakami, M., Maeda, K., & Arai, T. (2005) · The Journal of Physical Chemistry A · doi:10.1021/jp0519722 · Cited by 46
Cryptochrome: A photoreceptor with the properties of a magnetoreceptor?
Ritz, T., Yoshii, T., Foerster, C., & Ahmad, M. (2010) · Communicative & Integrative Biology · doi:10.4161/cib.3.1.9865 · Cited by 45
“If the internal magnetic fields are anisotropic, then the effect of the geomagnetic field depends not only on its intensity, but also on its direction, thereby potentially creating a magnetic compass.(5) The physical chemistry of this mechanism is well understood(6) and one can even design molecules that are sensitive…”
BackgroundSelf-citation
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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