The Radical-Pair Mechanism of Magnetoreception.

Although it has been known for almost half a century that migratory birds can detect the direction of the Earth's magnetic field, the primary sensory mechanism behind this remarkable feat is still unclear. The leading hypothesis centers on radical pairs-magnetically sensitive chemical intermediates formed by photoexcitation of cryptochrome proteins in the retina. Our primary aim here is to explain the chemical and physical aspects of the radical-pair mechanism to biologists and the biological and chemical aspects to physicists. In doing so, we review the current state of knowledge on magnetoreception mechanisms. We dare to hope that this tutorial will stimulate new interdisciplinary experimental and theoretical work that will shed much-needed additional light on this fascinating problem in sensory biology.

[1]  Simon C Benjamin,et al.  A new type of radical-pair-based model for magnetoreception. , 2010, Biophysical journal.

[2]  P. Hore,et al.  Chemical magnetoreception in birds: The radical pair mechanism , 2009, Proceedings of the National Academy of Sciences.

[3]  Allan R. Jones,et al.  A High-Resolution Spatiotemporal Atlas of Gene Expression of the Developing Mouse Brain , 2014, Neuron.

[4]  A. Buchachenko Magnetic Isotope Effect in Chemistry and Biochemistry , 2009 .

[5]  Henrik Mouritsen,et al.  Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds , 2010, PloS one.

[6]  Martin B. Plenio,et al.  Quantum limits for the magnetic sensitivity of a chemical compass , 2012 .

[7]  Vlatko Vedral,et al.  Living in a quantum world. , 2011, Scientific American.

[8]  Steven M. Reppert,et al.  Human cryptochrome exhibits light-dependent magnetosensitivity , 2011, Nature communications.

[9]  Henrik Mouritsen,et al.  Migratory blackcaps tested in Emlen funnels can orient at 85 degrees but not at 88 degrees magnetic inclination , 2015, Journal of Experimental Biology.

[10]  John R. Pannell,et al.  Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana , 2009, Journal of The Royal Society Interface.

[11]  Henrik Mouritsen,et al.  Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know? , 2010, Journal of The Royal Society Interface.

[12]  R. Blakemore,et al.  Magnetite and magnetotaxis in microorganisms. , 1988, Advances in Experimental Medicine and Biology.

[13]  A. Sancar,et al.  Mechanism of Photosignaling by Drosophila Cryptochrome , 2013, The Journal of Biological Chemistry.

[14]  Klaus Schulten,et al.  A Biomagnetic Sensory Mechanism Based on Magnetic Field Modulated Coherent Electron Spin Motion , 1978 .

[15]  How-Jing Lee,et al.  Cryptochrome 2 mediates directional magnetoreception in cockroaches , 2016, Proceedings of the National Academy of Sciences.

[16]  H. Mouritsen The Magnetic Senses , 2013 .

[17]  K. Lohmann,et al.  The magnetic map of hatchling loggerhead sea turtles , 2012, Current Opinion in Neurobiology.

[18]  S. Kais,et al.  Quantum coherence and entanglement in the avian compass. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  J. Bouly,et al.  Light-induced Electron Transfer in Arabidopsis Cryptochrome-1 Correlates with in Vivo Function* , 2005, Journal of Biological Chemistry.

[20]  Henrik Mouritsen,et al.  Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H Mouritsen,et al.  A mathematical expectation model for bird navigation based on the clock-and-compass strategy. , 2000, Journal of theoretical biology.

[22]  P. Berthold A comprehensive theory for the evolution, control and adaptability of avian migration , 1999 .

[23]  J. Massagué TGF-beta signal transduction. , 1998, Annual review of biochemistry.

[24]  H. Mouritsen,et al.  Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird , 2014, Nature.

[25]  R. Muheim,et al.  Polarized light modulates light-dependent magnetic compass orientation in birds , 2016, Proceedings of the National Academy of Sciences.

[26]  Richard A. Holland,et al.  True navigation in birds: from quantum physics to global migration , 2014 .

[27]  A. Davila,et al.  A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite , 2003 .

[28]  L. Peichl,et al.  Seasonally Changing Cryptochrome 1b Expression in the Retinal Ganglion Cells of a Migrating Passerine Bird , 2016, PloS one.

[29]  H. Mouritsen Magnetoreception in birds and its use for long-distance migration , 2022, Sturkie's Avian Physiology.

[30]  C. Dodson,et al.  A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. , 2013, Trends in biochemical sciences.

[31]  H. Mouritsen,et al.  Weak Broadband Electromagnetic Fields are More Disruptive to Magnetic Compass Orientation in a Night-Migratory Songbird (Erithacus rubecula) than Strong Narrow-Band Fields , 2016, Front. Behav. Neurosci..

[32]  Steven M. Reppert,et al.  Cryptochrome mediates light-dependent magnetosensitivity in Drosophila , 2008, Nature.

[33]  Joseph L. Kirschvink,et al.  A quantitative assessment of torque-transducer models for magnetoreception , 2010, Journal of The Royal Society Interface.

[34]  Hynek Burda,et al.  The magnetic compass mechanisms of birds and rodents are based on different physical principles , 2006, Journal of The Royal Society Interface.

[35]  V. Tarasov,et al.  Chapter One - Time-Resolved Electron Paramagnetic Resonance Spectroscopy: History, Technique, and Application to Supramolecular and Macromolecular Chemistry , 2013 .

[36]  Philipp Kukura,et al.  Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. , 2005, The journal of physical chemistry. A.

[37]  Dr. Roswitha Wiltschko,et al.  Magnetic Orientation in Animals , 1995, Zoophysiology.

[38]  Ilya Kuprov,et al.  Chemical compass model of avian magnetoreception , 2008, Nature.

[39]  P. Hore,et al.  Effects of disorder and motion in a radical pair magnetoreceptor , 2010, Journal of the Royal Society Interface.

[40]  D. Manolopoulos,et al.  Asymmetric recombination and electron spin relaxation in the semiclassical theory of radical pair reactions. , 2014, The Journal of chemical physics.

[41]  A. Perdeck,et al.  Two Types of Orientation in Migrating Starlings, Sturnus yulgaris L., and Chaffinches, Fringilla coelebs L., as Revealed by Displacement Experiments , 1958 .

[42]  K.V.Kavokin The puzzle of magnetic resonance effect on the magnetic compass of migratory birds , 2008, 0808.2401.

[43]  Swati Tiwari,et al.  Photobiology , 2002, Springer Netherlands.

[44]  L. Essen,et al.  Cellular Metabolites Enhance the Light Sensitivity of Arabidopsis Cryptochrome through Alternate Electron Transfer Pathways[C][W][OPEN] , 2014, Plant Cell.

[45]  Aziz Sancar,et al.  Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. , 2003, Chemical reviews.

[46]  Beason,et al.  Does the avian ophthalmic nerve carry magnetic navigational information? , 1996, The Journal of experimental biology.

[47]  W. Wiltschko,et al.  Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons , 2003, The Journal of comparative neurology.

[48]  R. Bittl,et al.  The Signaling State of Arabidopsis Cryptochrome 2 Contains Flavin Semiquinone* , 2007, Journal of Biological Chemistry.

[49]  H. Mouritsen Sensory biology: Search for the compass needles , 2012, Nature.

[50]  Danielle E. Chandler,et al.  Magnetic field effects in Arabidopsis thaliana cryptochrome-1. , 2007, Biophysical journal.

[51]  C. Rodgers Magnetic field effects in chemical systems , 2009 .

[52]  Kurt Warncke,et al.  Nature of biological electron transfer , 1992, Nature.

[53]  J. Lind,et al.  Bird migration: Magnetic cues trigger extensive refuelling , 2001, Nature.

[54]  Taijiao Jiang,et al.  A magnetic protein biocompass. , 2016, Nature materials.

[55]  H. Mouritsen,et al.  Localisation of the Putative Magnetoreceptive Protein Cryptochrome 1b in the Retinae of Migratory Birds and Homing Pigeons , 2016, PloS one.

[56]  S. Kais,et al.  The Radical Pair Mechanism and the Avian Chemical Compass: Quantum Coherence and Entanglement , 2015, 1502.00671.

[57]  Margaret Ahmad,et al.  Light-activated Cryptochrome Reacts with Molecular Oxygen to Form a Flavin–Superoxide Radical Pair Consistent with Magnetoreception* , 2011, The Journal of Biological Chemistry.

[58]  A. Bacher,et al.  Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase , 2008, Proceedings of the National Academy of Sciences.

[59]  Thorsten Ritz,et al.  Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field , 2005, Naturwissenschaften.

[60]  Onkar S. Dhande,et al.  Retinal ganglion cell maps in the brain: implications for visual processing , 2014, Current Opinion in Neurobiology.

[61]  Frank Noé,et al.  Higher-order architecture of rhodopsin in intact photoreceptors and its implication for phototransduction kinetics. , 2015, Structure.

[62]  K. Schulten,et al.  Decrypting cryptochrome: revealing the molecular identity of the photoactivation reaction. , 2012, Journal of the American Chemical Society.

[63]  P. Atkins,et al.  Spin polarization and magnetic effects in radical reactions , 1984 .

[64]  Wolfgang Wiltschko,et al.  Red light disrupts magnetic orientation of migratory birds , 1993, Nature.

[65]  Henrik Mouritsen,et al.  Eurasian reed warblers compensate for virtual magnetic displacement , 2015, Current Biology.

[66]  Harald Luksch,et al.  A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds , 2007, PloS one.

[67]  J. Clausen,et al.  Approaches to Measuring Entanglement in Chemical Magnetometers , 2013, The journal of physical chemistry. A.

[68]  U. Kaupp,et al.  Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. , 1992, Annual review of physiology.

[69]  A. Sancar,et al.  Reaction mechanism of Drosophila cryptochrome , 2010, Proceedings of the National Academy of Sciences.

[70]  W. Thoreson The Vertebrate Retina , 2008 .

[71]  H. Mouritsen,et al.  Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes , 2010, Journal of The Royal Society Interface.

[72]  Thorsten Ritz,et al.  Magnetic compass of birds is based on a molecule with optimal directional sensitivity. , 2009, Biophysical journal.

[73]  Anna Gagliardo,et al.  Forty years of olfactory navigation in birds , 2013, Journal of Experimental Biology.

[74]  Michael T. Wilson,et al.  Kinetic studies on the oxidation of semiquinone and hydroquinone forms of Arabidopsis cryptochrome by molecular oxygen , 2015, FEBS open bio.

[75]  K. Schulten,et al.  A model for photoreceptor-based magnetoreception in birds. , 2000, Biophysical journal.

[76]  P. Hore,et al.  Entanglement and sources of magnetic anisotropy in radical pair-based avian magnetoreceptors. , 2012, Physical review letters.

[77]  T. Ritz,et al.  The cryptochromes: blue light photoreceptors in plants and animals. , 2011, Annual review of plant biology.

[78]  R. Bittl,et al.  Lifetimes of Arabidopsis cryptochrome signaling states in vivo. , 2013, The Plant journal : for cell and molecular biology.

[79]  Steven M. Reppert,et al.  Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism , 2010, Nature.

[80]  Qing Ai,et al.  Sensitive chemical compass assisted by quantum criticality , 2011, 1105.1511.

[81]  H. Hamm,et al.  Heterotrimeric G protein activation by G-protein-coupled receptors , 2008, Nature Reviews Molecular Cell Biology.

[82]  E. Jarvis,et al.  Night-time neuronal activation of Cluster N in a day- and night-migrating songbird , 2010, The European journal of neuroscience.

[83]  S. Mills,et al.  Short-wavelength cone-opponent retinal ganglion cells in mammals , 2014, Visual Neuroscience.

[84]  A. Cohen Nanomagnetic control of intersystem crossing. , 2009, The journal of physical chemistry. A.

[85]  J. Cai Quantum probe and design for a chemical compass with magnetic nanostructures. , 2010, Physical review letters.

[86]  L. Peichl,et al.  Avian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors , 2011, PloS one.

[87]  E. Getzoff,et al.  Unexpected electron transfer in cryptochrome identified by time-resolved EPR spectroscopy. , 2011, Angewandte Chemie.

[88]  W. Wiltschko,et al.  Directional orientation of birds by the magnetic field under different light conditions , 2010, Journal of The Royal Society Interface.

[89]  Henrik Mouritsen,et al.  The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds , 2012, Current Opinion in Neurobiology.

[90]  A. Kappers Avian brains and a new understanding of vertebrate brain evolution , 2022 .

[91]  Chad A Brautigam,et al.  Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[92]  R. Frankel,et al.  Magnetosome formation in prokaryotes , 2004, Nature Reviews Microbiology.

[93]  Michael Winklhofer,et al.  Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons evidence of a magnetoreceptor? , 2001 .

[94]  R. Bittl,et al.  The photoinduced triplet of flavins and its protonation states. , 2004, Journal of the American Chemical Society.

[95]  H. Mouritsen,et al.  A Double-Clock or Jetlag Mechanism is Unlikely to be Involved in Detection of East—West Displacements in a Long-Distance Avian Migrant , 2010 .

[96]  E. Getzoff,et al.  Light-induced conformational changes in full-length Arabidopsis thaliana cryptochrome. , 2011, Journal of molecular biology.

[97]  Henrik Mouritsen,et al.  Night-vision brain area in migratory songbirds. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[98]  W. Wiltschko,et al.  Navigation in Birds and Other Animals , 1993, Journal of Navigation.

[99]  C. Timmel,et al.  Possible involvement of superoxide and dioxygen with cryptochrome in avian magnetoreception: Origin of Zeeman resonances observed by in vivo EPR spectroscopy , 2009 .

[100]  Thorsten Ritz,et al.  Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor , 2003 .

[101]  R. Holland Differential effects of magnetic pulses on the orientation of naturally migrating birds , 2010, Journal of The Royal Society Interface.

[102]  Masoud Mohseni,et al.  Quantum Effects in Biology , 2019, Optics and Photonics News.

[103]  M. Hastings,et al.  Genetic Analysis of Circadian Responses to Low Frequency Electromagnetic Fields in Drosophila melanogaster , 2014, PLoS genetics.

[104]  D. Stass,et al.  Magnetic Field Effect in the Reaction of Recombination of Nitric Oxide and Superoxide Anion , 2009 .

[105]  L. Peichl,et al.  Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle , 2014, Journal of Experimental Biology.

[106]  P. Hore,et al.  Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. , 2008, Biophysical journal.

[107]  H. Ågren,et al.  Activation of triplet dioxygen by glucose oxidase: Spin-orbit coupling in the superoxide ion , 2002 .

[108]  Henrik Mouritsen,et al.  Spatiotemporal Orientation Strategies of Long-Distance Migrants , 2003 .

[109]  D. Vicario,et al.  Song presentation induces gene expression in the songbird forebrain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[110]  J. L. Gould,et al.  Biogenic magnetite as a basis for magnetic field detection in animals. , 1981, Bio Systems.

[111]  F. Nottebohm,et al.  Motor-driven gene expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[112]  A. Cashmore,et al.  HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor , 1993, Nature.

[113]  S. Chris Borland,et al.  Behavioural evidence for use of a light-dependent magnetoreception mechanism by a vertebrate , 1992, Nature.

[114]  Andrew L. Lee,et al.  Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor. , 2005, Biochemistry.

[115]  H. Mouritsen,et al.  Migratory Reed Warblers Need Intact Trigeminal Nerves to Correct for a 1,000 km Eastward Displacement , 2013, PloS one.

[116]  Henrik Mouritsen,et al.  The neural mechanisms of long distance animal navigation , 2006, Current Opinion in Neurobiology.

[117]  Jim Al-Khalili,et al.  Life on the Edge: The Coming of Age of Quantum Biology , 2014 .

[118]  Andreas R. Pfenning,et al.  Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns , 2013, The Journal of comparative neurology.

[119]  J. Morton,et al.  Sustained quantum coherence and entanglement in the avian compass. , 2009, Physical review letters.

[120]  W. Wiltschko,et al.  Magnetic Compass of European Robins , 1972, Science.

[121]  D. Manolopoulos,et al.  An improved semiclassical theory of radical pair recombination reactions. , 2013, The Journal of chemical physics.

[122]  Joseph L. Kirschvink,et al.  Biophysics of magnetic orientation: strengthening the interface between theory and experimental design , 2010, Journal of The Royal Society Interface.

[123]  Thomas P. Quinn,et al.  Evidence for Geomagnetic Imprinting as a Homing Mechanism in Pacific Salmon , 2013, Current Biology.

[124]  W. Greiner,et al.  Iron-mineral-based magnetoreceptor in birds: polarity or inclination compass? , 2009 .

[125]  H. Mouritsen,et al.  The quantum needle of the avian magnetic compass , 2016, Proceedings of the National Academy of Sciences.

[126]  L. Peichl,et al.  Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds , 2013, Journal of The Royal Society Interface.

[127]  J. Kirschvink,et al.  The magnetic sense and its use in long-distance navigation by animals , 2002, Current Opinion in Neurobiology.

[128]  W. Greiner,et al.  Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. , 2007, Biophysical journal.

[129]  Jian Zou,et al.  Estimating the hyperfine coupling parameters of the avian compass by comprehensively considering the available experimental results. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[130]  Christiane R Timmel,et al.  Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. , 2007, Journal of the American Chemical Society.

[131]  Xuanming Liu,et al.  Arabidopsis cryptochrome 2 (CRY2) functions by the photoactivation mechanism distinct from the tryptophan (trp) triad-dependent photoreduction , 2011, Proceedings of the National Academy of Sciences.

[132]  Baldissera Giovani,et al.  Light-induced electron transfer in a cryptochrome blue-light photoreceptor , 2003, Nature Structural Biology.

[133]  E. Getzoff,et al.  Origin of light-induced spin-correlated radical pairs in cryptochrome. , 2010, The journal of physical chemistry. B.

[134]  Thorsten Ritz,et al.  Resonance effects indicate a radical-pair mechanism for avian magnetic compass , 2004, Nature.

[135]  A. Sancar,et al.  Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. , 2000, Annual review of biochemistry.

[136]  G. D. Bernard,et al.  Functional similarities between polarization vision and color vision , 1977, Vision Research.

[137]  B. Shao,et al.  Effect of radio frequency fields on the radical pair magnetoreception model. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[138]  N. Troje,et al.  Lateralized activation of Cluster N in the brains of migratory songbirds , 2007, The European journal of neuroscience.

[139]  F. Nori,et al.  Quantum biology , 2012, Nature Physics.

[140]  T. Ritz,et al.  Magnetoreception in birds: the effect of radio-frequency fields , 2015, Journal of The Royal Society Interface.

[141]  M. Elstner,et al.  Solvent driving force ensures fast formation of a persistent and well-separated radical pair in plant cryptochrome. , 2015, Journal of the American Chemical Society.

[142]  Stefan Weber,et al.  Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor , 2012, Proceedings of the National Academy of Sciences.

[143]  S. Weber Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. , 2005, Biochimica et biophysica acta.

[144]  P. Hore,et al.  Alternative radical pairs for cryptochrome-based magnetoreception , 2014, Journal of The Royal Society Interface.

[145]  H. Mouritsen,et al.  Migratory Birds Use Head Scans to Detect the Direction of the Earth's Magnetic Field , 2004, Current Biology.

[146]  Klaus Schulten,et al.  Magnetoreception through cryptochrome may involve superoxide. , 2009, Biophysical journal.

[147]  G. Scuseria,et al.  Gaussian 03, Revision E.01. , 2007 .

[148]  Joseph L. Kirschvink,et al.  Particle-Size Considerations for Magnetite-Based Magnetoreceptors , 1985 .

[149]  J. Kirschvink,et al.  Magnetite-based magnetoreception , 2001, Current Opinion in Neurobiology.

[150]  S. Huelga,et al.  Vibrations, quanta and biology , 2013, 1307.3530.

[151]  Anton Savitsky,et al.  High-Field EPR Spectroscopy on Proteins and their Model Systems: Characterization of Transient Paramagnetic States , 2008 .

[152]  W. Wiltschko [On the effect of static magnetic fields on the migratory orientation of the robin (Erithacus rubecula)]. , 2010, Zeitschrift fur Tierpsychologie.

[153]  T. Ritz,et al.  Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing , 2010, Journal of The Royal Society Interface.

[154]  Dora Biro,et al.  Route following and the pigeon's familiar area map , 2014, Journal of Experimental Biology.

[155]  P. Kukura,et al.  Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. , 2004, Journal of the American Chemical Society.

[156]  Philip Ball,et al.  Physics of life: The dawn of quantum biology , 2011, Nature.

[157]  U. Steiner,et al.  Kinetic magnetic-field effect involving the small biologically relevant inorganic radicals NO and O2(·-). , 2011, Chemphyschem : a European journal of chemical physics and physical chemistry.

[158]  D. Budil,et al.  Magnetic resonance spectroscopy of the primary state, PF, of bacterial photosynthesis , 1981 .

[159]  Onur Güntürkün,et al.  Lateralization of magnetic compass orientation in a migratory bird , 2002, Nature.

[160]  M. Davison,et al.  Magnetoreception and its trigeminal mediation in the homing pigeon , 2004, Nature.

[161]  Sensitivity and entanglement in the avian chemical compass. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[162]  K. Schulten,et al.  Separation of photo-induced radical pair in cryptochrome to a functionally critical distance , 2014, Scientific Reports.

[163]  F. Nori,et al.  Radical-pair model of magnetoreception with spin–orbit coupling , 2013, 1309.5882.

[164]  D. Saha,et al.  State transitions and decoherence in the avian compass. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[165]  O. Güntürkün,et al.  The Neural Basis of Long-Distance Navigation in Birds. , 2016, Annual review of physiology.

[166]  P. Hore,et al.  Electron spin relaxation in cryptochrome-based magnetoreception. , 2016, Physical chemistry chemical physics : PCCP.

[167]  V. Binhi Do naturally occurring magnetic nanoparticles in the human body mediate increased risk of childhood leukaemia with EMF exposure? , 2008, International journal of radiation biology.

[168]  M. F. Cornelio,et al.  Environment-induced anisotropy and sensitivity of the radical pair mechanism in the avian compass. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[169]  I. Kominis Magnetic sensitivity and entanglement dynamics of the chemical compass , 2011, 1111.3974.

[170]  S. Iwai,et al.  Discovery and functional analysis of a 4th electron-transferring tryptophan conserved exclusively in animal cryptochromes and (6-4) photolyases. , 2015, Chemical communications.

[171]  Bernd Schierwater,et al.  Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass , 2004, Naturwissenschaften.

[172]  E. Getzoff,et al.  Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. , 2009, Angewandte Chemie.

[173]  J. Wild,et al.  Magnetic field changes activate the trigeminal brainstem complex in a migratory bird , 2010, Proceedings of the National Academy of Sciences.

[174]  Henrik Mouritsen,et al.  Visual but not trigeminal mediation of magnetic compass information in a migratory bird , 2009, Nature.

[175]  P. Hore,et al.  Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes , 2012, Journal of The Royal Society Interface.

[176]  M. Byrdin,et al.  Reaction mechanisms of DNA photolyase. , 2010, Current opinion in structural biology.

[177]  C. Kyriacou,et al.  An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway , 2014, Nature Communications.

[178]  R. Blakemore,et al.  Magnetotactic bacteria , 1975, Science.

[179]  Quantum dynamics of the avian compass. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[180]  Peter Hore,et al.  Nuclear Magnetic Resonance , 1995 .

[181]  M. Vacha,et al.  Radio frequency magnetic fields disrupt magnetoreception in American cockroach , 2009, Journal of Experimental Biology.

[182]  Dagomir Kaszlikowski,et al.  Quantum coherence and sensitivity of avian magnetoreception. , 2012, Physical review letters.

[183]  I. K. Kominis,et al.  The quantum Zeno effect immunizes the avian compass against the deleterious effects of exchange and dipolar interactions , 2009, Biosyst..

[184]  P. Pernot,et al.  Energetics of Photoinduced Charge Migration within the Tryptophan Tetrad of an Animal (6-4) Photolyase. , 2016, Journal of the American Chemical Society.

[185]  N. Scrutton,et al.  Cryptochrome-dependent magnetic field effect on seizure response in Drosophila larvae , 2014, Scientific Reports.

[186]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[187]  P. Atkins,et al.  Chemically Induced Magnetic Polarization , 1977 .

[188]  H. Mouritsen,et al.  Night-Migratory Songbirds Possess a Magnetic Compass in Both Eyes , 2012, PloS one.

[189]  Murray Shanahan,et al.  Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis , 2013, Front. Comput. Neurosci..

[190]  Gian Giacomo Guerreschi,et al.  Quantum control and entanglement in a chemical compass. , 2009, Physical review letters.

[191]  I. Kominis Quantum Zeno effect explains magnetic-sensitive radical-ion-pair reactions. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[192]  Henrik Mouritsen,et al.  Molecular Mapping of Movement-Associated Areas in the Avian Brain: A Motor Theory for Vocal Learning Origin , 2008, PloS one.

[193]  Henrik Mouritsen,et al.  Chemical Magnetoreception: Bird Cryptochrome 1a Is Excited by Blue Light and Forms Long-Lived Radical-Pairs , 2007, PloS one.

[194]  S. Åkesson,et al.  Avian orientation at steep angles of inclination: experiments with migratory white–crowned sparrows at the magnetic North Pole , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[195]  M. Tiersch,et al.  Decoherence in the chemical compass: the role of decoherence for avian magnetoreception , 2012, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[196]  Thorsten Ritz,et al.  Can disordered radical pair systems provide a basis for a magnetic compass in animals? , 2010, Journal of The Royal Society Interface.

[197]  W. Cochran,et al.  Migrating Songbirds Recalibrate Their Magnetic Compass Daily from Twilight Cues , 2004, Science.

[198]  C. Galizia,et al.  Neurosciences - From Molecule to Behavior: a university textbook , 2013, Springer Berlin Heidelberg.

[199]  H. Mouritsen,et al.  Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia) , 2014, Journal of The Royal Society Interface.

[200]  T. Badea,et al.  Melanopsin cells are the principal conduits for rod–cone input to non-image-forming vision , 2008, Nature.

[201]  K. Schulten,et al.  Acuity of a cryptochrome and vision-based magnetoreception system in birds. , 2010, Biophysical journal.

[202]  D. Keays,et al.  High resolution anatomical mapping confirms the absence of a magnetic sense system in the rostral upper beak of pigeons , 2013, Communicative & integrative biology.

[203]  Sönke Johnsen,et al.  The physics and neurobiology of magnetoreception , 2005, Nature Reviews Neuroscience.

[204]  I. Kominis,et al.  Coherent triplet excitation suppresses the heading error of the avian compass , 2010 .

[205]  Paul Galland,et al.  Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana , 2007, Planta.

[206]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[207]  Charlotte Helfrich-Förster,et al.  Cryptochrome Mediates Light-Dependent Magnetosensitivity of Drosophila's Circadian Clock , 2009, PLoS biology.

[208]  K. Kavokin,et al.  Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field , 2014, Journal of The Royal Society Interface.

[209]  I. Newton The Migration Ecology of Birds , 2007 .

[210]  Jeremy Shaw,et al.  Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons , 2012, Nature.