1932

Abstract

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.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-032116-094545
2016-07-05
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/biophys/45/1/annurev-biophys-032116-094545.html?itemId=/content/journals/10.1146/annurev-biophys-032116-094545&mimeType=html&fmt=ahah

Literature Cited

  1. Ahmad M, Cashmore AR. 1.  1993. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366:162–66 [Google Scholar]
  2. Ahmad M, Galland P, Ritz T, Wiltschko R, Wiltschko W. 2.  2007. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225:615–24 [Google Scholar]
  3. Akesson S, Morin J, Muheim R, Ottosson U. 3.  2001. Avian orientation at steep angles of inclination: experiments with migratory white-crowned sparrows at the magnetic North Pole. Proc. R. Soc. B 268:1907–13 [Google Scholar]
  4. Alerstam T. 4.  1988. Findings of dead birds drifted ashore reveal catastrophic mortality among early spring migrants, especially rooks Corvus frugilegus over the southern Baltic Sea. Anser 27:181–218 [Google Scholar]
  5. Al-Khalili J, McFadden J. 5.  2014. Life on the Edge: The Coming of Age of Quantum Biology London: Bantam
  6. Ball P.6.  2011. Physics of life: the dawn of quantum biology. Nature 474:272–74 [Google Scholar]
  7. Bandyopadhyay JN, Paterek T, Kaszlikowski D. 7.  2012. Quantum coherence and sensitivity of avian magnetoreception. Phys. Rev. Lett. 109:110502 [Google Scholar]
  8. Banerjee R, Schleicher E, Meier S, Viana RM, Pokorny R. 8.  et al. 2007. The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J. Biol. Chem. 282:14916–22 [Google Scholar]
  9. Bazalova O, Kvicalovac M, Valkova T, Slaby P, Bartos P. 9.  et al. 2016. Cryptochrome 2 mediates directional magnetoreception in cockroaches. PNAS 113:1660–65 [Google Scholar]
  10. Bazylinski DA, Frankel RB. 10.  2004. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2:217–30 [Google Scholar]
  11. Beason RC, Semm P. 11.  1996. Does the avian ophthalmic nerve carry magnetic navigational information?. J. Exp. Biol. 199:1241–44 [Google Scholar]
  12. Bernard GD, Wehner R. 12.  1977. Functional similarities between polarization vision and color vision. Vis. Res. 17:1019–28 [Google Scholar]
  13. Berthold P.13.  1999. A comprehensive theory for the evolution, control and adaptability of avian migration. Ostrich 70:1–11 [Google Scholar]
  14. Binhi V.14.  2008. Do naturally occurring magnetic nanoparticles in the human body mediate increased risk of childhood leukaemia with EMF exposure?. Int. J. Radiat. Biol. 84:569–79 [Google Scholar]
  15. Biskup T, Hitomi K, Getzoff ED, Krapf S, Koslowski T. 15.  et al. 2011. Unexpected electron transfer in cryptochrome identified by time-resolved EPR spectroscopy. Angew. Chem. Int. Ed. Engl. 50:12647–51 [Google Scholar]
  16. Biskup T, Schleicher E, Okafuji A, Link G, Hitomi K. 16.  et al. 2009. Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew. Chem. Int. Ed. Engl. 48:404–7 [Google Scholar]
  17. Björn LO. 17.  2015. Photobiology: The Science of Light and Life New York: Springer
  18. Blakemore R. 18.  1975. Magnetotactic bacteria. Science 190:377–79 [Google Scholar]
  19. Bolte P, Bleibaum F, Einwich A, Günther A, Liedvogel M. 19.  et al. 2016. Localisation of the putative magnetoreceptive protein cryptochrome 1b in the retinae of migratory birds and homing pigeons. PLOS ONE 11:e0147819 [Google Scholar]
  20. Bowman MK, Budil DE, Closs GL, Kostka AG, Wraight CA, Norris JR. 20.  1981. Magnetic-resonance spectroscopy of the primary state, PF, of bacterial photosynthesis. PNAS 78:3305–7 [Google Scholar]
  21. Brautigam CA, Smith BS, Ma Z, Palnitkar M, Tomchick DR. 21.  et al. 2004. Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. PNAS 101:12142–47 [Google Scholar]
  22. Brettel K, Byrdin M. 22.  2010. Reaction mechanisms of DNA photolyase. Curr. Opin. Struct. Biol. 20:693–701 [Google Scholar]
  23. Buchachenko AL.23.  2009. Magnetic Isotope Effect in Chemistry and Biochemistry New York: Nova Science
  24. Cai CY, Ai Q, Quan HT, Sun CP. 24.  2012. Sensitive chemical compass assisted by quantum criticality. Phys. Rev. A 85:022315 [Google Scholar]
  25. Cai J.25.  2011. Quantum probe and design for a chemical compass with magnetic nanostructures. Phys. Rev. Lett. 106:100501 [Google Scholar]
  26. Cai J, Caruso F, Plenio MB. 26.  2012. Quantum limits for the magnetic sensitivity of a chemical compass. Phys. Rev. A 85:040304 [Google Scholar]
  27. Cai J, Guerreschi GG, Briegel HJ. 27.  2010. Quantum control and entanglement in a chemical compass. Phys. Rev. Lett. 104:220502 [Google Scholar]
  28. Cailliez F, Müller P, Firmino T, Pernot P, de la Lande A. 28.  2016. Energetics of photoinduced charge migration within the tryptophan tetrad of an animal (6−4) photolyase. J. Am. Chem. Soc. 138:1904–15 [Google Scholar]
  29. Carrillo A, Cornelio MF, de Oliveira MC. 29.  2015. Environment-induced anisotropy and sensitivity of the radical pair mechanism in the avian compass. Phys. Rev. E 92:012720 [Google Scholar]
  30. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T. 30.  et al. 2011. The cryptochromes: blue light photoreceptors in plants and animals. Annu. Rev. Plant Biol. 62:335–64 [Google Scholar]
  31. Cintolesi F, Ritz T, Kay CWM, Timmel CR, Hore PJ. 31.  2003. Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294:385–99 [Google Scholar]
  32. Cochran WW, Mouritsen H, Wikelski M. 32.  2004. Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304:405–8 [Google Scholar]
  33. Cohen AE.33.  2009. Nanomagnetic control of intersystem crossing. J. Phys. Chem. A 113:11084–92 [Google Scholar]
  34. Davila AF, Fleissner G, Winklhofer M, Petersen N. 34.  2003. A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys. Chem. Earth 28:647–52 [Google Scholar]
  35. Dellis AT, Kominis IK. 35.  2012. The quantum Zeno effect immunizes the avian compass against the deleterious effects of exchange and dipolar interactions. Biosystems 107:153–57 [Google Scholar]
  36. Dhande OS, Huberman AD. 36.  2014. Retinal ganglion cell maps in the brain: implications for visual processing. Curr. Opin. Neurobiol. 24:133–42 [Google Scholar]
  37. Dodson CA, Hore PJ, Wallace MI. 37.  2013. A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends Biochem. Sci. 38:435–46 [Google Scholar]
  38. Efimova O, Hore PJ. 38.  2008. Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 94:1565–74 [Google Scholar]
  39. Emlen ST. 39.  1980. Decision making by nocturnal bird migrants: the integration of multiple cues. Acta XVII Congr. Intern. Ornithol., Berlin553–60 Berlin: Deutschen Ornithologen-Gesellschaft [Google Scholar]
  40. Engelhard C, Wang XC, Robles D, Moldt J, Essen LO. 40.  et al. 2014. Cellular metabolites enhance the light sensitivity of Arabidopsis cryptochrome through alternate electron transfer pathways. Plant Cell 26:4519–31 [Google Scholar]
  41. Engels S, Hein CM, Lefeldt N, Prior H, Mouritsen H. 41.  2012. Night-migratory songbirds possess a magnetic compass in both eyes. PLOS ONE 7:e43271 [Google Scholar]
  42. Engels S, Schneider NL, Lefeldt N, Hein CM, Zapka M. 42.  et al. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509:353–56 [Google Scholar]
  43. Falkenberg G, Fleissner G, Schuchardt K, Kuehbacher M, Thalau P. 43.  et al. 2010. Avian magnetoreception: Elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLOS ONE 5:e9231 [Google Scholar]
  44. Fedele G, Edwards MD, Bhutani S, Hares JM, Murbach M. 44.  et al. 2014. Genetic analysis of circadian responses to low frequency electromagnetic fields in Drosophila melanogaster. PLOS Genet 10:e1004804 [Google Scholar]
  45. Fedele G, Green EW, Rosato E, Kyriacou CP. 45.  2014. An electromagnetic field disrupts negative geotaxis in Drosophila via a CRY-dependent pathway. Nat. Commun. 5:4391 [Google Scholar]
  46. Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H. 46.  et al. 2008. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLOS ONE 3:e1768 [Google Scholar]
  47. Fleissner G, Holtkamp-Rotzler E, Hanzlik M, Winklhofer M, Fleissner G. 47.  et al. 2003. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458:350–60 [Google Scholar]
  48. Foley LE, Gegear RJ, Reppert SM. 48.  2011. Human cryptochrome exhibits light-dependent magnetosensitivity. Nat. Commun. 2:356 [Google Scholar]
  49. Forbes MDE, Jarocha LE, Sim S, Tarasov VF. 49.  2013. Time-resolved electron paramagnetic resonance spectroscopy: history, technique, and application to supramolecular and macromolecular chemistry. Adv. Phys. Org. Chem. 47:1–83 [Google Scholar]
  50. Frankel RB, Blakemore RP. 50.  1989. Magnetite and magnetotaxis in microorganisms. Bioelectromagnetics 10:223–37 [Google Scholar]
  51. Frankevich EL, Kubarev SI. 51.  1982. Spectroscopy of reaction yield detected magnetic resonance. Triplet State ODMR Spectroscopy RH Clarke 137–83 New York: Wiley [Google Scholar]
  52. Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J, Vallin A. 52.  2001. Bird migration: Magnetic cues trigger extensive refuelling. Nature 414:35–36 [Google Scholar]
  53. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA. 53.  et al. 2004. Gaussian 03, Revision C.02 Wallingford, CT: Gaussian, Inc.
  54. Frost BJ, Mouritsen H. 54.  2006. The neural mechanisms of long distance animal navigation. Curr. Opin. Neurobiol. 16:481–88 [Google Scholar]
  55. Gagliardo A.55.  2013. Forty years of olfactory navigation in birds. J. Exp. Biol. 216:2165–71 [Google Scholar]
  56. Gauger EM, Rieper E, Morton JJL, Benjamin SC, Vedral V. 56.  2011. Sustained quantum coherence and entanglement in the avian compass. Phys. Rev. Lett. 106:040503 [Google Scholar]
  57. Gegear RJ, Casselman A, Waddell S, Reppert SM. 57.  2008. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454:1014–18 [Google Scholar]
  58. Gegear RJ, Foley LE, Casselman A, Reppert SM. 58.  2010. Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism. Nature 463:804–7 [Google Scholar]
  59. Giovani B, Byrdin M, Ahmad M, Brettel K. 59.  2003. Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Biol. 10:489–90 [Google Scholar]
  60. Goez M.60.  2013. Elucidating organic reaction mechanisms using photo-CIDNP spectroscopy. Top. Curr. Chem. 338:1–32 [Google Scholar]
  61. Gomperts BD, Kramer IM, Tatham PER. 61.  2013. Signal Transduction Amsterdam: Academic
  62. Guilford T, Biro D. 62.  2014. Route following and the pigeon's familiar area map. J. Exp. Biol. 217:169–79 [Google Scholar]
  63. Güler AD, Ecker JL, Lall GS, Haq S, Altimus CM. 63.  et al. 2008. Melanopsin cells are the principal conduits for rod–cone input to non-image-forming vision. Nature 453:102–5 [Google Scholar]
  64. Gunkel M, Schoneberg J, Alkhaldi W, Irsen S, Noe F. 64.  et al. 2015. Higher-order architecture of rhodopsin in intact photoreceptors and its implication for phototransduction kinetics. Structure 23:628–38 [Google Scholar]
  65. Harris S-R, Henbest KB, Maeda K, Pannell JR, Timmel CR. 65.  et al. 2009. Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana. J. R. Soc. Interface 6:1193–205 [Google Scholar]
  66. Hein CM, Engels S, Kishkinev D, Mouritsen H. 66.  2011. Robins have a magnetic compass in both eyes. Nature 471:E11–12 [Google Scholar]
  67. Hein CM, Zapka M, Heyers D, Kutzschbauch S, Schneider NL, Mouritsen H. 67.  2010. Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes. J. R. Soc. Interface 7:S227–33 [Google Scholar]
  68. Henbest KB, Kukura P, Rodgers CT, Hore PJ, Timmel CR. 68.  2004. Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. J. Am. Chem. Soc. 126:8102–3 [Google Scholar]
  69. Henbest KB, Maeda K, Hore PJ, Joshi M, Bacher A. 69.  et al. 2008. Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase. PNAS 105:14395–99 [Google Scholar]
  70. Herbel V, Orth C, Wenzel R, Ahmad M, Bittl R, Batschauer A. 70.  2013. Lifetimes of Arabidopsis cryptochrome signaling states in vivo. Plant J. 74:583–92 [Google Scholar]
  71. Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H. 71.  2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLOS ONE 2:e937 [Google Scholar]
  72. Heyers D, Zapka M, Hoffmeister M, Wild JM, Mouritsen H. 72.  2010. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. PNAS 107:9394–99 [Google Scholar]
  73. Hill E, Ritz T. 73.  2010. Can disordered radical pair systems provide a basis for a magnetic compass in animals?. J. R. Soc. Interface 7:S265–71 [Google Scholar]
  74. Hiscock HG, Worster S, Kattnig DR, Steers C, Jin Y. 74.  et al. 2016. The quantum needle of the avian magnetic compass. PNAS 113:4634–39 [Google Scholar]
  75. Hogben HJ, Biskup T, Hore PJ. 75.  2012. Entanglement and sources of magnetic anisotropy in radical pair-based avian magnetoreceptors. Phys. Rev. Lett. 109:220501 [Google Scholar]
  76. Hogben HJ, Efimova O, Wagner-Rundell N, Timmel CR, Hore PJ. 76.  2009. Possible involvement of superoxide and dioxygen with cryptochrome in avian magnetoreception: origin of Zeeman resonances observed by in vivo EPR spectroscopy. Chem. Phys. Lett. 480:118–22 [Google Scholar]
  77. Holland RA.77.  2010. Differential effects of magnetic pulses on the orientation of naturally migrating birds. J. R. Soc. Interface 7:1617–25 [Google Scholar]
  78. Holland RA.78.  2014. True navigation in birds: from quantum physics to global migration. J. Zool. 293:1–15 [Google Scholar]
  79. Hore PJ.79.  2011. The quantum robin. Navigation News November/December 15–17
  80. Hore PJ.80.  2015. Nuclear Magnetic Resonance Oxford: Oxford Univ. Press
  81. Huelga SF, Plenio MB. 81.  2013. Vibrations, quanta and biology. Contemp. Phys. 54:181–207 [Google Scholar]
  82. Jarvis ED, Güntürkün O, Bruce L, Csillag A, Karten H. 82.  et al. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat. Rev. Neurosci. 6:151–59 [Google Scholar]
  83. Jarvis ED, Nottebohm F. 83.  1997. Motor-driven gene expression. PNAS 94:4097–5102 [Google Scholar]
  84. Jarvis ED, Yu J, Rivas MV, Horita H, Feenders G. 84.  et al. 2013. Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J. Comp. Neurol. 521:3614–65 [Google Scholar]
  85. Johnsen S, Lohmann KJ. 85.  2005. The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 6:703–12 [Google Scholar]
  86. Karogodina TY, Dranov IG, Sergeeva SV, Stass DV, Steiner UE. 86.  2011. Kinetic magnetic-field effect involving the small biologically relevant inorganic radicals nitric oxide and superoxide. ChemPhysChem. 12:1714–28 [Google Scholar]
  87. Karogodina TY, Sergeeva SV, Stass DV. 87.  2009. Magnetic field effect in the reaction of recombination of nitric oxide and superoxide anion. Appl. Magn. Reson. 36:195–208 [Google Scholar]
  88. Katsoprinakis GE, Dellis AT, Kominis IK. 88.  2010. Coherent triplet excitation suppresses the heading error of the avian compass. New J. Phys. 12:085016 [Google Scholar]
  89. Kattnig DR, Solov'yov IA, Hore PJ. 89.  2016. Electron spin relaxation in cryptochrome-based magnetoreception. Phys. Chem. Chem. Phys. 1812443–56
  90. Kaupp UB, Koch KW. 90.  1992. Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu. Rev. Physiol. 54:153–75 [Google Scholar]
  91. Kavokin KV.91.  2009. The puzzle of magnetic resonance effect on the magnetic compass of migratory birds. Bioelectromagnetics 30:402–10 [Google Scholar]
  92. Kavokin KV, Chernetsov N, Pakhomov A, Bojarinova J, Kobylkov D, Namozov B. 92.  2014. Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field. J. R. Soc. Interface 11:20140451 [Google Scholar]
  93. Kirschvink JL, Gould JL. 93.  1981. Biogenic magnetite as a basis for magnetic-field detection in animals. Biosystems 13:181–201 [Google Scholar]
  94. Kirschvink JL, Walker MM. 94.  1985. Particle size considerations for magnetite based magnetoreceptors. Magnetite Biomineralization and Magnetoreception in Organisms: A New Biomagnetism JL Kirschvink, DS Jones, BJ McFadden 243–54 New York: Plenum [Google Scholar]
  95. Kirschvink JL, Walker MM, Diebel CE. 95.  2001. Magnetite-based magnetoreception. Curr. Opin. Neurobiol. 11:462–67 [Google Scholar]
  96. Kirschvink JL, Winklhofer M, Walker MM. 96.  2010. Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. J. R. Soc. Interface 7:S179–91 [Google Scholar]
  97. Kishkinev D, Chernetsov N, Heyers D, Mouritsen H. 97.  2013. Migratory reed warblers need intact trigeminal nerves to correct for a 1,000 km eastward displacement. PLOS ONE 8:e65847 [Google Scholar]
  98. Kishkinev D, Chernetsov N, Mouritsen H. 98.  2010. A double-clock or jetlag mechanism is unlikely to be involved in detection of east-west displacements in a long-distance avian migrant. Auk 127:773–80 [Google Scholar]
  99. Kishkinev D, Chernetsov N, Pakhomov A, Heyers D, Mouritsen H. 99.  2015. Eurasian reed warblers compensate for virtual magnetic displacement. Curr. Biol. 25:R822–24 [Google Scholar]
  100. Kominis IK.100.  2009. Quantum Zeno effect explains magnetic-sensitive radical-ion-pair reactions. Phys. Rev. E 80:056115 [Google Scholar]
  101. Kominis IK.101.  2012. Magnetic sensitivity and entanglement dynamics of the chemical compass. Chem. Phys. Lett. 542:143–46 [Google Scholar]
  102. Kondoh M, Shiraishi C, Müller P, Ahmad M, Hitomi K. 102.  et al. 2011. Light-induced conformational changes in full-length Arabidopsis thaliana cryptochrome. J. Mol. Biol. 413:128–37 [Google Scholar]
  103. Kowalczyk RM, Schleicher E, Bittl R, Weber S. 103.  2004. The photoinduced triplet of flavins and its protonation states. J. Am. Chem. Soc. 126:11393–99 [Google Scholar]
  104. Lambert N, Chen YN, Cheng YC, Li CM, Chen GY, Nori F. 104.  2013. Quantum biology. Nat. Phys. 9:10–18 [Google Scholar]
  105. Lambert N, De Liberato S, Emary C, Nori F. 105.  2013. Radical-pair model of magnetoreception with spin-orbit coupling. New J. Phys. 15:083024 [Google Scholar]
  106. Lau JCS, Rodgers CT, Hore PJ. 106.  2012. Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes. J. R. Soc. Interface 9:3329–37 [Google Scholar]
  107. Lau JCS, Wagner-Rundell N, Rodgers CT, Green NJB, Hore PJ. 107.  2010. Effects of disorder and motion in a radical pair magnetoreceptor. J. R. Soc. Interface 7:S257–64 [Google Scholar]
  108. Lee AA, Lau JCS, Hogben HJ, Biskup T, Kattnig DR, Hore PJ. 108.  2014. Alternative radical pairs for cryptochrome-based magnetoreception. J. R. Soc. Interface 11:20131063 [Google Scholar]
  109. Lefeldt N, Dreyer D, Schneider NL, Steenken F, Mouritsen H. 109.  2015. Migratory blackcaps tested in Emlen funnels can orient at 85 degrees but not at 88 degrees magnetic inclination. J. Exp. Biol. 218:206–11 [Google Scholar]
  110. Lefeldt N, Heyers D, Schneider NL, Engels S, Elbers D, Mouritsen H. 110.  2014. Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J. R. Soc. Interface 11:20140777 [Google Scholar]
  111. Lewis AM, Manolopoulos DE, Hore PJ. 111.  2014. Asymmetric recombination and electron spin relaxation in the semiclassical theory of radical pair reactions. J. Chem. Phys. 141:044111 [Google Scholar]
  112. Li X, Wang Q, Yu XH, Liu HT, Yang H. 112.  et al. 2011. Arabidopsis cryptochrome 2 (CRY2) functions by the photoactivation mechanism distinct from the tryptophan (Trp) triad-dependent photoreduction. PNAS 108:20844–49 [Google Scholar]
  113. Liedvogel M, Feenders G, Wada K, Troje NF, Jarvis ED, Mouritsen H. 113.  2007. Lateralized activation of Cluster N in the brains of migratory songbirds. Eur. J. Neurosci. 25:1166–73 [Google Scholar]
  114. Liedvogel M, Maeda K, Henbest K, Schleicher E, Simon T. 114.  et al. 2007. Chemical magnetoreception: Bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLOS ONE 2:e1106 [Google Scholar]
  115. Liedvogel M, Mouritsen H. 115.  2010. Cryptochromes—a potential magnetoreceptor: What do we know and what do we want to know?. J. R. Soc. Interface 7:S147–62 [Google Scholar]
  116. Lin CT, Todo T. 116.  2005. The cryptochromes. Genome Biol. 6:220 [Google Scholar]
  117. Lohmann KJ, Putman NF, Lohmann CMF. 117.  2012. The magnetic map of hatchling loggerhead sea turtles. Curr. Opin. Neurobiol. 22:336–42 [Google Scholar]
  118. Lüdemann G, Solov'yov IA, Kubar T, Elstner M. 118.  2015. Solvent driving force ensures fast formation of a persistent and well-separated radical pair in plant cryptochrome. J. Am. Chem. Soc. 137:1147–56 [Google Scholar]
  119. Maeda K, Henbest KB, Cintolesi F, Kuprov I, Rodgers CT. 119.  et al. 2008. Chemical compass model of avian magnetoreception. Nature 453:387–90 [Google Scholar]
  120. Maeda K, Robinson AJ, Henbest KB, Hogben HJ, Biskup T. 120.  et al. 2012. Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. PNAS 109:4774–79 [Google Scholar]
  121. Manolopoulos DE, Hore PJ. 121.  2013. An improved semiclassical theory of radical pair recombination reactions. J. Chem. Phys. 139:124106 [Google Scholar]
  122. Marley R, Giachello CNG, Scrutton NS, Baines RA, Jones AR. 122.  2014. Cryptochrome-dependent magnetic field effect on seizure response in Drosophila larvae. Sci. Rep. 4:5799 [Google Scholar]
  123. Marshak DW, Mills SL. 123.  2014. Short-wavelength cone-opponent retinal ganglion cells in mammals. Vis. Neurosci. 31:165–75 [Google Scholar]
  124. Mello CV, Vicario DS, Clayton DF. 124.  1992. Song presentation induces gene-expression in the songbird forebrain. PNAS 89:6818–22 [Google Scholar]
  125. Möbius K, Savitsky A. 125.  2009. High-Field EPR Spectroscopy on Proteins and Their Model Systems Cambridge, UK: R. Soc. Chem.
  126. Mohseni M, Omar Y, Engel GS, Plenio MB. 126.  2014. Quantum Effects in Biology Cambridge, UK: Cambridge Univ. Press
  127. Möller A, Sagasser S, Wiltschko W, Schierwater B. 127.  2004. Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585–88 [Google Scholar]
  128. Mora CV, Davison M, Wild JM, Walker MM. 128.  2004. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–11 [Google Scholar]
  129. Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL. 129.  1992. Nature of biological electron transfer. Nature 355:796–802 [Google Scholar]
  130. Mouritsen H.130.  2001. Navigation in birds and other animals. Image Vis. Comput. 19:713–31 [Google Scholar]
  131. Mouritsen H.131.  2003. Spatiotemporal orientation strategies of long-distance migrants. Avian Migration P Berthold, E Gwinner, E Sonnenschein 493–513 Berlin: Springer-Verlag [Google Scholar]
  132. Mouritsen H.132.  2012. Search for the compass needles. Nature 484:320–21 [Google Scholar]
  133. Mouritsen H.133.  2013. The magnetic senses. Neurosciences - From Molecule to Behavior: A University Textbook CG Galizia, P-M Lledo 427–43 Berlin: Springer-Verlag [Google Scholar]
  134. Mouritsen H.134.  2014. Magnetoreception in birds and its use for long-distance migration. Sturkie's Avian Physiology C Scanes 113–33 New York: Elsevier [Google Scholar]
  135. Mouritsen H, Feenders G, Liedvogel M, Kropp W. 135.  2004. Migratory birds use head scans to detect the direction of the Earth's magnetic field. Curr. Biol. 14:1946–49 [Google Scholar]
  136. Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED. 136.  2005. Night-vision brain area in migratory songbirds. PNAS 102:8339–44 [Google Scholar]
  137. Mouritsen H, Heyers D, Güntürkün O. 137.  2016. The neural basis of long-distance navigation in birds. Annu. Rev. Physiol. 78:133–54 [Google Scholar]
  138. Mouritsen H, Hore PJ. 138.  2012. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22:343–52 [Google Scholar]
  139. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J. 139.  et al. 2004. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. PNAS 101:14294–99 [Google Scholar]
  140. Mouritsen H, Mouritsen O. 140.  2000. A mathematical expectation model for bird navigation based on the clock-and-compass strategy. J. Theor. Biol. 207:283–91 [Google Scholar]
  141. Muheim R, Sjöberg S, Pinzon-Rodriguez A. 141.  2016. Polarized light modulates light-dependent magnetic compass orientation in birds. PNAS 113:1654–59 [Google Scholar]
  142. Müller P, Ahmad M. 142.  2011. Light-activated cryptochrome reacts with molecular oxygen to form a flavin-superoxide radical pair consistent with magnetoreception. J. Biol. Chem. 286:21033–40 [Google Scholar]
  143. Müller P, Yamamoto J, Martin R, Iwai S, Brettel K. 143.  2015. Discovery and functional analysis of a 4th electron-transferring tryptophan conserved exclusively in animal cryptochromes and (6-4) photolyases. Chem. Commun. 51:15502–5 [Google Scholar]
  144. Muus LT, Atkins PW, McLauchlan KA, Pedersen JB. 144.  1977. Chemically Induced Magnetic Polarization Dordrecht, Neth.: D. Reidel
  145. Newton I.145.  2010. The Migration Ecology of Birds London, UK: Academic [Google Scholar]
  146. Nießner C, Denzau S, Gross JC, Peichl L, Bischof HJ. 146.  et al. 2011. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLOS ONE 6:e20091 [Google Scholar]
  147. Nießner C, Denzau S, Peichl L, Wiltschko W, Wiltschko R. 147.  2014. Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle. J. Exp. Biol. 217:4221–24 [Google Scholar]
  148. Nießner C, Denzau S, Stapput K, Ahmad M, Peichl L. 148.  et al. 2013. Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds. J. R. Soc. Interface 10:20130638 [Google Scholar]
  149. Nießner C, Gross JC, Denzau S, Peichl L, Fleissner G. 149.  et al. 2016. Seasonally changing cryptochrome 1b expression in the retinal ganglion cells of a migrating passerine bird. PLOS ONE 11:e0150377 [Google Scholar]
  150. Oldham WM, Hamm HE. 150.  2008. Heterotrimeric G protein activation by G-protein-coupled receptors. Nat. Rev. Mol. Cell Biol. 9:60–71 [Google Scholar]
  151. Ozturk N, Selby CP, Annayev Y, Zhong DP, Sancar A. 151.  2011. Reaction mechanism of Drosophila cryptochrome. PNAS 108:516–21 [Google Scholar]
  152. Ozturk N, Selby CP, Zhong DP, Sancar A. 152.  2014. Mechanism of photosignaling by Drosophila cryptochrome. Role of the redox status of the flavin chromophore. J. Biol. Chem. 289:4634–42 [Google Scholar]
  153. Partch CL, Clarkson MW, Ozgur S, Lee AL, Sancar A. 153.  2005. Role of structural plasticity in signal transduction by the cryptochrome blue-light photoreceptor. Biochemistry 44:3795–805 [Google Scholar]
  154. Pauls JA, Zhang YT, Berman GP, Kais S. 154.  2013. Quantum coherence and entanglement in the avian compass. Phys. Rev. E 87:062704 [Google Scholar]
  155. Perdeck AC.155.  1958. Two types of orientation in migrating Sturnus vulgaris and Fringilla coelebs as revealed by displacement experiments. Ardea 46:1–37 [Google Scholar]
  156. Phillips JB, Borland SC. 156.  1992. Behavioral evidence for use of a light-dependent magnetoreception mechanism by a vertebrate. Nature 359:142–44 [Google Scholar]
  157. Poonia VS, Saha D, Ganguly S. 157.  2015. State transitions and decoherence in the avian compass. Phys. Rev. E 91:052709 [Google Scholar]
  158. Prabhakar R, Siegbahn PEM, Minaev BF, Agren H. 158.  2002. Activation of triplet dioxygen by glucose oxidase: spin-orbit coupling in the superoxide ion. J. Phys. Chem. B 106:3742–50 [Google Scholar]
  159. Putman NF, Lohmann KJ, Putman EM, Quinn TP, Klimley AP, Noakes DLG. 159.  2013. Evidence for geomagnetic imprinting as a homing mechanism in pacific salmon. Curr. Biol. 23:312–16 [Google Scholar]
  160. Qin S, Yin H, Yang C, Dou Y, Liu Z. 160.  et al. 2016. A magnetic protein biocompass. Nat. Mater. 15:217–26 [Google Scholar]
  161. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A. 161.  et al. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473:377–414 [Google Scholar]
  162. Ritz T, Adem S, Schulten K. 162.  2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78:707–18 [Google Scholar]
  163. Ritz T, Ahmad M, Mouritsen H, Wiltschko R, Wiltschko W. 163.  2010. Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing. J. R. Soc. Interface 7:S135–46 [Google Scholar]
  164. Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W. 164.  2004. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429:177–80 [Google Scholar]
  165. Ritz T, Wiltschko R, Hore PJ, Rodgers CT, Stapput K. 165.  et al. 2009. Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 96:3451–57 [Google Scholar]
  166. Rodgers CT.166.  2007. Magnetic field effects in chemical systems PhD thesis University of Oxford United Kingdom:
  167. Rodgers CT.167.  2009. Magnetic field effects in chemical systems. Pure Appl. Chem. 81:19–43 [Google Scholar]
  168. Rodgers CT, Henbest KB, Kukura P, Timmel CR, Hore PJ. 168.  2005. Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. J. Phys. Chem. A 109:5035–41 [Google Scholar]
  169. Rodgers CT, Hore PJ. 169.  2009. Chemical magnetoreception in birds: a radical pair mechanism. PNAS 106:353–60 [Google Scholar]
  170. Rodgers CT, Norman SA, Henbest KB, Timmel CR, Hore PJ. 170.  2007. Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. J. Am. Chem. Soc. 129:6746–55 [Google Scholar]
  171. Salikhov KM, Molin YN, Sagdeev RZ, Buchachenko AL. 171.  1984. Spin Polarization and Magnetic Field Effects in Radical Reactions New York: Elsevier
  172. Sancar A.172.  2000. Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annu. Rev. Biochem. 69:31–67 [Google Scholar]
  173. Sancar A.173.  2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203–37 [Google Scholar]
  174. Schulten K, Swenberg CE, Weller A. 174.  1978. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. 111:1–5 [Google Scholar]
  175. Schwarze S, Schneider N-L, Reichl T, Dreyer D, Lefeldt N. 175.  et al. 2016. Weak broadband electromagnetic fields are more disruptive to magnetic compass orientation in a night-migratory songbird (Erithacus rubecula) than strong narrow-band fields. Front. Behav. Neurosci. 10:55 [Google Scholar]
  176. Shanahan M, Bingman VP, Shimizu T, Wild M, Güntürkün O. 176.  2013. Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis. Front. Comput. Neurosci. 7:89 [Google Scholar]
  177. Solov'yov IA, Chandler DE, Schulten K. 177.  2007. Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 92:2711–26 [Google Scholar]
  178. Solov'yov IA, Domratcheva T, Schulten K. 178.  2014. Separation of photo-induced radical pair in cryptochrome to a functionally critical distance. Sci. Rep. 4:3845 [Google Scholar]
  179. Solov'yov IA, Domratcheva T, Shahi ARM, Schulten K. 179.  2012. Decrypting cryptochrome: revealing the molecular identity of the photoactivation reaction. J. Am. Chem. Soc. 134:18046–52 [Google Scholar]
  180. Solov'yov IA, Greiner W. 180.  2007. Theoretical analysis of an iron mineral-based magnetoreceptor model in birds. Biophys. J. 93:1493–509 [Google Scholar]
  181. Solov'yov IA, Greiner W. 181.  2009. Iron-mineral-based magnetoreceptor in birds: polarity or inclination compass?. Eur. Phys. J. D 51:161–72 [Google Scholar]
  182. Solov'yov IA, Mouritsen H, Schulten K. 182.  2010. Acuity of a cryptochrome and vision-based magnetoreception system in birds. Biophys. J. 99:40–49 [Google Scholar]
  183. Solov'yov IA, Schulten K. 183.  2009. Magnetoreception through cryptochrome may involve superoxide. Biophys. J. 96:4804–13 [Google Scholar]
  184. Steiner UE, Ulrich T. 184.  1989. Magnetic field effects in chemical kinetics and related phenomena. Chem. Rev. 89:51–147 [Google Scholar]
  185. Stoneham AM, Gauger EM, Porfyrakis K, Benjamin SC, Lovett BW. 185.  2012. A new type of radical-pair-based model for magnetoreception. Biophys. J. 102:961–68 [Google Scholar]
  186. Thalau P, Ritz T, Burda H, Wegner RE, Wiltschko R. 186.  2006. The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3:583–87 [Google Scholar]
  187. Thalau P, Ritz T, Stapput K, Wiltschko R, Wiltschko W. 187.  2005. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92:86–90 [Google Scholar]
  188. Thompson CL, Ng L, Menon V, Martinez S, Lee CK. 188.  et al. 2014. A high-resolution spatiotemporal atlas of gene expression of the developing mouse brain. Neuron 83:309–23 [Google Scholar]
  189. Thoreson W.189.  2008. The vertebrate retina. Neuroimmune Pharmacology T Ikezu, HE Gendelman 123–34 New York: Springer [Google Scholar]
  190. Tiersch M, Briegel HJ. 190.  2012. Decoherence in the chemical compass: the role of decoherence for avian magnetoreception. Philos. Trans. R. Soc. A 370:4517–40 [Google Scholar]
  191. Tiersch M, Guerreschi GG, Clausen J, Briegel HJ. 191.  2014. Approaches to measuring entanglement in chemical magnetometers. J. Phys. Chem. A 118:13–20 [Google Scholar]
  192. Treiber CD, Salzer M, Breuss M, Ushakova L, Lauwers M. 192.  et al. 2013. High resolution anatomical mapping confirms the absence of a magnetic sense system in the rostral upper beak of pigeons. Commun. Integr. Biol. 6:e24859 [Google Scholar]
  193. Treiber CD, Salzer MC, Riegler J, Edelman N, Sugar C. 193.  et al. 2012. Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484:367–70 [Google Scholar]
  194. Vacha M, Puzova T, Kvicalova M. 194.  2009. Radio frequency magnetic fields disrupt magnetoreception in American cockroach. J. Exp. Biol. 212:3473–77 [Google Scholar]
  195. van Wilderen LJGW, Silkstone G, Mason M, van Thor JJ, Wilson MT. 195.  2015. Kinetic studies on the oxidation of semiquinone and hydroquinone forms of Arabidopsis cryptochrome by molecular oxygen. FEBS Open Bio 5:885–92 [Google Scholar]
  196. Vedral V.196.  2011. Living in a quantum world. Sci. Am. 304:38–43 [Google Scholar]
  197. Walker MM, Dennis TE, Kirschvink JL. 197.  2002. The magnetic sense and its use in long-distance navigation by animals. Curr. Opin. Neurobiol. 12:735–44 [Google Scholar]
  198. Walters ZB.198.  2014. Quantum dynamics of the avian compass. Phys. Rev. E 90:042710 [Google Scholar]
  199. Wässle H.199.  2004. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5:747–57 [Google Scholar]
  200. Weber S.200.  2005. Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyase. Biochim. Biophys. Acta 1707:1–23 [Google Scholar]
  201. Weber S, Biskup T, Okafuji A, Marino AR, Berthold T. 201.  et al. 2010. Origin of light-induced spin-correlated radical pairs in cryptochrome. J. Phys. Chem. B 114:14745–54 [Google Scholar]
  202. Wiltschko R, Stapput K, Thalau P, Wiltschko W. 202.  2010. Directional orientation of birds by the magnetic field under different light conditions. J. R. Soc. Interface 7:S163–77 [Google Scholar]
  203. Wiltschko R, Thalau P, Gehring D, Nießner C, Ritz T, Wiltschko W. 203.  2015. Magnetoreception in birds: the effect of radio-frequency fields. J. R. Soc. Interface 12:20141103 [Google Scholar]
  204. Wiltschko R, Wiltschko W. 204.  1995. Magnetic Orientation in Animals Berlin: Springer-Verlag
  205. Wiltschko W.205.  1968. Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z. Tierpsychol. 25:537–58 [Google Scholar]
  206. Wiltschko W, Munro U, Ford H, Wiltschko R. 206.  1993. Red-light disrupts magnetic orientation of migratory birds. Nature 364:525–27 [Google Scholar]
  207. Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R. 207.  2002. Lateralization of magnetic compass orientation in a migratory bird. Nature 419:467–70 [Google Scholar]
  208. Wiltschko W, Wiltschko R. 208.  1972. Magnetic compass of European robins. Science 176:62–64 [Google Scholar]
  209. Winklhofer M, Holtkamp-Rotzler E, Hanzlik M, Fleissner G, Petersen N. 209.  2001. Clusters of superparamagnetic magnetite particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor?. Eur. J. Mineral. 13:659–69 [Google Scholar]
  210. Winklhofer M, Kirschvink JL. 210.  2010. A quantitative assessment of torque-transducer models for magnetoreception. J. R. Soc. Interface 7:S273–89 [Google Scholar]
  211. Woodward JR.211.  2002. Radical pairs in solution. Prog. React. Kinet. Mech. 27:165–207 [Google Scholar]
  212. Xu BM, Zou J, Li H, Li JG, Shao B. 212.  2014. Effect of radio frequency fields on the radical pair magnetoreception model. Phys. Rev. E 90:042711 [Google Scholar]
  213. Xu BM, Zou J, Li JG, Shao B. 213.  2013. Estimating the hyperfine coupling parameters of the avian compass by comprehensively considering the available experimental results. Phys. Rev. E 88:032703 [Google Scholar]
  214. Yoshii T, Ahmad M, Helfrich-Forster C. 214.  2009. Cryptochrome mediates light-dependent magnetosensitivity of Drosophila's circadian clock. PLOS Biol. 7:813–19 [Google Scholar]
  215. Zapka M, Heyers D, Hein CM, Engels S, Schneider NL. 215.  et al. 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461:1274–78 [Google Scholar]
  216. Zapka M, Heyers D, Liedvogel M, Jarvis ED, Mouritsen H. 216.  2010. Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. Eur. J. Neurosci. 32:619–24 [Google Scholar]
  217. Zeugner A, Byrdin M, Bouly J-P, Bakrim N, Giovani B. 217.  et al. 2005. Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. J. Biol. Chem. 280:19437–40 [Google Scholar]
  218. Zhang YT, Berman GP, Kais S. 218.  2014. Sensitivity and entanglement in the avian chemical compass. Phys. Rev. E 90:042707 [Google Scholar]
  219. Zhang YT, Berman GP, Kais S. 219.  2015. The radical pair mechanism and the avian chemical compass: quantum coherence and entanglement. Int. J. Quant. Chem. 115:1327–41 [Google Scholar]
/content/journals/10.1146/annurev-biophys-032116-094545
Loading
/content/journals/10.1146/annurev-biophys-032116-094545
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error