Photoreceptor-based magnetoreception: Optimal design of receptor molecules, cells, and neuronal processing

Journal of the Royal Society Interface

Volumn 7, Issue SUPPL. 2, 2010, Pages

  Ritz, Thorsten ^a   Ahmad, Margaret ^b   Mouritsen, Henrik ^c   Wiltschko, Roswitha ^d   Wiltschko, Wolfgang ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITY OF OLDENBURG   (Germany)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

Magnetic sensing; Photoreceptor; Radical pair mechanism

Indexed keywords

ANIMALS; BIOINFORMATICS; BIOMAGNETISM; PHOTOCHEMICAL REACTIONS;

CRYPTOCHROMES; MAGNETIC SENSING; NEURONAL PROCESSING; OPTIMAL DESIGN; PHOTORECEPTOR; PHOTORECEPTOR CELL; RADICAL PAIR; RADICAL-PAIR MECHANISM;

VISION;

CRYPTOCHROME;

BIOMAGNETISM; MAGNETIC FIELD; MAGNETIC STIMULATION; MAGNETORECEPTION; MEDICAL RESEARCH; NEUROPHYSIOLOGY; PHOTOACTIVATION; PHOTORECEPTOR; PHOTORECEPTOR CELL; PHOTORECEPTOR POTENTIAL; PHOTOTRANSDUCTION; RADICAL PAIR PHOTORECEPTOR; REVIEW; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ELECTROMAGNETIC FIELD; HUMAN; MAGNETISM; ORIENTATION; PERCEPTION; PHYSIOLOGY; RADIATION EXPOSURE;

ANIMALIA;

ANIMALS; ELECTROMAGNETIC FIELDS; HUMANS; MAGNETICS; MODELS, BIOLOGICAL; ORIENTATION; PERCEPTION; PHOTORECEPTOR CELLS;

EID: 77953243604     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0456.focus     Document Type: Review

References (112)

1. Ahmad, M., Galland, P., Ritz, T., Wiltschko, R. & Wiltschko, W. 2007 Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225, 615-624. (doi:10.1007/s00425-006-0383-0)
2. Åkesson, S., Morin, J., Muheim, R. & Ottosson, U. 2001 Avian orientation at steep angles of inclination: experiments with migratory white-crowned sparrows at the magnetic north pole. Proc. R. Soc. Lond. B 268, 1907-1913. (doi:10.1098/rspb.2001.1736)
3. Biskup, T., Schleicher, E., Okafuji, A., Link, G., Hitomi, K., Getzoff, E. D. & Weber, S. 2009 Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. Angew. Chem. 48, 404-407. (doi:10.1002/anie.200803102)
4. Bouly, J. P. et al. 2007 Cryptochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol. Chem. 282, 9383-9391. (doi:10.1074/jbe.M609842200)
5. Brocklehurst, B. 2002 Magnetic fields and radical reactions: recent developments and their role in nature. Chem. Soc. Rev. 31, 301-311. (doi:10.1039/b107250c)
6. Cai, J., Guerreschi, G. G. & Briegel, H. J. 2009 Quantum control and entanglement in a chemical compass. (http://arxiv.org/ans/0906.2383)
7. Cintolesi, F., Ritz, T., Kay, C., Timmel, C. & Hore, P. 2003 Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: a model avian photomagnetoreceptor. Chem. Phys. 294, 385-399. (doi:10.1016/S0301-0104(03)00320-3)
8. Cochran, W., Mouritsen, H. & Wikelski, M. 2004 Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304, 405-408. (doi:10.1126/science.1095844)
9. Dommer, D. H., Gazzolo, P. J., Painter, M. S. & Phillips, J. B. 2008 Magnetic compass orientation by larval Drosophila melanogaster. J. Insect Physiol. 54, 719-726. (doi:10.1016/j.jinsphys.2008.02.001)
10. Efimova, O. & Hore, P. J. 2008 Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 94, 1565-1574. (doi:10.1529/biophysj.107.119362)
11. Efimova, O. & Hore, P. J. 2009 Evaluation of nuclear quadrupole interactions as a source of magnetic anisotropy in the radical pair model of the avian magnetic compass. Mol. Phys. 107, 665-671. (doi:10.1080/ 00268970902852624)
12. Feenders, G., Liedvogel, M., Rivas, M., Zapka, M., Horita, H., Hara, E., Kazuhiro, W., Mouritsen, H. & Jarvis, E. D. 2008 Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3, e1768. (doi:10.1371/journal.pone.0001768)
13. Freake, M. & Phillips, J. 2005 Light-dependent shift in bullfrog tadpole magnetic compass orientation: evidence for a common magnetoreception mechanism in anuran and urodele amphibians. Ethology 111, 241-254.
14. Freire, R., Munro, U., Rogers, L. J., Sagasser, S., Wiltschko, R. & Wiltschko, W. 2008 Different responses in two strains of chickens (Gallus gallus) in a magnetic orientation test. Anim. Cogn. 11, 547-552. (doi:10.1007/s10071-008-0147-2)
15. Gegear, R. J., Casselman, A., Waddell, S. & Reppert, S. M. 2008 Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature 454, 1014-1018. (doi:10.1038/nature07183)
16. Giovani, B., Byrdin, M., Ahmad, M. & Brettel, K. 2003 Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Mol. Biol. 10, 489-490. (doi:10.1038/nsb933)
17. Gould, J. L. 2005 Animal navigation: northern exposure. Curr. Biol. 15, R653-R655. (doi:10.1016/j.cub.2005.08.029)
18. Gould, J. L. 2008 Animal navigation: the evolution of magnetic orientation. Curr. Biol. 18, R482-R484. (doi:10.1016/j.cub.2008.03.052)
19. Harris, S.-R., Henbest, K. B., Maeda, K., Pannell, J. R., Timmel, C. R., Hore, P. J. & Okamoto, H. 2009 Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana. J. R. Soc. Interface 6, 1193-1205. (doi:10.1098/rsif.2008.0519)
20. Hein, C. M., Zapka, M., Heyers, D., Kutzschbauch, S., Schneider, N.-L. & Mouritsen, H. 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-S233. (doi:10.1098/rsif.2009.0376.focus)
21. Henbest, K., Kukura, P., Rodgers, C., Hore, P. & Timmel, C. 2004 Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. J. Am. Chem. Soc. 126, 8102-8103. (doi:10.1021/ja048220q)
22. Henbest, K. B., Maeda, K., Hore, P. J., Joshi, M., Bacher, A., Bittl, R., Weber, S., Timmel, C. R. & Schleicher, E. 2008 Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase. Proc. Natl Acad. Sci. USA 105, 14 395-14 399. (doi:10.1073/pnas.0803620105)
23. Heyers, D., Manns, M., Luksch, H., Güntürkün, O. & Mouritsen, H. 2007 A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS ONE 2, e937. (doi:10.1371/journal.pone.0000937)
24. Hill, E. & Ritz, T. 2010 Can disordered radical pair systems provide a basis for a magnetic compass in animals? J. R. Soc. Interface 7, S265-S271. (doi:10.1098/rsif.2009.0378.focus)
25. Hoang, N. et al. 2008 Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol. 6, e160. (doi:10.1371/journal.pbio.0060160)
26. Hogben, H. J., Efimova, O., Wagner-Rundell, N., Timmel, C. R. & Hore, P. 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, 118-122. (doi:10.1016/j.cplett.2009.08.051)
27. Irwin, W. & Lohmann, K. 2003 Magnet-induced disorientation in hatchling loggerhead sea turtles. J. Exp. Biol. 206, 497-501. (doi:10.1242/jeb.00108)
28. Johnsen, S. & Lohmann, K. J. 2005 The physics and neurobiology of magnetoreception. Nat. Rev. Neurosci. 6, 703-712. (doi:10.1038/nrn1745)
29. Johnsen, S. & Lohmann, K. J. 2008 Magnetoreception in animals. Phys. Today 61, 29-35. (doi:10.1063/1.2897947)
30. Kavokin, K. V. 2009 The puzzle of magnetic resonance effect on the magnetic compass of migratory birds. Bioelectromagnetics 30, 402-410. (doi:10.1002/bem.20485)
31. Keary, N., Ruploh, T., Voss, J., Thalau, P., Wiltschko, R., Wiltschko, W. & Bischof, H.-J. 2009 Oscillating magnetic field disrupts magnetic orientation in zebra finches, Taeniopygia guttata. Front. Zool. 6, 25. (doi:10.1186/1742-9994-6-25)
32. Lau, J. C. S., Wagner-Rundell, N., Rodgers, C. T., Green, N. J. B. & Hore, P. J. 2010 Effects of disorder and motion in a radical pair magnetoreceptor. J. R. Soc. Interface 7, S257-S264. (doi:10.1098/rsif.2009.0399. focus)
33. Liedvogel, M. & Mouritsen, H. 2010 Cryptochromes - a potential magnetoreceptor: what do we know and what do we want to know? J. R. Soc. Interface 7, S147-S162. (doi:10.1098/rsif.2009.0411.focus)
34. Liedvogel, M., Feenders, G., Wada, K., Troje, N. F., Jarvis, E. D. & Mouritsen, H. 2007a Lateralized activation of cluster N in the brains of migratory songbirds. Eur. J. Neurosci. 25, 1166-1173. (doi:10.1111/j.1460-9568. 2007.05350.x)
35. Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C. R., Hore, P. J. & Mouritsen, H. 2007b Chemical magnetoreception: bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLoS ONE 2, e1106. (doi:10.1371/journal.pone.0001106)
36. Liu, Y., Edge, R., Henbest, K., Timmel, C. R., Hore, P. J. & Gast, P. 2005 Magnetic field effect on singlet oxygen production in a biochemical system. Chem. Commun. 174-176. (doi:10.1039/b413489c)
37. Maeda, K., Henbest, K. B., Cintolesi, F., Kuprov, I., Rodgers, C. T., Liddell, P. A., Gust, D., Timmel, C. R. & Hore, P. J. 2008 Chemical compass model of avian magnetoreception. Nature 453, 387-390. (doi:10.1038/nature06834)
38. Miura, T. & Murai, H. 2008 Real-time observation of the spin-state mixing process of a micellized radical pair in weak magnetic fields by nanosecond fast field switching. J. Phys. Chem. A 112, 2526-2532. (doi:10.1021/jp077505x)
39. Möller, A., Sagasser, S., Wiltschko, W. & Schierwater, B. 2004 Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91, 585-588. (doi:10.1007/s00114-004-0578-9)
40. Mouritsen, H. & Ritz, T. 2005 Magnetoreception and its use in bird navigation. Curr. Opin. Neurobiol. 15, 406-414. (doi:10.1016/j.conb.2005.06.003)
41. Mouritsen, H., Huyvaert, K., Frost, B. & Anderson, D. 2003 Waved albatrosses can navigate with strong magnets attached to their head. J. Exp. Biol. 206, 4155-4166.
42. Mouritsen, H., Feenders, G., Liedvogel, M. & Kropp, W. 2004a Migratory birds use head scans to detect the direction of the earth's magnetic field. Curr. Biol. 14, 1946-1949. (doi:10.1016/j.cub.2004.10.025)
43. Mouritsen, H., Janssen-Bienhold, U., Liedvogel, M., Feenders, G., Stalleicken, J., Dirks, P. & Weiler, R. 2004b Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl Acad. Sci. USA 101, 14294-14299. (doi:10.1073/pnas.0405968101)
44. Mouritsen, H., Feenders, G., Liedvogel, M., Wada, K. & Jarvis, E. D. 2005 Night-vision brain area in migratory songbirds. Proc. Natl Acad. Sci. USA 102, 8339-8344. (doi:10.1073/pnas.0409575102)
45. Muheim, R., Bäckman, J. & Åkesson, S. 2002 Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J. Exp. Biol. 205, 3845-3856.
46. Muheim, R., Edgar, N. M., Sloan, K. A. & Phillips, J. B. 2006 Magnetic compass orientation in c57bl/6j mice. Learn. Behav. 34, 366-373.
47. Nemec, P., Altmann, K., Marhold, S., Burda, H. & Oelschlager, H. 2001 Neuroanatomy of magnetoreception: the superior colliculus involved in magnetic orientation in a mammal. Science 294, 366-368. (doi:10.1126/science.1063351)
48. Nemec, P., Burda, H. & Oelschlager, H. 2005 Towards the neural basis of magnetoreception: a neuroanatomical approach. Naturwissenschaften 92, 151-157. (doi:10.1007/s00114-005-0612-6)
49. O'Dea, A., Curtis, A., Green, N., Timmel, C. & Hore, P. 2005 Influence of dipolar interactions on radical pair recombination reactions subject to weak magnetic fields. J. Phys. Chem. A 109, 869-873. (doi:10.1021/jp0456943)
50. Pazur, A., Schimek, C. & Galland, P. 2007 Magnetoreception in microorganisms and fungi. Central Eur. J. Biol. 2, 597-659. (doi:10.2478/s11535- 007-0032-z)
51. Phillips, J. B., Deutschlander, M. E., Freake, M. J. & Borland, S. C. 2001 The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 204, 2543-2552.
52. Phillips, J., Borland, S., Freake, M., Brassart, J. & Kirschvink, J. 2002 'Fixed-axis' magnetic orientation by an amphibian: non-shoreward-directed compass orientation, misdirected homing or positioning a magnetite-based map detector in a consistent alignment relative to the magnetic field? J. Exp. Biol. 205, 3903-3914.
53. Prior, H., Wiltschko, R., Stapput, K., Gunturkun, O. & Wiltschko, W. 2004 Visual lateralization and homing in pigeons. Behav. Brain Res. 154, 301-310. (doi:10.1016/j.bbr.2004.02.018)
54. Rappl, R., Wiltschko, R., Weindler, P., Berthold, P. & Wiltschko, W. 2000 Orientation behaviour of garden warblers (Sylvia borin) under monochromatic light of various wavelengths. Auk 117, 256-260.
55. Rieper, E., Gauger, E., Morton, J. J. L., Benjamin, S. C. & Vedral, V. 2009 Quantum coherence and entanglement in the avian compass. (http://arxiv.org/abs/0906.3725)
56. Ritz, T., Adem, S. & Schulten, K. 2000 A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707-718. (doi:10.1016/S0006-3495(00)76629-X)
57. Ritz, T., Dommer, D. H. & Phillips, J. B. 2002 Shedding light on vertebrate magnetoreception. Neuron 34, 503-506.
58. Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. & Wiltschko, W. 2004 Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177-180. (doi:10.1038/nature02534)
59. Ritz, T., Wiltschko, R., Hore, P. J., Rodgers, C. T., Stapput, K., Thalau, P., Timmel, C. R. & Wiltschko, W. 2009 Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 96, 3451-3457. (doi:10.1016/j.bpj.2008.11.072)
60. Rodgers, C. T. & Hore, P. J. 2009 Chemical magnetoreception in birds: the radical pair mechanism. Proc. Natl Acad. Sci. USA 106, 353-360. (doi:10.1073/pnas.0711968106)
61. Rodgers, C. T., Henbest, K. B., Kukura, P., Timmel, C. R. & Hore, P. J. 2005 Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. J. Phys. Chem. A 109, 5035-5041. (doi:10.1021/jp050765z)
62. Rodgers, C. T., Norman, S. A., Henbest, K. B., Timmel, C. R. & Hore, P. J. 2007 Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. J. Am. Chem. Soc. 129, 6746-6755. (doi:10.1021/ja0682069l)
63. Rogers, L. J., Munro, U., Freire, R., Wiltschko, R. & Wiltschko, W. 2008 Lateralized response of chicks to magnetic cues. Behav. Brain Res. 186, 66-71. (doi:10.1016/j.bbr.2007.07.029)
64. Schlegel, P. A. 2007 Spontaneous preferences for magnetic compass direction in the American red-spotted newt, Notophthalmus viridescens (Salamandridae, Urodela). J. Ethol. 25, 177-184. (doi:10.1007/s10164-006-0016-x)
65. Schulten, K., Swenberg, C. E. & Weller, A. 1978 A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. NF111, 1-5.
66. Shakirov, S., Purtov, P., Grishin, Y. & Bagryanskaya, E. 2006 Electron spin exchange relaxation of radicals in low magnetic field. Mol. Phys. 104, 1739-1749. (doi:10.1080/00268970600564976)
67. Solov'yov, I. A. & Schulten, K. 2009 Magnetoreception through cryptochrome may involve superoxide. Biophys. J. 96, 4804-4813. (doi:10.1016/j.bpj.2009.03.048)
68. Solov'yov, I. A., Chandler, D. E. & Schulten, K. 2007 Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 92, 2711-2726. (doi:10.1529/biophysj.106.097139)
69. Stapput, K., Thalau, P., Wiltschko, R. & Wiltschko, W. 2008 Orientation of birds in total darkness. Curr. Biol. 18, 602-606. (doi:10.1016/j.cub.2008.03.046)
70. Stass, D., Woodward, J., Timmel, C., Hore, P. & McLauchlan, K. 2000 Radiofrequency magnetic field effects on chemical reaction yields. Chem. Phys. Lett. 329, 15-22. (doi:10.1016/S0009-2614(00)00980-5)
71. Thalau, P., Ritz, T., Stapput, K., Wiltschko, R. & Wiltschko, W. 2005 Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92, 86-90. (doi:10.1007/s00114-004-0595- 8)
72. Thalau, P., Ritz, T., Burda, H., Wegner, R. E. & Wiltschko, R. 2006 The magnetic compass mechanisms of birds and rodents are based on different physical principles. J. R. Soc. Interface 3, 583-587. (doi:10.1098/rsif.2006. 0130)
73. Timmel, C. & Henbest, K. 2004 A study of spin chemistry in weak magnetic fields. Phil. Trans. R. Soc. Lond. A 362, 2573-2589. (doi:10.1098/rsta.2004.1459)
74. Timmel, C. & Hore, P. 1996 Oscillating magnetic field effects on the yields of radical pair reactions. Chem. Phys. Lett. 257, 401-408. (doi:10.1016/0009-2614(96)00466-6)
75. Timmel, C., Till, U., Brocklehurst, B., McLauchlan, K. & Hore, P. 1998 Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys. 95, 71-89. (doi:10.1080/00268979809483134)
76. Timmel, C., Cintolesi, F., Brocklehurst, B. & Hore, P. 2001 Model calculations of magnetic field effects on the recombination reactions of radicals with anisotropic hyperfine interactions. Chem. Phys. Lett. 334, 387-395. (doi:10.1016/S0009-2614(00)01436-6)
77. Ugolini, A. 2006 Equatorial sandhoppers use body scans to detect the earth's magnetic field. J. Comp. Physiol. A 192, 45-49. (doi:10.1007/s00359-005- 0046-9)
78. Vacha, M. & Soukopova, H. 2004 Magnetic orientation in the mealworm beetle tenebrio and the effect of light. J. Exp. Biol. 207, 1241-1248. (doi:10.1242/jeb.00874)
79. Vacha, M., Drstkova, D. & Puzova, T. 2008a Tenebrio beetles use magnetic inclination compass. Naturwissenschaften 95, 761-765. (doi:10.1007/s00114-008-0377-9)
80. Vacha, M., Puzova, T. & Drstkova, D. 2008b Effect of light wavelength spectrum on magnetic compass orientation in Tenebrio molitor. J. Comp. Physiol. A 194, 853-859. (doi:10.1007/s00359-008-0356-9)
81. Vacha, M., Puzova, T. & Kvícalova, M. 2009 Radiofrequency magnetic fields disrupt magnetoreception in American cockroach. J. Exp. Biol. 212, 3473-3477. (doi:10.1242/jeb.028670)
82. Vaughan, T. & Weaver, J. 2005 Molecular change signal-tonoise criteria for interpreting experiments involving exposure of biological systems to weakly interacting electromagnetic fields. Bioelectromagnetics 26, 305-322. (doi:10.1002/bem.20094)
83. Vink, C. & Woodward, J. 2004 Effect of a weak magnetic field on the reaction between neutral free radicals in isotropic solution. J. Am. Chem. Soc. 126, 16730-16731. (doi:10.1021/ja043945f)
84. Voss, J., Keary, N. & Bischof, H.-J. 2007 The use of the geomagnetic field for short distance orientation in zebra finches. Neuroreport 18, 1053-1057.
85. Wang, K. & Ritz, T. 2006 Zeeman resonances for radical-pair reactions in weak static magnetic fields. Mol. Phys. 104, 1649-1658. (doi:10.1080/ 00268970600564869)
86. Wang, K., Mattern, E. & Ritz, T. 2006 On the use of magnets to disrupt the physiological compass of birds. Phys. Biol. 3, 220-231. (doi:10.1088/1478-3975/3/3/007)
87. Weaver, J. 2002 Understanding conditions for which biological effects of nonionizing electromagnetic fields can be expected. Bioelectrochemistry 56, 207-209.
88. Weaver, J., Vaughan, T. & Astumian, R. 2000 Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature 405, 707-709. (doi:10.1038/35015128)
89. Wiltschko, W. & Wiltschko, R. 2007 Magnetoreception in birds: two receptors for two different tasks. J. Ornithol. 148, S61-S76. (doi:10.1007/s10336-007-0233-2)
90. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. 1993 Red light disrupts magnetic orientation of migratory birds. Nature 364, 525-527. (doi:10.1038/364525a0)
91. Wiltschko, W., Beason, R. B., Munro, U., Ford, H. & Wiltschko, R. 1994 A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Cell. Mol. Life Sci. 50, 697-700. (doi:10.1007/BF01952877)
92. Wiltschko, W., Wiltschko, R. & Munro, U. 2000a Light-dependent magnetoreception in birds: does directional information change with light intensity? Naturwissenschaften 87, 36-40.
93. Wiltschko, W., Wiltschko, R. & Munro, U. 2000b Light-dependent magnetoreception in birds: the effect of intensity of 565-nm green light. Naturwissenschaften 87, 366-369.
94. Wiltschko, W., Gesson, M. & Wiltschko, R. 2001 Magnetic compass orientation of European robins under 565 nm green light. Naturwissenschaften 88, 387-390.
95. Wiltschko, W., Numro, U., Wiltschko, R. & Kirschvink, J. 2002a Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behaviour. J. Exp. Biol. 205, 3031-3037.
96. Wiltschko, W., Traudt, J., Güntürkün, O., Prior, H. & Wiltschko, R. 2002b Lateralization of magnetic compass orientation in a migratory bird. Nature 419, 467-470. (doi:10.1038/nature00958)
97. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. 2003a Magnetic orientation in birds: non-compass responses under monochromatic light of increased intensity. Proc. R. Soc. Lond. B 270, 2133-2140. (doi:10.1098/rspb. 2003.2476)
98. Wiltschko, W., Munro, U., Ford, H. & Wiltschko, R. 2003b Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis. Austral. J. Zool. 51, 597-602. (doi:10.1071/ZO03022)
99. Wiltschko, W., Gesson, M., Stapput, K. & Wiltschko, R. 2004a Light-dependent magnetoreception in birds: interaction of at least two different receptors. Naturwissenschaften 91, 130-134. (doi:10.1007/s00114-003-0500-x)
100. Wiltschko, W., Möller, A., Gesson, M., Noll, C. & Wiltschko, R. 2004b Light-dependent magnetoreception in birds: analysis of the behaviour under red light after pre-exposure to red light. J. Exp. Biol. 207, 1193-1202. (doi:10.1242/jeb.00873)
101. Wiltschko, R., Ritz, T., Stapput, K., Thalau, P. & Wiltschko, W. 2005 Two different types of light-dependent responses to magnetic fields in birds. Curr. Biol. 15, 1518-1523. (doi:10.1016/j.cub.2005.07.037)
102. Wiltschko, W., Stapput, K., Thalau, P. & Wiltschko, R. 2006 Avian magnetic compass: fast adjustment to intensities outside the normal functional window. Naturwissenschaften 93, 300-304. (doi:10.1007/s00114-006-0102-5)
103. Wiltschko, R., Stapput, K., Bischof, H.-J. & Wiltschko, W. 2007a Light-dependent magnetoreception in birds: increasing intensity of monochromatic light changes the nature of the response. Front. Zool. 4, 5. (doi:10.1186/1742-9994-4-5)
104. Wiltschko, R., Stapput, K., Ritz, T., Thalau, P. & Wiltschko, W. 2007b Magnetoreception in birds: different physical processes for two types of directional responses. HFSP J. 1, 41-48. (doi:10.2976/1.2714294)
105. Wiltschko, W., Ford, H., Munro, U., Winklhofer, M. & Wiltschko, R. 2007c Magnetite-based magnetoreception: the effect of repeated pulsing on the orientation of migratory birds. J. Comp. Physiol. A 193, 515-522. (doi:10.1007/s00359-006-0207-5)
106. Wiltschko, W., Freire, R., Munro, U., Ritz, T., Rogers, L., Thalau, P. & Wiltschko, R. 2007d The magnetic compass of domestic chickens, Gallus gallus. J. Exp. Biol. 210, 2300-2310. (doi:10.1242/jeb.004853)
107. Wiltschko, R., Stapput, K., Thalau, P. & Wiltschko, W. 2010 Directional orientation of birds by the magnetic field under different light conditions. J. R. Soc. Interface 7, S163-S177. (doi:10.1098/rsif.2009.0367. focus)
108. Wilzeck, C., Wiltschko, W., Güntürkün, O., Wiltschko, R. & Prior, H. 2010 Lateralization of magnetic compass orientation in pigeons. J. R. Soc. Interface 7, S235-S240. (doi:10.1098/rsif.2009.0436.focus)
109. Woodward, J., Timmel, C., McLauchlan, K. & Hore, P. 2001 Radio frequency magnetic field effects on electron-hole recombination. Phys. Rev. Lett. 87, 077 602. (doi:10.1103/PhysRevLett.87.077602)
110. Woodward, J. R. & Vink, C. B. 2007 Hyperfine coupling dependence of the effects of weak magnetic fields on the recombination reactions of radicals generated from polymerisation photoinitiators. Phys. Chem. Chem. Phys. 9, 6272-6278. (doi:10.1039/b711635g)
111. Yoshii, T., Ahmad, M. & Helfrich-Foerster, C. 2009 Cryptochrome mediates light-dependent magnetosensitivity of drosophila's circadian clock. PLoS Biol. 7, 813-819. (doi:10.1371/journal.pbio.1000086)
112. Zapka, M. et al. 2009 Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274-1277. (doi:10.1038/nature08528)