Sensory SystemsSensory SystemsСенсорные системы0235-00923034-5936The Russian Academy of Sciences67581510.31857/S023500922301002XATMYMYОБЗОРЫRelationship of the magnetic compass and vision in birds: in search of a receptor cellСвязь магнитного компаса и зрения у птиц: в поисках рецепторной клеткиAstakhovaL. A.АстаховаЛ. А.lubkins@yandex.ruRotovA. Yu.РотовА. Ю.lubkins@yandex.ruChernetsovN. S.ЧернецовН. С.lubkins@yandex.ruSechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of SciencesИнститут эволюционной физиологии и биохимии им. И.М. Сеченова РАНSt. Petersburg State UniversityИнститут физиологии им. Л.А. Орбели НАН РАSt. Petersburg State UniversityС.-Петербургский государственный университетOrbeli Institute of Physiology of NAS RAЗоологический институт РАН0101202337131628022025Copyright ©; 2023, Russian Academy of SciencesCopyright ©; 2023, Российская академия наук2023Russian Academy of SciencesРоссийская академия наукhttps://journals.eco-vector.com/0235-0092/article/view/675815

The existence of the magnetic compass system was first shown in birds. Since then, a large amount of data has been accumulated on the performance of the avian magnetic compass and its relationship with visual reception. The current dominant concept is that the receptor for the magnetic compass in birds is located in the retina. The most popular hypothesis for the mechanism of operation of magnetic field receptors is the radical pair model, and a candidate for the role of the primary magnetoreceptor molecule is cryptochrome, and more specifically, its isoform, cryptochrome 4a. In recent years, data have been published on the interaction of cryptochrome with some proteins involved in the phototransduction cascade, as well as promising data from electrophysiological studies combining light and magnetic stimuli. In addition, a number of morphological studies of the avian retina also allow us to narrow down the range of promising cells for the role of a magnetoreceptor, and the double cone is currently the most likely candidate. In this review, we discuss the latest research data in this area.

Наличие системы магнитного компаса было впервые показано у птиц. С тех пор было аккумулировано большое количество данных о работе магнитного компаса птиц и его взаимосвязи со зрительной рецепцией. Сейчас доминирует представление о том, что рецептор, обеспечивающий работу магнитного компаса, у птиц находится в сетчатке глаза. Наиболее популярной гипотезой относительно того, как работают рецепторы магнитного поля, является гипотеза радикальных пар, а кандидатом на роль первичной магниторецепторной молекулы является криптохром, и более конкретно, его изоформа криптохром типа 4a. В последние годы появились сведения о взаимодействии криптохрома с некоторыми белками-участниками каскада фототрансдукции, а также многообещающие данные электрофизиологических исследований, сочетающих в себе зрительные (световые) и магнитные стимулы. Кроме того, ряд морфологических исследований сетчатки птиц также помогает сузить круг возможных клеток-кандидатов на роль магниторецептора, и наиболее вероятной такой клеткой в настоящее время является двойная колбочка. В настоящем обзоре мы обсуждаем последние исследования в данной области.

birdsmagnetic compassretinacryptochromeconeптицымагнитный компассетчаткакриптохромколбочкаAstakhova L.A., Rotov A.Yu., Kavokin K.V., Chernetsov N.S., Firsov M.L. Relationship between avian magnetic compass and photoreception: hypotheses and unresolved questions. Biology Bulletin Reviews. 2020. V. 10 (1). P. 1–10. https://doi.org/10.1134/S2079086420010028Chernetsov N.S. Orientation and navigation of migrating birds. Biology Bulletin. 2016. V. 43 (8). P. 788–803. https://doi.org/10.1134/S1062359016080069Ahlers M.T., Block C.T., Winklhofer M., Greschner M. Integration and evaluation of magnetic stimulation in physiology setups. PloS one. 2022. V. 17 (7). P. e0271765. https://doi.org/10.1371/journal.pone.0271765Åkesson S. The ecology of polarisation vision in birds. In: Polarized light and polarization vision in animal sciences. Berlin. Springer, Heidelberg. 2014. P. 275–292. https://doi.org/10.1007/978-3-642-54718-8_12Arshavsky V.Y., Burns M.E. Current understanding of signal amplification in phototransduction. Cell. Logist. 2014. V. 4. P. e28680. https://doi.org/10.4161/cl.29390Astakhova L.A., Rotov A.Y., Cherbunin R.V., Goriachenkov A.A., Kavokin K.V., Firsov M.L., Chernetsov N. Electroretinographic study of the magnetic compass in European robins. Proceedings of the Royal Society B. 2020.б V. 287. № 1940. P. 20202507. https://doi.org/10.1098/rspb.2020.2507Baden T., Osorio D. The retinal basis of vertebrate color vision. Annu. ReV. Vis. Sci. 2019. V. 5. P. 177–200. https://doi.org/10.20944/preprints201811.0498.v1Bailey M.J., Cassone, V.M. Melanopsin expression in the chick retina and pineal gland. Molecular Brain Research. 2005. V. 134 (2). P. 345–348. https://doi.org/10.1016/j.molbrainres.2004.11.003Balay S.D., Hochstoeger T., Vilceanu A., Malkemper E.P., Snider W., Dürnberger G., Mechtler K., Schuechner S., Ogris E., Nordmann G.C., Ushakova L. The expression, localisation and interactome of pigeon CRY2. Scientific reports. 2021. V. 11 (1). P. 1–13. https://doi.org/10.1038/s41598-021-99207-xBeason R.C., Semm P. Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neuroscience letters. 1987. V. 80 (2). P. 229–234. https://doi.org/10.1016/0304-3940(87)90659-8Bischof H.J., Nießner C., Peichl L., Wiltschko R., Wiltschko W. Avian ultraviolet/violet cones as magnetoreceptors: The problem of separating visual and magnetic information. Communicative and integrative biology. 2011. V. 4 (6). P. 713–716. https://doi.org/10.4161/cib.17338Bolte P., Einwich A., Seth P.K., Chetverikova R., Heyers D., Wojahn I., Janssen-Bienhold U., Feederle R., Hore P., Dedek K., Mouritsen Y. Cryptochrome 1a localisation in light- and dark-adapted retinae of several migratory and non-migratory bird species: No signs of light-dependent activation. Ethol. Ecol. Evol. 2021. V. 33. P. 248–272. https://doi.org/10.1080/03949370.2020.1870571Bottesch M., Gerlach G., Halbach M., Bally A., Kingsford M.J., Mouritsen M. A magnetic compass that might help coral reef fish larvae return to their natal reef. Curr. Biol. 2016. V. 26. P. R1266–R1267. https://doi.org/10.1016/j.cub.2016.10.051Briggman K.L., Euler T. Bulk electroporation and population calcium imaging in the adult mammalian retina. Journal of neurophysiology. 2011. V. 105 (5). P. 2601–2609. https://doi.org/10.1152/jn.00722.2010Chaves I., Pokorny R., Byrdin M., Hoang N., Ritz T., Brettel K., Essen L.O., van der Horst G.T., Batschauer A., Ahmad M. The cryptochromes: blue light photoreceptors in plants and animals. Annu. ReV. Plant. Biol. 2011. V. 62 (1). P. 335–364. https://doi.org/10.1146/annurev-arplant-042110-103759Chernetsov N., Nikishena I., Zavarzina N., Kulbach O. Perception of static magnetic field by humans: a review. Biol. Comm. 2021. V. 66 (2). P. 171–178. https://doi.org/10.21638/spbu03.2021.208Chetverikova R., Dautaj G., Schwigon L., Dedek K., Mouritsen H. Double cones in the avian retina form an oriented mosaic which might facilitate magnetoreception and/or polarized light sensing. J. R. Soc. Interface. 2022. V. 19. P. 20210877. https://doi.org/10.1098/rsif.2021.0877Collin J.P., Oksche A., Structural and functional relationships in the nonmammalian pineal gland. The pineal gland. 1981. V. 1. P. 27–67.Deutschlander M.E., Freake M.J., Borland S.C., Phillips J.B., Madden R.C., Anderson L.E., Wilson B.W. Learned magnetic compass orientation by the Siberian hamster, Phodopus sungorus. Anim. Behav. 2003. V. 65 (4). P. 779–786. https://doi.org/10.1006/anbe.2003.2111Diego-Rasilla F.J., Luengo R.M., Phillips J.B. Use of a light-dependent magnetic compass for y-axis orientation in European common frog (Rana temporaria) tadpoles. J. Comp. Physiol. A. 2013. V. 199. P. 619–628. https://doi.org/10.1007/s00359-013-0811-0Dreyer D., Frost B., Mouritsen H., Günther A., Green K., Whitehouse M., Johnsen S., Heinze S., Warrant E. The Earth’s magnetic field and visual landmarks steer migratory flight behaviour in the nocturnal Australian Bogong moth. Curr. Biol. 2018. V. 28 (13). P. 2160–2166.e5. https://doi.org/10.1016/j.cub.2018.05.030Einwich A., Seth P.K., Bartölke R., Bolte P., Feederle R., Dedek K., Mouritsen H. Localisation of cryptochrome 2 in the avian retina. Journal of Comparative Physiology A. 2022. V. 208 (1). P. 69–81. https://doi.org/10.1007/s00359-021-01506-1Engels S., Schneider N.-L., Lefeldt N., Hein C.M., Zapka M., Michalik A., Elbers D., Kittel A., Hore P.J., Mouritsen H. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature. 2014. V. 509 (7500). P. 353–356. https://doi.org/10.1038/nature13290Euler T., Franke K., Baden T. Studying a light sensor with light: multiphoton imaging in the retina. Multiphoton Microscopy. Humana, New York, NY, 2019. P. 225–250. https://doi.org/10.1007/978-1-4939-9702-2_10Finkelstein A., Las L., Ulanovsky N. 3-D maps and compasses in the brain. Annu. Re.V. Neurosci. 2016. V. 39. P. 171–196. https://doi.org/10.1146/annurev-neuro-070815-013831Fleischmann P.N., Grob R., Müller V.L., Wehner R., Rössler W. The geomagnetic field is a compass cue in Cataglyphis ant navigation. Current Biology, (2018). V. 28 (9). P. 1440–1444. https://doi.org/10.1016/j.cub.2018.03.043Gegear R.J., Casselman A., Waddell S., Reppert S.M. Cryptochrome mediates light-dependent magnetosensitivity in Drosophila. Nature. 2008. V. 454. P. 1014–1018. https://doi.org/10.1038/nature07183Görtemaker K., Yee C., Bartölke R., Behrmann H., Voß J.-O., Schmidt J., Xu J., Solovyeva V., Leberecht B., Behrmann E., Mouritsen H., Koch K.-W. Direct interaction of avian cryptochrome 4 with a cone specific G-protein. Cells. 2022. V. 11. P. 2043. https://doi.org/10.3390/cells11132043Guerra P.A., Gegear R.J., Reppert S.M., 2014. A magnetic compass aids monarch butterfly migration. Nature Comm. 2014. V. 5. P. 4164. https://doi.org/10.1038/ncomms5164Günther A., Dedek K., Haverkamp S., Irsen S., Briggman K.L., Mouritsen H. Double cones and the diverse connectivity of photoreceptors and bipolar cells in an avian retina. Journal of Neuroscience. 2021. V. 41 (23). P. 5015–5028. https://doi.org/10.1523/JNEUROSCI.2495-20.2021Günther A., Einwich A., Sjulstok E., Feederle R., Bolte P., Koch K.-W., Solov’yov I.A., Mouritsen H. Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4. Curr. Biol. 2018. V. 28. P. 211–223. https://doi.org/10.1016/j.cub.2017.12.003Hart N.S. The visual ecology of avian photoreceptors. Progress in retinal and eye research. 2001. V. 20 (5). P. 675–703. https://doi.org/10.1016/S1350-9462(01)00009-XHeyers D., Manns M., Luksch H., Güntürkün O., Mouritsen H. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One. 2007. V. 2 (9). P. e937. https://doi.org/10.1371/journal.pone.0000937Heyers D., Musielak I., Haase K. Herold C., Bolte P. Güntürkün O., Mouritsen H. Morphology, biochemistry and connectivity of Cluster N and the hippocampal formation in a migratory bird. Brain Struct Funct. 2022 P. 1–19. https://doi.org/10.1007/s00429-022-02566-yHiscock H.G., Mouritsen H., Manolopoulos D.E., Hore P.J. Disruption of magnetic compass orientation in migratory birds by radiofrequency electromagnetic fields. Biophys. J. 2017. V. 113 (7). P. 1475–1484. https://doi.org/10.1016/j.bpj.2017.07.031Holland R., Thorup K., Vonhof M.J., Cochran W.W., Wikelski M. Bat orientation using Earth’s magnetic field. Nature. 2006. V. 444. P. 702. https://doi.org/10.1038/444702aHore P.J., Mouritsen H. The radical-pair mechanism of magnetoreception. Annu. ReV. Biophys. 2016. V. 45. P. 299–344. https://doi.org/10.1146/annurev-biophys-032116-09454Jasiński A. Fine structure of capillaries in the pecten oculi of the sparrow, Passer domesticus. Zeitschriftfür Zellforschung und Mikroskopische Anatomie. 1973. V. 146 (2). P. 281–292. https://doi.org/10.1007/BF00307352Johnsen S., Mattern E., Ritz T. Light-dependent magnetoreception: quantum catches and opponency mechanisms of possible photosensitive molecules. J. ExP. Biol. 2007. V. 210 (18). P. 3171–3178. https://doi.org/10.1242/jeb.007567Kavokin K. The puzzle of magnetic resonance effect on the magnetic compass of migratory birds. Bioelectromagnetics. 2009. V. 30. P. 402–410. https://doi.org/10.1002/bem.20485Kelber A. Bird colour vision–from cones to perception. Current Opinion in Behavioral Sciences. 2019. V. 30. P. 34–40. https://doi.org/10.1016/j.cobeha.2019.05.003Kirschfeld K. Spectral sensitivity of the accessory optic system of the pigeon. J Comp Physiol A. 1998. V. 183. P. 1–6. https://doi.org/10.1007/s003590050229Kobylkov D., Wynn J., Winklhofer M., Chetverikova R., Xu J., Hiscock H., Hore P. J., Mouritsen H. Electromagnetic 0.1–100 kHz noise does not disrupt orientation in a night-migrating songbird implying a spin coherence lifetime of less than 10 µs. J. R. Soc. Interface. 2019. V. 16 (161). P. 20190716. https://doi.org/10.1098/rsif.2019.0716Leberecht B., Kobylkov D., Karwinkel T., Döge S., Burnus L., et al.. Broadband 75–85 MHz radiofrequency fields disrupt magnetic compass orientation in night‑migratory songbirds consistent with a flavin‑based radical pair magnetoreceptor. J. ComP. Physiol. A. 2022. V. 208: P. 97–106. https://doi.org/10.1007/s00359-021-01537-8Lohmann K.L., Pentcheff N.D., Nevitt G.A., Stetten G.D., Zimmer-Faust R.K., Jarrard H.E., Boles L.S. Magnetic orientation of spiny lobsters in the ocean: experiments with undersea coil systems. J. ExP. Biol. 1995. V. 198. P. 2041–2048. https://doi.org/10.1242/jeb.198.10.2041Malewski S., Begall S., Burda H. Learned and spontaneous magnetosensitive behaviour in the Roborovski hamster (Phodopus roborovskii). Ethology. 2018. V. 124 (6). P. 423–431. https://doi.org/10.1111/eth.12744Melgar J., Lind O., Muheim R. No response to linear polarization cues in operant conditioning experiments with zebra finches. The Journal of Experimental Biology. 2015. V. 218 (13). P. 2049–2054. https://doi.org/10.1242/jeb.122309Michael A.K., Fribourgh J.L., Van Gelder R.N., Partch C.L., Animal cryptochromes: Divergent roles in light perception, circadian timekeeping and beyond. Photochem. Photobiol. 2017. V. 93. P. 128–140. https://doi.org/10.1111/phP.12677Mouritsen H. Long-distance navigation and magnetoreception in migratory animals. Nature. 2018. V. 558 (7708). P. 50–59. https://doi.org/10.1038/s41586-018-0176-1Mouritsen H., Feenders G., Liedvogel M., Wada K., Jarvis E.D. Night-vision brain area in migratory songbirds. Proc. Natl. Acad. Sci. U.S.A. 2005. V. 102 (23). P. 8339–8344. https://doi.org/10.1073/pnas.0409575102Muheim R. Behavioural and physiological mechanisms of polarized light sensitivity in birds. Philosophical Transactions of the Royal Society B: Biological Sciences. 2011. V. 366 (1565). P. 763–771. https://doi.org/10.1098/rstb.2010.0196Muheim R., Bäckman J., Åkesson S. Magnetic compass orientation in European robins is dependent on both wavelength and intensity of light. J. ExP. Biol. 2002. V. 205. № 24. P. 3845–3856. https://doi.org/10.1242/jeb.205.24.3845Munro U., Munro J.A., Phillips J.B., Wiltschko W. Effect of wavelength of light and pulse magnetisation on different magnetoreception systems in a migratory bird. Aust. J. Zool. 1997. V. 45 (2). P. 189–198. https://doi.org/10.1071/ZO96066Nießner C., Denzau S., Gross J.C., Peichl L., Bischof H.J., Fleissner G., WiltschkoW., Wiltschko R. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS ONE. 2011. V. 6. P. e20091. https://doi.org/10.1371/journal.pone.0020091Nießner C., Denzau S., Peichl L., Wiltschko W., Wiltschko R. Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle. J. ExP. Biol. 2014. V. 217. P. 4221–4224. https://doi.org/10.1242/jeb.110965Pakhomov A., Bojarinova J., Cherbunin R., Chetverikova R., Grigoryev P.S., Kavokin K., Kobylkov D., Lubkov-skaja R., Chernetsov N. Very weak oscillating magnetic field disrupts the magnetic compass of songbird migrants. J. R. Soc. Interface. 2017. V. 14 (133). P. 20170364. https://doi.org/10.1098/rsif.2017.0364Pinzon-Rodriguez A., Muheim R. Zebra finches have a light-dependent magnetic compass similar to migratory birds. J. Exp Biol. 2017. V. 220. P. 1202–1209. https://doi.org/10.1242/jeb.148098Pinzon-Rodriguez A., Muheim R. Cryptochrome expression in avian UV cones: revisiting the role of CRY1 as magnetoreceptor. Scientific reports. 2021. V. 11 (1). P. 1–13. https://doi.org/10.1038/s41598-021-92056-8Pugh E.N.Jr., Lamb T.D. Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and light adaptation. In Handbook of Biological Physics. New York, NY, USA. Elsevier Science. 2000. P. 183–255.10. https://doi.org/10.1016/S1383-8121(00)80008-1Quesada A., Génis-Gálvez J. M. Morphological and structural study of Landolt’s club in the chick retina. Journal of Morphology. 1985. V. 184 (2). P. 205–214. https://doi.org/10.1002/jmor.1051840210Quinn T.P. Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J. ComP. Physiol. 1980. V. 137. P. 243–248. https://doi.org/10.1007/BF00657119Ramírez E., Marín G., Mpodozis J., Letelier J.C. Extracellular recordings reveal absence of magneto sensitive units in the avian optic tectum. J. ComP. Physiol. A. 2014. V. 200(12). P. 983-996. https://doi.org/10.1007/s00359-014-0947-6Rappl R., Wiltschko R., Weindler P., Berthold P., Wiltschko W. Orientation behavior of Garden Warblers, Sylvia borin, under monochromatic light of various wavelengths. Auk. 2000. V. 117 (1). P. 256–260. https://doi.org/10.1093/auk/117.1.256Ritz T., Adem S., Schulten K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 2000. V. 78 (2). P. 707–718. https://doi.org/10.1016/S0006-3495(00)76629-XRitz T., Thalau P., Phillips J.B., Wiltschko R., Wiltschko W. Resonance effects indicate a radical pair mechanism for avian magnetic compass. Nature. 2004. V. 429. P. 177–180. https://doi.org/10.1038/nature02534Ritz T., Wiltschko R., Hore P.J., Rodgers C.T., Stapput K., Thalau P., Timmel C.R., Wiltschko W. Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophys. J. 2009. V. 96. P. 3451–3457. https://doi.org/10.1016/j.bpj.2008.11.072Roberts N.W., Porter M.L., Cronin T.W. The molecular basis of mechanisms underlying polarization vision. Philosophical Transactions of the Royal Society B: Biological Sciences. 2011. V. 366 (1565). P. 627–637. https://doi.org/10.1098/rstb.2010.0206Rotov A.Y., Cherbunin R.V., Anashina A., Kavokin K.V., Chernetsov N., Firsov M.L., Astakhova L.A. Searching for magnetic compass mechanism in pigeon retinal photoreceptors. Plos one. 2020. V. 15 (3). P. e0229142. https://doi.org/10.1371/journal.pone.0229142Rotov A.Y., Cherbunin R.V., Kavokin K.V., Chernetsov N.S., Firsov M.L., Astakhova L.A. Magnetoreception in the retina of the domestic pigeon Columbia livia: a retinographic search. Journal of Evolutionary Biochemistry and Physiology. 2018. V. 54 (6), P. 498–501. https://doi.org/10.1134/S00220930180600121Rotov A.Y., Goriachenkov A.A., Cherbunin R.V., Firsov M.L., Chernetsov N., Astakhova L.A. Magnetoreceptory Function of European Robin Retina: Electrophysiological and Morphological Non-Homogeneity. Cells. 2022. V. 11 (9). P. 3056. https://doi.org//10.3390/cells11193056Schneider T., Thalau H.P., Semm P., Wiltschko W. Melatonin is crucial for the migratory orientation of pied flycatchers (Ficedula hypoleuca Pallas). J. Exp. Biol. 1994. V. 194 (1). P. 255–262. https://doi.org/10.1242/jeb.194.1.255Schulten K. Magnetic field effects in chemistry and biology. Festkörperprobleme. 1982. V. 22. P. 61–83. https://doi.org/10.1007/BFb0107935Schulten K., Swenberg C.E., Weller A. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. (NF). 1978. V. 111 (1). P. 1–5. https://doi.org/10.1524/zpch.1978.111.1.001Schulten K., Windemuth A. Model for a physiological magnetic compass. Biophysical Effects of Steady Magnetic Fields. Proc. Physics. Ed. Maret G., Boccara N., Kiepenheuer J. Berlin: Springer. 1986. V. 11. P. 99–106.Seifert M., Baden T., Osorio D. The retinal basis of vision in chicken. Seminars in cell & developmental biology. 2020. V. 106. P. 106–115. https://doi.org/10.1016/j.semcdb.2020.03.011Semm P., Beason R.C. Responses to small magnetic variations by the trigeminal system of the bobolink. Brain research bulletin. 1990. V. 25 (5). P. 735–740. https://doi.org/10.1016/0361-9230(90)90051-ZSemm P., Demaine C. Neurophysiological properties of magnetic cells in the pigeon’s visual system. J. Comp. Physiol. A. 1986. V. 159 (5). P. 619–625. https://doi.org/10.1007/BF00612035Seth P.K., Balaji V., Dedek K. The retinal circuitry for magnetoreception in migratory birds. Neuroforum. 2021. V. 27 (3). P. 159–166. https://doi.org/10.1515/nf-2021-0007Shakhparonov V.V., Ogurtsov S.V. Marsh frogs, Pelophylax ridibundus, determine migratory direction by magnetic field. J. Comp. Physiol. A. 2017. V. 203 (1). P. 35–43. https://doi.org/10.1007/s00359-016-1132-xSmith E.L., Greenwood V.J., Bennett A.T.D. Ultraviolet colour perception in European starlings and Japanese quail. Journal of Experimental Biology. 2002. V. 205 (21). P. 3299–3306. https://doi.org/10.1242/jeb.205.21.3299Stapput K., Thalau P., Wiltschko R., Wiltschko W. Orientation of birds in total darkness. Curr. Biol. 2008. V. 18 (8). P. 602–606. https://doi.org/10.1016/j.cub.2008.03.046Thalau P., Ritz T., Stapput K., Wiltschko R., Wiltschko W. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften. 2005. V. 92 (2). P. 86–90. https://doi.org/10.1007/s00114-004-0595Toomey M.B., Corbo J.C. Evolution, development and function of vertebrate cone oil droplets. Frontiers in Neural Circuits. 2017. V. 11. P. 97. https://doi.org/10.3389/fncir.2017.00097Walcott C., Green R.P. Orientation of homing pigeons altered by a change in the direction of an applied magnet field. Science. 1974. V. 184. P. 180–182. https://doi.org/10.1126/science.184.4133.180Wilby D., Roberts N.W. Optical influence of oil droplets on cone photoreceptor sensitivity. Journal of Experimental Biology. 2017. V. 220 (11). P. 1997–2004. https://doi.org/10.1242/jeb.152918Willis A.M., Wilkie D.A. Avian ophthalmology part 1: anatomy, examination, and diagnostic techniques. Journal of Avian Medicine and Surgery. 1999. P. 160–166. https://doi.org/www.jstor.org/stable/30130679Wiltschko R., Munro U., Ford H., Stapput K., Wiltschko W. Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light. J. Exp. Biol. 2008. V. 211 (20). P. 3344–3350. https://doi.org/10.1242/jeb.020313Wiltschko R., Nießner C., Wiltschko W. The magnetic compass of birds: The role of cryptochrome. Front. Physiol. 2021. V. 12. P. 667000. https://doi.org/10.3389/fphys.2021.667000Wiltschko R., Ritz T., Stapput K., Thalau P., Wiltschko W. Two different types of light-dependent responses to magnetic fields in birds. Curr. Biol. 2008. V. 15 (16). P. 1518–1523. https://doi.org/10.1016/j.cub.2005.07.037Wiltschko R., Wiltschko W. Pigeon homing: effect of various wavelengths of light during displacement. Naturwissenschaften. 1998. V. 85. P. 164–167.Wiltschko W. Über den Einfluβ statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z. Tierpsychol. 1968. V. 25. P. 537–558. https://doi.org/10.1111/j.1439-0310.1968.tb00028.xWiltschko W. Further analysis of the magnetic compass of migratory birds. In Animal migration, navigation and homing. Berlin. Springer. 1978. P. 301–310. https://doi.org/10.1007/978-3-662-11147-5_29Wiltschko W., Freire R., Munro U., Ritz T., Rogers L., Thalau P., Wiltschko R. The magnetic compass of domestic chickens. J. Exp. Biol. 2007. V. 210. P. 2300–2310.Wiltschko W., Gesson M., Wiltschko R. Magnetic compass orientation of European robins under 565 nm green light. Naturwissenschaften. 2001. V. 88 (9). P. 387–390. https://doi.org/10.1007/s001140100248Wiltschko W., Munro U., Ford H., Wiltschko R. Red light disrupts magnetic orientation of migratory birds. Nature. 1993. V. 364 (6437). P. 525–527. https://doi.org/10.1038/364525a0Wiltschko W., Wiltschko R. Magnetic compass of European robins. Science. 1972. V. 176 (4030). P. 62–64. https://doi.org/10.1126/science.176.4030.62Wiltschko W., Wiltschko R. Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse. J. Comp. Physiol. A. 1995. V. 177 (3). P. 363–369. https://doi.org/10.1007/BF00192425Wiltschko W., Wiltschko R. The effect of yellow and blue light on magnetic compass orientation in European Robins, Erithacus rubecula. J. Comp. Physiol. A. 1999. V. 184 (3). P. 295–299. https://doi.org/10.1007/s003590050327Wiltschko W., Wiltschko R. Light-dependent magnetoreception in birds: the behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J. Exp. Biol. 2001. V. 204(19). P. 3295–3302. https://doi.org/10.1242/jeb.204.19.3295Wiltschko W., Wiltschko R., Munro U. Light-dependent magnetoreception in birds: the effect of intensity of 565 nm green light. Naturwissenschaften. 2000. V. 87(8). P. 366–369. https://doi.org/10.1007/s001140050742Wingstrand K.G., Munk O. The pectin oculi of the pigeon with particular regard to its function. Biol. Skr. Danske Viden. Selsk. (Copenhagen) 1965. V. 14. P. 1–64.Woodcock M.E., Idoko-Akoh A., McGrew M. J. Gene editing in birds takes flight. Mammalian Genome. 2017. V. 28 (7). P. 315–323. https://doi.org/10.1007/s00335-017-9701-zWorster S., Mouritsen H., Hore P.J. A light-dependent magnetoreception mechanism insensitive to light intensity and polarization. J. Royal society interface. 2017. V. 14 (134). P. 20170405. https://doi.org/10.1098/rsif.2017.0405Wu H., Scholten A., Einwich A., Mouritsen H., Koch K.W. Protein-protein interaction of the putative magnetoreceptor cryptochrome 4 expressed in the avian retina. Scientific reports, 2020. V. 10 (1). P. 1–13. https://doi.org/10.1038/s41598-020-64429-yXu J., Jarocha L.E., Zollitsch T., Konowalczyk M., Henbest K.B., et al. Magnetic sensitivity of cryptochrome 4 from a migratory songbird. Nature 2021. V. 594. P. 535–540. https://doi.org/10.1038/s41586-021-03618-9Zapka M., Heyers D., Hein C.M., Engels S., Schneider N.-L., Hans J., Weiler S., Dreyer D., Kishkinev D., Wild M., Mouritsen H. Visual, but not trigeminal, mediation of magnetic compass information in a migratory bird. Nature. 2009. V. 461 (7268). P. 1274–1277. https://doi.org/10.1038/nature08528Zoltowski B.D., Chelliah Y., Wickramaratne A., Jarocha L., Karki N., Xu W., Takahashi J. S. Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon. PNAS. 2019. V. 116 (39). P. 19449–19457. https://doi.org/10.1073/pnas.190787511