- Physical Review Journals
All JournalsPhysics Magazine

PRX Life

Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Featured in Physics
  • Open Access

Approaching the Quantum Limit of Energy Resolution in Animal Magnetoreception

I. K. Kominis* and E. Gkoudinakis

  • Department of Physics and Institute of Theoretical and Computational Physics, University of Crete, Heraklion 70013, Greece

  • *Contact author: ikominis@uoc.gr
PDF

PRX Life 3, 013004 – Published 16 January, 2025

DOI: https://doi.org/10.1103/PRXLife.3.013004

Abstract

A large number of magnetic sensors, like superconducting quantum interference devices, optical pumping, and nitrogen vacancy magnetometers, were shown to satisfy the energy resolution limit. This limit states that the magnetic sensitivity of the sensor, when translated into a product of energy with time, is bounded below by Planck's constant, ℏ. This bound implies a fundamental limitation as to what can be achieved in magnetic sensing. Here we explore biological magnetometers, in particular three magnetoreception mechanisms thought to underly animals' geomagnetic field sensing: the radical-pair, the magnetite, and the MagR mechanism. We address the question of how close these mechanisms approach the energy resolution limit. At the quantitative level, the utility of the energy resolution limit is that it informs the workings of magnetic sensing in model-independent ways and thus can provide subtle consistency checks for theoretical models and estimated or measured parameter values, particularly needed in complex biological systems. At the qualitative level, the closer the energy resolution is to ℏ, the more “quantum” is the sensor. This offers an alternative route towards understanding the quantum biology of magnetoreception. It also quantifies the room for improvement, illuminating what nature has achieved, and stimulating the engineering of biomimetic sensors exceeding nature's magnetic sensing performance.

View figure in article

Physics Subject Headings (PhySH)

synopsis

Biological Magnetic Sensing Comes Close to Quantum Limit

Published 16 January, 2025

Researchers find that two types of biological magnetic sensor can sense fields close to the quantum limit, a finding that could guide the design of lab-made devices.

See more in Physics

Article Text

References (205)

  1. W. T. Keeton, Magnets interfere with pigeon homing, Proc. Natl. Acad. Sci. USA 68, 102 (1971).
  2. A. J. Kalmijn, Biophysics of geomagnetic field detection, IEEE Trans. Magn. 17, 1113 (1981).
  3. S. Johnsen and K. J. Lohmann, The physics and neurobiology of magnetoreception, Nat. Rev. Neurosci. 6, 703 (2005).
  4. W. Wiltschko and R. Wiltschko, Magnetic orientation and magnetoreception in birds and other animals, J. Comp. Physiol. A 191, 675 (2005).
  5. S. Johnsen and K. J. Lohmann, Magnetoreception in animals, Phys. Today 61, 29 (2008).
  6. H. Mouritsen, Long-distance navigation and magnetoreception in migratory animals, Nature (London) 558, 50 (2018).
  7. J. Xu, L. E. Jarocha, T. Zollitsch, M. Konowalczyk, K. B. Henbest, S. Richert, M. J. Golesworthy, J. Schmidt, V. Déjean, D. J. C. Sowood, M. Bassetto, J. Luo, J. R. Walton, J. Fleming, Y. Wei, T. L. Pitcher, G. Moise, M. Herrmann, H. Yin, H. Wu, R. Bartölke, S. J. Käsehagen, S. Horst, G. Dautaj, P. D. F. Murton, A. S. Gehrckens, Y. Chelliah, J. S. Takahashi, K.-W. Koch, S. Weber, I. A. Solov'yov, C. Xie, S. R. Mackenzie, C. R. Timmel, H. Mouritsen, and P. J. Hore, Magnetic sensitivity of cryptochrome 4 from a migratory songbird, Nature (London) 594, 535 (2021).
  8. M. R. Bellinger, J. Wei, U. Hartmann, H. Cadiou, M. Winklhofer, and M. A. Banks, Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing, Proc. Natl. Acad. Sci. USA 119, e2108655119 (2022).
  9. C. Xie, Searching for unity in diversity of animal magnetoreception: From biology to quantum mechanics and back, Innov. 3, 100229 (2022).
  10. K. J. Lohmann, Magnetic-field perception, Nature (London) 464, 1140 (2010).
  11. W. Wiltschko and R. Wiltschko, Magnetic orientation in birds, J. Exp. Biol. 199, 29 (1996).
  12. H. Mouritsen and T. Ritz, Magnetoreception and its use in bird navigation, Curr. Opin. Neurobiol. 15, 406 (2005).
  13. D. A. Kishkinev and N. S. Chernetsov, Magnetoreception systems in birds: A review of current research, Biol. Bull. Rev. 5, 46 (2015).
  14. R. Wiltschko, M. Ahmad, C. Nießner, D. Gehring, and W. Wiltschko, Light-dependent magnetoreception in birds: The crucial step occurs in the dark, J. R. Soc. Interface 13, 20151010 (2016).
  15. R. Wiltschko and W. Wiltschko, Magnetoreception in birds, J. R. Soc. Interface 16, 20190295 (2019).
  16. J. B. Phillips and O. Sayeed, Wavelength-dependent effects of light on magnetic compass orientation in Drosophila melanogaster, J. Comp. Physiol. A 172, 303 (1993).
  17. R. J. Gegear, A. Casselman, S. Waddell, and S. M. Reppert, Cryptochrome mediates light-dependent magnetosensitivity in Drosophila, Nature (London) 454, 1014 (2008).
  18. D. H. Dommer, P. J. Gazzolo, M. S. Painter, and J. B. Phillips, Magnetic compass orientation by larval Drosophila melanogaster, J. Insect Physiol. 54, 719 (2008).
  19. J.-E. Bae, S. Bang, S. Min, S.-H. Lee, S.-H. Kwon, Y. Lee, Y.-H. Lee, J. Chung, and K.-S. Chae, Positive geotactic behaviors induced by geomagnetic field in Drosophila, Mol. Brain 9, 55 (2016).
  20. I.-T. Oh, H.-J. Kwon, S.-C. Kim, H.-J. Kim, K. J. Lohmann, and K.-S. Chae, Behavioral evidence for geomagnetic imprinting and transgenerational inheritance in fruit flies, Proc. Natl. Acad. Sci. USA 117, 1216 (2020).
  21. A. Bradlaugh, A. L. Munro, A. R. Jones, and R. A. Baines, Exploiting the fruitfly, Drosophila melanogaster, to identify the molecular basis of cryptochrome-dependent magnetosensitivity, Quantum Rep. 3, 127 (2021).
  22. A. A. Bradlaugh, G. Fedele, A. L. Munro, C. N. Hansen, J. M. Hares, S. Patel, C. P. Kyriacou, A. R. Jones, E. Rosato, and R. A. Baines, Essential elements of radical pair magnetosensitivity in Drosophila, Nature (London) 615, 111 (2023).
  23. M. Bassetto, T. Reichl, D. Kobylkov, D. R. Kattnig, M. Winklhofer, P. J. Hore, and H. Mouritsen, No evidence for magnetic field effects on the behaviour of Drosophila, Nature (London) 620, 595 (2023).
  24. S. M. Reppert, Magnetic field effects on behaviour in Drosophila, Nature (London) 629, E1 (2024).
  25. S. M. Reppert, R. J. Gegear, and C. Merlin, Navigational mechanisms of migrating monarch butterflies, Trends Neurosci. 33, 399 (2010).
  26. P. A. Guerra, R. J. Gegear, and S. M. Reppert, A magnetic compass aids monarch butterfly migration, Nat. Commun. 5, 4164 (2014).
  27. G. Wan, A. N. Hayden, S. E. Iiams, and C. Merlin, Cryptochrome 1 mediates light-dependent inclination magnetosensing in monarch butterflies, Nat. Commun. 12, 771 (2021).
  28. V. Courtillotl, G. Hulot, M. Alexandrescu, J.-L. le Mouë, and J. L. Kirschvink, Sensitivity and evolution of sea-turtle magnetoreception: Observations, modelling and constraints from geomagnetic secular variation, Terra Nova 9, 203 (1997).
  29. K. J. Lohmann, Sea turtles: Navigating with magnetism, Curr. Biol. 17, R102 (2007).
  30. W. P. Irwin and K. J. Lohmann, Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields, J. Comp. Physiol. A 191, 475 (2005).
  31. J. M. Anderson, T. M. Clegg, L. V. M. V. Q. Véras, and K. N. Holland, Insight into shark magnetic field perception from empirical observations, Sci. Rep. 7, 11042 (2017).
  32. B. A. Keller, N. F. Putman, R. D. Grubbs, D. S. Portnoy, and T. P. Murphy, Map-like use of Earth's magnetic field in sharks, Curr. Biol. 31, 2881 (2021).
  33. C. G. Meyer, K. N. Holland, and Y. P. Papastamatiou, Sharks can detect changes in the geomagnetic field, J. R. Soc. Interface 2, 129 (2005).
  34. T. Nishi, G. Kawamura, and K. Matsumoto, Magnetic sense in the Japanese eel, Anguilla japonica, as determined by conditioning and electrocardiography, J. Exp. Biol. 207, 2965 (2004).
  35. C. M. F. Durif, H. I. Browman, J. B. Phillips, A. B. Skiftesvik, L. A. Vøllestad, and H. H. Stockhausen, Magnetic compass orientation in the European eel, PLoS ONE 8, e59212 (2013).
  36. A. Cresci, C. B. Paris, C. M. F. Durif, S. Shema, R. M. Bjelland, A. B. Skiftesvik, and H. I. Browman, Glass eels (Anguilla anguilla) have a magnetic compass linked to the tidal cycle, Sci. Adv. 3, e1602007 (2017).
  37. M. Baltazar-Soares and C. Eizaguirre, Animal navigation: The eel's magnetic guide to the Gulf stream, Curr. Biol. 27, R604 (2017).
  38. A. Cresci, C. M. Durif, C. B. Paris, S. D. Shema, A. B. Skiftesvik, and H. I. Browman, Glass eels (Anguilla anguilla) imprint the magnetic direction of tidal currents from their juvenile estuaries, Commun. Biol. 2, 366 (2019).
  39. T. P. Quinn, Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry, J. Comp. Physiol. 137, 243 (1980).
  40. N. F. Putman, Inherited magnetic maps in salmon and the role of geomagnetic change, Integr. Comp. Biol. 55, 396 (2015).
  41. L. C. Naisbett-Jones, N. F. Putman, M. M. Scanlan, D. L. G. Noakes, and K. J. Lohmann, Magnetoreception in fishes: The effect of magnetic pulses on orientation of juvenile Pacific salmon, J. Exp. Biol. 223, jeb222091 (2020).
  42. K. Schulten, C. E. Swenberg, and A. Weller, A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion, Z. Phys. Chem. 111, 1 (1978).
  43. C. B. Grissom, Magnetic field effects in biology: A survey of possible mechanisms with emphasis on radical-pair recombination, Chem. Rev. 95, 3 (1995).
  44. T. Ritz, S. Adem, and K. Schulten, A model for photoreceptor-based magnetoreception in birds, Biophys. J. 78, 707 (2000).
  45. P. J. Hore and H. Mouritsen, The radical-pair mechanism of magnetoreception, Annu. Rev. Biophys. 45, 299 (2016).
  46. H. G. Hiscock, S. Worster, D. R. Kattnig, C. Steers, Y. Jin, D. E. Manolopoulos, H. Mouritsen, and P. J. Hore, The quantum needle of the avian magnetic compass, Proc. Natl. Acad. Sci. USA 113, 4634 (2016).
  47. S. Mann, N. H. C. Sparks, M. M. Walker, and J. L. Kirschvink, Ultrastructure, morphology and organization of biogenic magnetite from sockeye salmon, Oncorhynchus nerka: Implications for magnetoreception, J. Exp. Biol. 140, 35 (1988).
  48. J. L. Kirschvink, M. M. Walker, and C. E. Diebel, Magnetite-based magnetoreception, Curr. Op. Neurobiol. 11, 462 (2001).
  49. M. Winklhofer, Magnetite-based magnetoreception in higher organisms, in Magnetoreception and Magnetosomes in Bacteria, Microbiology Monographs, edited by D. Schüler (Springer-Verlag, Berlin, 2006).
  50. G. Fleissner, B. Stahl, P. Thalau, G. Falkenberg, and G. Fleissner, A novel concept of Fe-mineral-based magnetoreception: Histological and physicochemical data from the upper beak of homing pigeons, Naturwissenschaften 94, 631 (2007).
  51. H. Cadiou and P. A. McNaughton, Avian magnetite-based magnetoreception: A physiologist's perspective, J. R. Soc. Interface 7, S193 (2010).
  52. A. J. Kalmijn, Electric and magnetic field detection in elasmobranch fishes, Science 218, 916 (1982).
  53. B. Rosenblum, R. L. Jungerman, and L. Longfellow, Limits to induction-based magnetoreception, in Magnetite Biomineralization and Magnetoreception in Organisms, edited by J. L. Kirschvink, D. S. Jones, and B. J. MacFadden (Springer, Boston, 1985).
  54. T. C. A. Molteno and W. L. Kennedy, Navigation by induction-based magnetoreception in elasmobranch fishes, J. Biophys. 2009, 380976 (2009).
  55. S. Nimpf, G. C. Nordmann, D. Kagerbauer, E. P. Malkemper, L. Landler, A. Papadaki-Anastasopoulou, L. Ushakova, A. Wenninger-Weinzierl, M. Novatchkova, P. Vincent, T. Lendl, M. Colombini, M. J. Mason, and D. A. Keays, A putative mechanism for magnetoreception by electromagnetic induction in the pigeon inner ear, Curr. Biol. 29, 4052 (2019).
  56. S. Qin, H. Yin, C. Yang, Y. Dou, Z. Liu, P. Zhang, H. Yu, Y. Huang, J. Feng, J. Hao, J. Hao, L. Deng, X. Yan, X. Dong, Z. Zhao, T. Jiang, H.-W. Wang, S.-J. Luo, and C. Xie, A magnetic protein biocompass Nat. Mater. 15, 217 (2016).
  57. D. I. Gordon and R. E. Brown, Recent advances in fluxgate magnetometry, IEEE Trans. Magn. 8, 76 (1972).
  58. P. Ripka, Review of fluxgate sensors, Sens. Actuat. A: Phys. 33, 129 (1992).
  59. P. Ripka and M. Janošek, Advances in magnetic field sensors, IEEE Sensors J. 10, 1108 (2010).
  60. J. P. Dowling and G. J. Milburn, Quantum technology: The second quantum revolution, Phil. Trans. R. Soc. A 361, 1655 (2003).
  61. I. H. Deutsch, Harnessing the power of the second quantum revolution, PRX Quantum 1, 020101 (2020).
  62. C. L. Degen, F. Reinhard, and P. Cappellaro, Quantum sensing, Rev. Mod. Phys. 89, 035002 (2017).
  63. J. Clarke, SQUID fundamentals, in SQUlD Sensors: Fundamentals, Fabrication and Applications, edited by W. H. Dordrecht (Kluwer Academic Press, Amsterdam, 1996)
  64. R. L. Fagaly, SQUID instruments and applications, Rev. Sci. Instr. 77, 101101 (2006).
  65. M. Schmelz, V. Zakosarenko, T. Schönau, S. Anders, S. Linzen, R. Stolz, and H.-G. Meyer, Nearly quantum limited nanoSQUIDs based on cross-type Nb/AlOx/Nb junctions, Supercond. Sci. Technol. 30, 014001 (2017).
  66. I. K. Kominis, T. W. Kornack, J. C. Allred, and M. V. Romalis, A subfemtotesla multichannel atomic magnetometer, Nature (London) 422, 596 (2003).
  67. A. Fabricant, I. Novikova, and G. Bison, How to build a magnetometer with thermal atomic vapor: A tutorial, New J. Phys. 25, 025001 (2023).
  68. G. Balasubramanian, I. Y. Chan, R. Kolesov, M. Al-Hmoud, J. Tisler, C. Shin, C. Kim, A. Wojcik, P. R. Hemmer, A. Krueger, T. Hanke, A. Leitenstorfer, R. Bratschitsch, F. Jelezko, and J. Wrachtrup, Nanoscale imaging magnetometry with diamond spins under ambient conditions, Nature (London) 455, 648 (2008).
  69. J. M. Taylor, P. Cappellaro, L. Childress, L. Jiang, D. Budker, P. R. Hemmer, A. Yacoby, R. Walsworth, and M. D. Lukin, High-sensitivity diamond magnetometer with nanoscale resolution, Nat. Phys. 4, 810 (2008).
  70. H. Zheng, Z. Sun, G. Chatzidrosos, C. Zhang, K. Nakamura, H. Sumiya, T. Ohshima, J. Isoya, J. Wrachtrup, A. Wickenbrock, and D. Budker, Microwave-free vector magnetometry with nitrogen-vacancy centers along a single axis in diamond, Phys. Rev. Appl. 13, 044023 (2020).
  71. M. Vengalattore, J. M. Higbie, S. R. Leslie, J. Guzman, L. E. Sadler, and D. M. Stamper-Kurn, High-resolution magnetometry with a spinor Bose-Einstein condensate, Phys. Rev. Lett. 98, 200801 (2007).
  72. P. Gomez, F. Martin, C. Mazzinghi, D. Benedicto Orenes, S. Palacios, and M. W. Mitchell, Bose-Einstein condensate comagnetometer, Phys. Rev. Lett. 124, 170401 (2020).
  73. K. Gietka, F. Mivehvar, and T. Busch, Cavity-enhanced magnetometer with a spinor Bose-Einstein condensate, New J. Phys. 23, 043020 (2021).
  74. M. Hämäläinen, R. Hari, R. J. Ilmoniemi, J. Knuutila, and O. V. Lounasmaa, Magnetoencephalography—Theory, instrumentation, and applications to noninvasive studies of the working human brain, Rev. Mod. Phys. 65, 413 (1993).
  75. H. Xia, A. B.-A. Baranga, D. Hoffman, and M. V. Romalis, Magnetoencephalography with an atomic magnetometer, Appl. Phys. Lett. 89, 211104 (2006).
  76. E. J. Pratt, M. Ledbetter, R. Jiménez-Martínez, B. Shapiro, A. Solon, G. Z. Iwata, S. Garber, J. Gormley, D. Decker, D. Delgadillo, A. T. Dellis, J. Phillips, G. Sundar, J. Leung, J. Coyne, M. McKinley, G. Lopez, S. Homan, L. Marsh, M. Zhang, V. Maurice, B. Siepser, T. Giovannoli, B. Leverett, G. Lerner, S. Seidman, V. DeLuna, K. Wright-Freeman, J. Kates-Harbeck, T. Lasser, H. Mohseni, T. J. Sharp, A. Zorzos, A. H. Lara, A. Kouhzadi, A. Ojeda, P. Chopra, Z. Bednarke, M. Henninger, and J. K. Alford, Kernel Flux: A whole-head 432-magnetometer optically-pumped magnetoencephalography (OP-MEG) system for brain activity imaging during natural human experiences, Proc. SPIE 11700, 1170032 (2021).
  77. T. M. Tierney, N. Holmes, S. Mellor, J. D. López, G. Roberts, R. M. Hill, E. Boto, J. Leggett, V. Shah, M. J. Brookes, R. Bowtell, and G. R. Barnes, Optically pumped magnetometers: From quantum origins to multi-channel magnetoencephalography, NeuroImage 199, 598 (2019).
  78. R. Zhang, W. Xiao, Y. Ding, Y. Feng, X. Peng, L. Shen, C. Sun, T. Wu, Y. Wu, Y. Yang, Z. Zheng, X. Zhang, J. Chen, and H. Guo, Recording brain activities in unshielded Earth's field with optically pumped atomic magnetometers, Sci. Adv. 6, eaba8792 (2020).
  79. G. Bison, R. Wynands, and A. Weis, A laser-pumped magnetometer for the mapping of human cardiomagnetic fields, Appl. Phys. B 76, 325 (2003).
  80. Y. J. Kim, I. Savukov, and S. Newman, Magnetocardiography with a 16-channel fiber-coupled single-cell Rb optically pumped magnetometer, Appl. Phys. Lett. 114, 143702 (2019).
  81. M. V. Romalis and H. B. Dang, Atomic magnetometers for materials characterization, Mater. Today 14, 258 (2011).
  82. F. Fabre, A. Finco, A. Purbawati, A. Hadj-Azzem, N. Rougemaille, J. Coraux, I. Philip, and V. Jacques, Characterization of room-temperature in-plane magnetization in thin flakes of CrTe2 with a single-spin magnetometer, Phys. Rev. Mater. 5, 034008 (2021).
  83. N. Aslam, H. Zhou, E. K. Urbach, M. J. Turner, R. L. Walsworth, M. D. Lukin, and H. Park, Quantum sensors for biomedical applications, Nat. Rev. Phys. 5, 157 (2023).
  84. B. Bao, Y. Hua, R. Wang, and D. Li, Quantum-based magnetic field sensors for biosensing, Adv. Quantum Technol. 6, 2200146 (2023).
  85. M. W. Mitchell and S. Palacios Alvarez, Colloquium: Quantum limits to the energy resolution of magnetic field sensors, Rev. Mod. Phys. 92, 021001 (2020).
  86. M. Meister, Physical limits to magnetogenetics, eLife 5, e17210 (2016).
  87. S. F. Huelga and M. B. Plenio, Vibrations, quanta and biology, Contemp. Phys. 54, 181 (2013).
  88. I. K. Kominis, Quantum Zeno effect explains magnetic-sensitive radical-ion-pair reactions, Phys. Rev. E 80, 056115 (2009).
  89. J. Cai, G. G. Guerreschi, and H. J. Briegel, Quantum control and entanglement in a chemical compass, Phys. Rev. Lett. 104, 220502 (2010).
  90. I. K. Kominis, Magnetic sensitivity and entanglement dynamics of the chemical compass, Chem. Phys. Lett. 542, 143 (2012).
  91. C. Y. Cai, Q. Ai, H. T. Quan, and C. P. Sun, Sensitive chemical compass assisted by quantum criticality, Phys. Rev. A 85, 022315 (2012).
  92. J. Cai and M. B. Plenio, Chemical compass model for avian magnetoreception as a quantum coherent device, Phys. Rev. Lett. 111, 230503 (2013).
  93. Y. Zhang, G. P. Berman, and S. Kais, Sensitivity and entanglement in the avian chemical compass, Phys. Rev. E 90, 042707 (2014).
  94. V. S. Poonia, K. Kondabagil, D. Saha, and S. Ganguly, Functional window of the avian compass, Phys. Rev. E 95, 052417 (2017).
  95. K. M. Vitalis and I. K. Kominis, Quantum-limited biochemical magnetometers designed using the Fisher information and quantum reaction control, Phys. Rev. A 95, 032129 (2017).
  96. M. Tolunay, I. Liepuoniute, M. Vyushkova, and B. A. Jones, Hamiltonian simulation of quantum beats in radical pairs undergoing thermal relaxation on near-term quantum computers, Phys. Chem. Chem. Phys. 25, 15115 (2023).
  97. A. Streltsov, G. Adesso, and M. B. Plenio, Colloquium: Quantum coherence as a resource, Rev. Mod. Phys. 89, 041003 (2017).
  98. M. B. Plenio and S. Virmani, An introduction to entanglement measures, Quant. Inf. Comput. 7, 1 (2007).
  99. I. K. Kominis, Quantum relative entropy shows singlet-triplet coherence is a resource in the radical-pair mechanism of biological magnetic sensing, Phys. Rev. Res. 2, 023206 (2020).
  100. I. K. Kominis, Physiological search for quantum biological sensing effects based on the Wigner-Yanase connection between coherence and uncertainty, Adv. Quantum Technol. 2300292 (2023).
  101. G. Hou, D. Wang, K. Xiao, H. Zhang, S. Zheng, P. Li, Y. Tian, and L. Jiang, Magnetic gated biomimetic artificial nanochannels for controllable ion transportation inspired by homing pigeon, Small 14, 1703369 (2018).
  102. Y. H. Jung, B. Park, J. U. Kim, and T.-I. Kim, Bioinspired electronics for artificial sensory systems, Adv. Mater. 31, 1803637 (2019).
  103. L. Xue, T. Hu, Z. Guo, C. Yang, Z. Wang, S. Qin, P. Yang, C. Xie, J. Xu, N. Li, Y. Shen, H. Jiang, D. Deng, N. Gu, and J. Sun, A novel biomimetic magnetosensor based on magneto-optically involved conformational variation of MagR/Cry4 complex, Adv. Electron. Mater. 6, 1901168 (2020).
  104. I. K. Kominis, Quantum thermodynamic derivation of the energy resolution limit in magnetometry, Phys. Rev. Lett. 133, 263201 (2024).
  105. A. Vinante, C. Timberlake, D. Budker, Derek F. Jackson Kimball, A. O. Sushkov, and H. Ulbricht, Surpassing the energy resolution limit with ferromagnetic torque sensors, Phys. Rev. Lett. 127, 070801 (2021).
  106. S. Palacios Alvarez, P. Gomez, S. Coop, R. Zamora-Zamora, C. Mazzinghi, and M. W. Mitchell, Single-domain Bose condensate magnetometer achieves energy resolution per bandwidth below ℏ, Proc. Natl. Acad. Sci. USA 119, e2115339119 (2022).
  107. F. Ahrens, W. Ji, D. Budker, C. Timberlake, H. Ulbricht, and A. Vinante, Levitated ferromagnetic magnetometer with energy resolution well below ℏ, arXiv:2401.03774.
  108. I. K. Kominis, The radical-pair mechanism as a paradigm for the emerging science of quantum biology, Mod. Phys. Lett. B 29, 1530013 (2015).
  109. R. E. Blankenship, T. J. Schaafsma, and W. W. Parson, Magnetic field effects on radical pair intermediates in bacterial photosynthesis, Biochim. Biophys. Acta 461, 297 (1977).
  110. U. E. Steiner and T. Ulrich, Magnetic field effects in chemical kinetics and related phenomena, Chem. Rev. 89, 51 (1989).
  111. C. R. Timmel, U. Till, B. Brocklehurst, K. A. Mclauchlan, and P. J. Hore, Effects of weak magnetic fields on free radical recombination reactions, Mol. Phys. 95, 71 (1998).
  112. A. M. Lewis, T. P. Fay, D. E. Manolopoulos, C. Kerpal, S. Richert, and C. R. Timmel, On the low magnetic field effect in radical pair reactions, J. Chem. Phys. 149, 034103 (2018).
  113. S. Y. Wong, P. Benjamin, and P. J. Hore, Magnetic field effects on radical pair reactions: Estimation of B1/2 for flavin-tryptophan radical pairs in cryptochromes, Phys. Chem. Chem. Phys. 25, 975 (2023).
  114. T. Ritz, R. Wiltschko, P. J. Hore, C. T. Rodgers, K. Stapput, P. Thalau, C. R. Timmel, and W. Wiltschko, Magnetic compass of birds is based on a molecule with optimal directional sensitivity, Biophys. J. 96, 3451 (2009).
  115. G. E. Katsoprinakis, A. T. Dellis, and I. K. Kominis, Coherent triplet excitation suppresses the heading error of the avian compass, New J. Phys. 12, 085016 (2010).
  116. J. C. S. Lau, C. T. Rodgers, and P. J. Hore, Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes, J. R. Soc. Interface 9, 3329 (2012).
  117. Y. Zhang, Z. Hu, Y. Wang, and S. Kais, Quantum simulation of the radical pair dynamics of the avian compass, J. Phys. Chem. Lett. 14, 832 (2023).
  118. T. Ritz, P. Thalau, J. B. Phillips, R. Wiltschko, and W. Wiltschko, Resonance effects indicate a radical-pair mechanism for avian magnetic compass, Nature (London) 429, 177 (2004).
  119. N. Keary, T. Ruploh, J. Voss, P. Thalau, R. Wiltschko, W. Wiltschko, and H.-J. Bischof, Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata, Front. Zool. 6, 25 (2009).
  120. S. Engels, N.-L. Schneider, N. Lefeldt, C. M. Hein, M. Zapka, A. Michalik, D. Elbers, A. Kittel, P. J. Hore, and H. Mouritsen, Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird, Nature (London) 509, 353 (2014).
  121. B. Leberecht, D. Kobylkov, T. Karwinkel, S. Döge, L. Burnus, S. Y. Wong, S. Apte, K. Haase, I. Musielak, R. Chetverikova, G. Dautaj, M. Bassetto, M. Winklhofer, P. J. Hore, and H. Mouritsen, Broadband 75-85 MHz radiofrequency fields disrupt magnetic compass orientation in night-migratory songbirds consistent with a flavin-based radical pair magnetoreceptor, J. Compar. Physiol. A 208, 97 (2022).
  122. C. L. Thompson, C. Bowes Rickman, S. J. Shaw, J. N. Ebright, U. Kelly, A. Sancar, and D. W. Rickman, Expression of the blue-light receptor cryptochrome in the human retina, Invest. Ophthalmol. Vis. Sci. 44, 4515 (2003).
  123. D. Heyers, M. Manns, H. Luksch, O. Güntürkün, and H. Mouritsen, A visual pathway links brain structures active during magnetic compass orientation in migratory birds, PLoS ONE 2, e937 (2007).
  124. C. Nießner, S. Denzau, E. P. Malkemper, J. C. Gross, H. Burda, M. Winklhofer, and L. Peichl, Cryptochrome 1 in retinal cone photoreceptors suggests a novel functional role in mammals, Sci. Rep. 6, 21848 (2016).
  125. H. Mouritsen, U. Janssen-Bienhold, M. Liedvogel, G. Feenders, J. Stalleicken, P. Dirks, and R. Weiler, Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation, Proc. Natl. Acad. Sci. USA 101, 14294 (2004).
  126. J. C. Weaver, T. E. Vaughan, and R. D. Astumian, Biological sensing of small field differences by magnetically sensitive chemical reactions, Nature (London) 405, 707 (2000).
  127. K. Maeda, K. B. Henbest, F. Cintolesi, I. Kuprov, C. T. Rodgers, P. A. Liddell, D. Gust, C. R. Timmel, and P. J. Hore, Chemical compass model of avian magnetoreception, Nature (London) 453, 387 (2008).
  128. C. Kerpal, S. Richert, J. G. Storey, S. Pillai, P. A. Liddell, D. Gust, S. R. Mackenzie, P. J. Hore, and C. R. Timmel, Chemical compass behaviour at microtesla magnetic fields strengthens the radical pair hypothesis of avian magnetoreception, Nat. Commun. 10, 3707 (2019).
  129. D. Budker and M. V. Romalis, Optical magnetometry, Nat. Phys. 3, 227 (2007).
  130. S. G. Boxer, C. E. D. Chidsey, and M. G. Roelofs, Anisotropic magnetic interactions in the primary radical ion-pair of photosynthetic reaction centers, Proc. Natl. Acad. Sci. USA 79, 4632 (1982).
  131. F. Cintolesi, T. Ritz, C. W. M. Kay, C. R. Timmel, and P. J. Hore, Anisotropic recombination of an immobilized photoinduced radical pair in a 50−μT magnetic field: A model avian photomagnetoreceptor, Chem. Phys. 294, 385 (2003).
  132. J. Luo, On the anisotropic weak magnetic field effect in radical-pair reactions, J. Chem. Phys. 158, 234302 (2023).
  133. Y. Ren, H. G. Hiscock, and P. J. Hore, Angular precision of radical pair compass magnetoreceptors, Biophys. J. 120, 547 (2021).
  134. A. V. Komolkin, P. Kupriyanov, A. Chudin, J. Bojarinova, K. Kavokin, and N. Chernetsov, Theoretically possible spatial accuracy of geomagnetic maps used by migrating animals, J. R. Soc. Interface 14, 20161002 (2017).
  135. K. J. Lohmann, K. M. Goforth, A. G. Mackiewicz, D. S. Lim, and C. M. F. Lohmann, Magnetic maps in animal navigation, J. Comp. Physiol. A 208, 41 (2022).
  136. P. Semm and R. C. Beason, Responses to small magnetic variations by the trigeminal system of the bobolink, Brain Res. Bull. 25, 735 (1990).
  137. K. J. Lohmann, N. F. Putman, S. Johnsen, and C. M. F. Lohmann, Animal magnetic sensitivity and magnetic displacement experiments, Commun. Biol. 7, 650 (2024).
  138. I. A. Solov'yov, T. Domratcheva, A. R. M. Shahi, and K. Schulten, Decrypting cryptochrome: Revealing the molecular identity of the photoactivation reaction, J. Am. Chem. Soc. 134, 18046 (2012).
  139. K. Maeda, A. J. Robinson, K. B. Henbest, H. J. Hogben, T. Biskup, M. Ahmad, E. Schleicher, S. Weber, C. R. Timmel, and P. J. Hore, Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor, Proc. Natl. Acad. Sci. USA 109, 4774 (2012).
  140. I. A. Solov'yov, T. Domratcheva, and K. Schulten, Separation of photo-induced radical pair in cryptochrome to a functionally critical distance, Sci. Rep. 4, 3845 (2014).
  141. D. Nohr, S. Franz, R. Rodriguez, B. Paulus, L.-O. Essen, S. Weber, and E. Schleicher, Extended electron-transfer in animal cryptochromes mediated by a tetrad of aromatic amino acids, Biophys. J. 111, 301 (2016).
  142. A. K. Michael, J. L. Fribourgh, R. N. Van Gelder, and C. L. Partch, Animal cryptochromes: Divergent roles in light perception, circadian timekeeping and beyond, Photochem. Photobiol. 93, 128 (2017).
  143. D. R. Kattnig, C. Nielsen, and I. A. Solov'yov, Molecular dynamics simulations disclose early stages of the photoactivation of cryptochrome 4, New J. Phys. 20, 083018 (2018).
  144. B. D. Zoltowski, Y. Chelliah, A. Wickramaratne, L. Jarocha, N. Karki, W. Xu, H. Mouritsen, P. J. Hore, R. E. Hibbs, C. B. Green, and J. S. Takahashi, Chemical and structural analysis of a photoactive vertebrate cryptochrome from pigeon, Proc. Natl. Acad. Sci. USA 116, 19449 (2019).
  145. T. Hochstoeger, T. Al Said, D. Maestre, F. Walter, A. Vilceanu, M. Pedron, T. D. Cushion, W. Snider, S. Nimpf, G. C. Nordmann, L. Landler, N. Edelman, L. Kruppa, G. Dürnberger, K. Mechtler, S. Schuechner, E. Ogris, E. P. Malkemper, S. Weber, E. Schleicher, and D. A. Keays, The biophysical, molecular, and anatomical landscape of pigeon CRY4: A candidate light-based quantal magnetosensor, Sci. Adv. 6, eabb9110 (2020).
  146. G. C. G. Parico and C. L. Partch, The tail of cryptochromes: An intrinsically disordered cog within the mammalian circadian clock, Cell Commun. Signal. 18, 182 (2020).
  147. S. Y. Wong, Y. Wei, H. Mouritsen, I. A. Solov'yov, and P. J. Hore, Cryptochrome magnetoreception: four tryptophans could be better than three, J. R. Soc. Interface 18, 20210601 (2021).
  148. S. Chandrasekaran, C. M. Schneps, R. Dunleavy, C. Lin, C. C. DeOliveira, A. Ganguly, and B. R. Crane, Tuning flavin environment to detect and control light-induced conformational switching in Drosophila cryptochrome, Commun. Biol. 4, 249 (2021).
  149. A. Frederiksen, M. Aldag, I. A. Solov'yov, and L. Gerhards, Activation of cryptochrome 4 from Atlantic herring, Biology 13, 262 (2024).
  150. J. Deviers, F. Cailliez, A. de la Lande, and D. R. Kattnig, Avian cryptochrome 4 binds superoxide, Comput. Struct. Biotechnol. J. 26, 11 (2024).
  151. F. Schuhmann, J. L. Ramsay, D. R. Kattnig, and I. A. Solov'yov, Structural rearrangements of pigeon cryptochrome 4 undergoing a complete redox cycle, J. Phys. Chem. B 128, 3844 (2024).
  152. H. Wu, A. Scholten, A. Einwich, H. Mouritsen, and K.-W. Koch, Protein-protein interaction of the putative magnetoreceptor cryptochrome 4 expressed in the avian retina, Sci. Rep. 10, 7364 (2020).
  153. A. Günther, A. Einwich, E. Sjulstok, R. Feederle, P. Bolte, K.-W. Koch, I. A. Solov'yov, and H. Mouritsen, Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4, Curr. Biol. 28, 211 (2018).
  154. A. Pinzon-Rodriguez, S. Bensch, and R. Muheim, Expression patterns of cryptochrome genes in avian retina suggest involvement of Cry4 in light-dependent magnetoreception, J. R. Soc. Interface 15, 20180058 (2018).
  155. T. Biskup, E. Schleicher, A. Okafuji, G. Link, K. Hitomi, E. D. Getzoff, and S. Weber, Direct observation of a photoinduced radical-pair intermediate in a cryptochrome blue-light photoreceptor, Angew. Chem. Int. Ed. 48, 404 (2009).
  156. D. R. Kattnig, I. A. Solov'yov, and P. J. Hore, Electron spin relaxation in cryptochrome-based magnetoreception, Phys. Chem. Chem. Phys. 18, 12443 (2016).
  157. T. P. Fay, L. P. Lindoy, D. E. Manolopoulos, and P. J. Hore, How quantum is radical pair magnetoreception?, Faraday Discuss. 221, 77 (2020).
  158. S. Worster, D. R. Kattnig, and P. J. Hore, Spin relaxation of radicals in cryptochrome and its role in avian magnetoreception, J. Chem. Phys. 145, 035104 (2016).
  159. R. H. Masland, The neuronal organization of the retina, Neuron 76, 266 (2012).
  160. O. Efimova and P. J. Hore, Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass, Biophys. J. 94, 1565 (2008).
  161. Z. B. Walters, Quantum dynamics of the avian compass, Phys. Rev. E 90, 042710 (2014).
  162. R. P. Blakemore, Magnetotactic bacteria, Annu. Rev. Microbiol. 36, 217 (1982).
  163. H. A. Lowenstam, Minerals formed by organisms, Science 211, 1126 (1981).
  164. D. Faivre and D. Schüler, Magnetotactic bacteria and magnetosomes, Chem. Rev. 108, 4875 (2008).
  165. W. Lin, J. L. Kirschvink, G. A. Paterson, D. A. Bazylinski, and Y. Pan, On the origin of microbial magnetoreception, Natl. Sci. Rev. 7, 472 (2020).
  166. C. L. Monteil and C. T. Lefevre, Magnetoreception in microorganisms, Trends Microbiol. 28, 266 (2020).
  167. J. L. Gould, J. L. Kirschvink, and K. S. Deffeyes, Bees have magnetic remanence, Science 201, 1026 (1978).
  168. C.-H. Liang, C.-L. Chuang, J.-A. Jiang, and E.-C. Yang, Magnetic sensing through the abdomen of the honey bee, Sci. Rep. 6, 23657 (2016).
  169. S. H. K. Eder, H. Cadiou, A. Muhamad, P. A. McNaughton, J. L. Kirschvink, and M. Winklhofer, Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells, Proc. Natl. Acad. Sci. USA 109, 12022 (2012).
  170. C. E. Diebel, R. Proksch, C. R. Green, P. Neilson, and M. M. Walker, Magnetite defines a vertebrate magnetoreceptor, Nature (London) 406, 299 (2000).
  171. M. M. Walker, C. E. Diebel, C. V. Haugh, P. M. Pankhurst, J. C. Montgomery, and C. R. Green, Structure and function of the vertebrate magnetic sense, Nature (London) 390, 371 (1997).
  172. R. C. Beason and W. J. Brennan, Natural and induced magnetization in the bobolink, Dolichonyx oryzivorus, J. Exp. Biol. 125, 49 (1986).
  173. J. L. Kirschvink and J. L. Gould, Biogenic magnetite as a basis for magnetic field detection in animals, Biosystems 13, 181 (1981).
  174. J. L. Kirschvink, Magnetite biomineralization and geomagnetic sensitivity in higher animals: An update and recommendations for future study, Bioelectromagnetics 10, 239 (1989).
  175. S. Begall, H. Burda, and E. P. Malkemper, Magnetoreception in mammals, Adv. Stud. Behav. 46, 45 (2014).
  176. M. Hanzlik, C. Heunemann, E. Holtkamp-Rötzler, M. Winklhofer, N. Petersen, and G. Fleissner, Superparamagnetic magnetite in the upper beak tissue of homing pigeons, Biometals 13, 325 (2000).
  177. G. Falkenberg, G. Fleissner, K. Schuchardt, M. Kuehbacher, P. Thalau, H. Mouritsen, D. Heyers, G. Wellenreuther, and G. Fleissner, Avian magnetoreception: Elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds, PLoS ONE 5, e9231 (2010).
  178. D. Heyers, M. Zapka, M. Hoffmeister, J. M. Wild, and H. Mouritsen, Magnetic field changes activate the trigeminal brainstem complex in a migratory bird, Proc. Natl. Acad. Sci. USA 107, 9394 (2010).
  179. R. Wiltschko and W. Wiltschko, The magnetite-based receptors in the beak of birds and their role in avian navigation, J. Comp. Physiol. A 199, 89 (2013).
  180. V. P. Shcherbakov and M. Winklhofer, The osmotic magnetometer: A new model for magnetite-based magnetoreceptors in animals, Eur. Biophys. J. 28, 380 (1999).
  181. G. Fleissner, G. Fleissner, B. Stahl, and G. Falkenberg, Iron-mineral-based magnetoreception in birds: The stimulus conducting system, J. Ornithol. 148, 643 (2007).
  182. I. A. Solov'yov and W. Greiner, Theoretical analysis of an iron mineral-based magnetoreceptor model in birds, Biophys. J. 93, 1493 (2007).
  183. M. Winklhofer and J. L. Kirschvink, A quantitative assessment of torque-transducer models for magnetoreception, J. R. Soc. Interface 7, S273 (2010).
  184. A. F. Davila, G. Fleissner, M. Winklhofer, and N. Petersen, A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite, Phys. Chem. Earth 28, 647 (2003).
  185. M. Torbati, K. Mozaffari, L. Liu, and P. Sharma, Coupling of mechanical deformation and electromagnetic fields in biological cells, Rev. Mod. Phys. 94, 025003 (2022).
  186. D. T. Grob, N. Wise, O. Oduwole, and S. Sheard, Magnetic susceptibility characterisation of superparamagnetic microspheres, J. Magn. Magn. Mater. 452, 134 (2018).
  187. J. Ashmore, Cochlear outer hair cell motility, Physiol. Rev. 88, 173 (2008).
  188. P. S. Langan, V. G. Vandavasi, W. Kopec, B. Sullivan, P. V. Afonne, K. L. Weiss, B. L. de Groot, and L. Coates, The structure of a potassium-selective ion channel reveals a hydrophobic gate regulating ion permeation, IUCrJ 7, 835 (2020).
  189. V. Puerto-Belda, J. J. Ruz, C. Millá, A. Cano, M. L. Yubero, S. García, P. M. Kosaka, M. Calleja, and J. Tamayo, Measuring vibrational modes in living human cells, PRX Life 2, 013003 (2024).
  190. P. Jandačka, P. Alexa, J. Pištora, and J. Trojková, Hypothetical superparamagnetic magnetometer in a pigeon's upper beak probably does not work, Eur. Phys. J. E 36, 40 (2013).
  191. F. Curdt, K. Haase, L. Ziegenbalg, H. Greb, D. Heyers, and M. Winklhofer, Prussian blue technique is prone to yield false negative results in magnetoreception research, Sci. Rep. 12, 8803 (2022).
  192. Z. Guo, S. Xu, X. Chen, C. Wang, P. Yang, S. Qin, C. Zhao, F. Fei, X. Zhao, P.-H. Tan, J. Wang, and C. Xie, Modulation of MagR magnetic properties via iron-sulfur cluster binding, Sci. Rep. 11, 23941 (2021).
  193. T. Tong, Y. Zhou, F. Fei, X. Zhou, Z. Guo, S. Wang, J. Zhang, P. Zhang, T. Cai, G. Li, Y. Zhang, J. Wang, and C. Xie, The rational design of iron-sulfur cluster binding site for prolonged stability in magnetoreceptor MagR, Front. Mol. Biosci. 9, 1051943 (2022).
  194. P. Yang, T. Cai, L. Zhang, D. Yu, Z. Guo, Y. Zhang, G. Li, X. Zhang, and C. Xie, A rationally designed building block of the putative magnetoreceptor MagR, Bioelectromagnetics 43, 317 (2022).
  195. Y. Zhou, T. Tong, M. Wei, P. Zhang, F. Fei, X. Zhou, Z. Guo, J. Zhang, H. Xu, L. Zhang, S. Wang, J. Wang, T. Cai, X. Zhang, and C. Xie, Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically, Zool. Res. 44, 142 (2023).
  196. J. Zhang, Y. Chang, P. Zhang, Y. Zhang, M. Wei, C. Han, S. Wang, H.-M. Lu, T. Cai, and C. Xie, On the evolutionary trail of MagRs, Zool. Res. 45, 821 (2024).
  197. S. Wang, P. Zhang, F. Fei, T. Tong, X. Zhou, Y. Zhou, J. Zhang, M. Wei, Y. Zhang, L. Zhang, Y. Huang, L. Zhang, X. Zhang, T. Cai, and C. Xie, Unexpected divergence in magnetoreceptor MagR from robin and pigeon linked to two sequence variations, Zool. Res. 45, 69 (2024).
  198. Y. Zhang, P. Zhang, J. Wang, J. Zhang, T. Tong, X. Zhou, Y. Zhou, M. Wei, C. Feng, J. Li, X. Zhang, C. Xie, and T. Cai, Mitochondrial targeting sequence of magnetoreceptor MagR: More than just targeting, Zool. Res. 45, 468 (2024).
  199. M. Wei, C. Han, X. Zhou, T. Tong, J. Zhang, X. Ji, P. Zhang, Y. Zhang, Y. Liu, X. Zhang, T. Cai, and C. Xie, Filamentous morphology engineering of bacteria by iron metabolism modulation through MagR expression, Synthet. Syst. Biotechnol. 9, 522 (2024).
  200. Z. Zhou, X. Peng, J. Chen, X. Wu, Y. Wang, and Y. Hong, Identification of zebrafish magnetoreceptor and cryptochrome homologs, Sci. China Life Sci. 59, 1324 (2016).
  201. M. Jiang, L. Zhang, F. Wang, J. Zhang, G. Liu, B. Gao, and D. Wei, Novel application of magnetic protein: Convenient one-step purification and immobilization of proteins, Sci. Rep. 7, 13329 (2017).
  202. H. Chang, X. Fu, S. Zhao, L. He, Y. Hou, and K. Wu, Molecular characterization, tissue, and developmental expression profiles of MagR and cryptochrome genes in Agrotis ipsilon (Lepidoptera: Noctuidae), Ann. Entomol. Soc. Am. 110, 422 (2017).
  203. J. Kang, D. Kang, G. Yeom, and C.-J. Park, Molecular diagnostic system using engineered fusion protein-conjugated magnetic nanoparticles, Anal. Chem. 93, 16804 (2021).
  204. S. L. Mayo, W. R. Ellis, Jr., R. J. Crutchley, and H. B. Gray, Long-range electron transfer in heme proteins, Science 233, 948 (1986).
  205. M. Kuss-Petermann and O. S. Wenger, Electron transfer rate maxima at large donor-acceptor distances, J. Am. Chem. Soc. 138, 1349 (2016).

Outline

Information

PRX Life 3, 013004– Published 16 January, 2025
  • Received 22 September 2024
  • Accepted 20 December 2024
Crossmark - Check for updates button
Creative Commons Logo

Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

Published by the American Physical Society

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation