Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T02:54:50.882Z Has data issue: false hasContentIssue false
  • English
  • Français

Navigating at night: fundamental limits on the sensitivity of radical pair magnetoreception under dim light

Published online by Cambridge University Press:  22 October 2019

H. G. Hiscock ,
T. W. Hiscock ,
D. R. Kattnig ,
T. Scrivener ,
A. M. Lewis ,
D. E. Manolopoulos  and
P. J. Hore
H. G. Hiscock
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
T. W. Hiscock
Affiliation:
Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge, UK Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge, UK
D. R. Kattnig
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
T. Scrivener
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
A. M. Lewis
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
D. E. Manolopoulos
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
P. J. Hore*
Affiliation:
Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, Oxford OX1 3QZ, UK
*
Author for correspondence: P. J. Hore, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Night-migratory songbirds appear to sense the direction of the Earth's magnetic field via radical pair intermediates formed photochemically in cryptochrome flavoproteins contained in photoreceptor cells in their retinas. It is an open question whether this light-dependent mechanism could be sufficiently sensitive given the low-light levels experienced by nocturnal migrants. The scarcity of available photons results in significant uncertainty in the signal generated by the magnetoreceptors distributed around the retina. Here we use results from Information Theory to obtain a lower bound estimate of the precision with which a bird could orient itself using only geomagnetic cues. Our approach bypasses the current lack of knowledge about magnetic signal transduction and processing in vivo by computing the best-case compass precision under conditions where photons are in short supply. We use this method to assess the performance of three plausible cryptochrome-derived flavin-containing radical pairs as potential magnetoreceptors.

Keywords

Cryptochromeinformation theorylight-dependent magnetoreceptionnight-migratory songbirdsradical pair mechanismspin dynamics
Type
Report
Information
Quarterly Reviews of Biophysics , Volume 52 , 2019 , e9
Copyright
Copyright © Cambridge University Press 2019. 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Department of Chemistry, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.

†

Permanent address: Living Systems Institute and Department of Physics, University of Exeter, Exeter EX4 4QD, UK.

‡

Present address: Department of Chemistry, University of Chicago, 5735 S Ellis Ave, Chicago, IL 60637, USA.

References

Al-Khalili, J and Mcfadden, J (2014) Life on the Edge: The Coming of age of Quantum Biology. London: Bantam Press.Google Scholar
Beaudry, NJ and Renner, R (2011) An intuitive proof of the data processing inequality. arXiv:1107.0740 [quant-ph].Google Scholar
Bolte, P, Bleibaum, F, Einwich, A, Günther, A, Liedvogel, M, Heyers, D, Depping, A, Wöhlbrand, L, Rabus, R, Janssen-Bienhold, U and Mouritsen, H (2016) Localisation of the putative magnetoreceptive protein cryptochrome 1b in the retinae of migratory birds and homing pigeons. PLoS One 11, e0147819.Google Scholar
Cai, J, Guerreschi, GG and Briegel, HJ (2010) Quantum control and entanglement in a chemical compass. Physical Review Letters 104, 220502.Google Scholar
Cochran, WW, Mouritsen, H and Wikelski, M (2004) Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304, 405–408.Google Scholar
Cover, TM and Thomas, JA (2012) Elements of Information Theory. Hoboken: John Wiley & Sons.Google Scholar
Cramér, H (1999) Mathematical Methods of Statistics. Princeton: Princeton University Press.Google Scholar
Dodson, CA, Hore, PJ and Wallace, MI (2013) A radical sense of direction: signalling and mechanism in cryptochrome magnetoreception. Trends in Biochemical Sciences 38, 435–446.Google Scholar
Gauger, EM, Rieper, E, Morton, JJL, Benjamin, SC and Vedral, V (2011) Sustained quantum coherence and entanglement in the avian compass. Physical Review Letters 106, 040503.Google Scholar
Günther, A, Einwich, A, Sjulstok, E, Feederle, R, Bolte, P, Koch, KW, Solov'yov, IA and Mouritsen, H (2018) Double-cone localization and seasonal expression pattern suggest a role in magnetoreception for European robin cryptochrome 4. Current Biology 28, 211–223.Google Scholar
Guo, LS, Xu, BM, Zou, J and Shao, B (2017) Quantifying magnetic sensitivity of radical pair based compass by quantum fisher information. Scientific Reports 7, 5826.Google Scholar
Haberkorn, R (1976) Density matrix description of spin-selective radical pair reactions. Molecular Physics 32, 1491–1493.Google Scholar
Heyers, D, Manns, M, Luksch, H, Güntürkün, O and Mouritsen, H (2007) A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLoS One 2, e937.Google Scholar
Hilfinger, A, Norman, TM, Vinnicombe, G and Paulsson, J (2016) Constraints on fluctuations in sparsely characterized biological systems. Physical Review Letters 116, 058101.Google Scholar
Hiscock, HG, Worster, S, Kattnig, DR, Steers, C, Jin, Y, Manolopoulos, DE, Mouritsen, H and Hore, PJ (2016) The quantum needle of the avian magnetic compass. Proceedings of the National Academy of Sciences, USA 113, 4634–4639.Google Scholar
Hiscock, HG, Mouritsen, H, Manolopoulos, DE and Hore, PJ (2017) Disruption of magnetic compass orientation in migratory birds by radiofrequency electromagnetic fields. Biophysical Journal 113, 1475–1484.Google Scholar
Hogben, HJ, Efimova, O, Wagner-Rundell, N, Timmel, CR and Hore, PJ (2009) Possible involvement of superoxide and dioxygen with cryptochrome in avian magnetoreception: origin of Zeeman resonances observed by in vivo EPR spectroscopy. Chemical Physics Letters 480, 118–122.Google Scholar
Hogben, HJ, Biskup, T and Hore, PJ (2012) Entanglement and sources of magnetic anisotropy in radical pair-based avian magnetoreceptors. Physical Review Letters 109, 220501.Google Scholar
Hore, PJ and Mouritsen, H (2016) The radical pair mechanism of magnetoreception. Annual Review of Biophysics 45, 299–344.Google Scholar
Hubel, DH (1995) Eye, Brain and Vision. New York: W. H. Freeman, Scientific American Library Series.Google Scholar
Huelga, SF and Plenio, MB (2013) Vibrations, quanta and biology. Contemporary Physics 54, 181–207.Google Scholar
Ihara, S (1993) Information Theory for Continuous Systems. Singapore: World Scientific.Google Scholar
Jaynes, ET (1957) Information theory and statistical mechanics. Physical Review 106, 620–630.Google Scholar
Kattnig, DR (2017) Radical-pair-based magnetoreception amplified by radical scavenging: resilience to spin relaxation. Journal of Physical Chemistry B 121, 10215–10227.Google Scholar
Kattnig, DR and Hore, PJ (2017) The sensitivity of a radical pair compass magnetoreceptor can be significantly amplified by radical scavengers. Scientific Reports 7, 11640.Google Scholar
Kattnig, DR, Evans, EW, Déjean, V, Dodson, CA, Wallace, MI, Mackenzie, SR, Timmel, CR and Hore, PJ (2016) Chemical amplification of magnetic field effects relevant to avian magnetoreception. Nature Chemistry 8, 384–391.Google Scholar
Kram, YA, Mantey, S and Corbo, JC (2010) Avian cone photoreceptors tile the retina as five independent, self-organizing mosaics. PLoS One 5, e8992.Google Scholar
Lambert, N, Chen, YN, Cheng, YC, Li, CM, Chen, GY and Nori, F (2013) Quantum biology. Nature Physics 9, 10–18.Google Scholar
Lau, JCS, Rodgers, CT and Hore, PJ (2012) Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes. Journal of the Royal Society, Interface 9, 3329–3337.Google Scholar
Lee, AA, Lau, JCS, Hogben, HJ, Biskup, T, Kattnig, DR and Hore, PJ (2014) Alternative radical pairs for cryptochrome-based magnetoreception. Journal of the Royal Society, Interface 11, 20131063.Google Scholar
Lehmann, EL and Casella, G (1998) Theory of Point Estimation. New York: Springer-Verlag.Google Scholar
Lestas, I, Vinnicombe, G and Paulsson, J (2010) Fundamental limits on the suppression of molecular fluctuations. Nature 467, 174–178.Google Scholar
Lewis, A (2018) Spin Dynamics in Radical Pairs. Cham: Springer International Publishing.Google Scholar
Liedvogel, M and Mouritsen, H (2010) Cryptochromes – a potential magnetoreceptor: what do we know and what do we want to know? Journal of the Royal Society, Interface 7, S147–S162.Google Scholar
Maeda, K, Henbest, KB, Cintolesi, F, Kuprov, I, Rodgers, CT, Liddell, PA, Gust, D, Timmel, CR and Hore, PJ (2008) Chemical compass model of avian magnetoreception. Nature 453, 387–390.Google Scholar
Maeda, K, Robinson, AJ, Henbest, KB, Hogben, HJ, Biskup, T, Ahmad, M, Schleicher, E, Weber, S, Timmel, CR and Hore, PJ (2012) Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor. Proceedings of the National Academy of Sciences, USA 109, 4774–4779.Google Scholar
Manolopoulos, DE and Hore, PJ (2013) An improved semiclassical theory of radical pair recombination reactions. Journal of Chemical Physics 139, 124106.Google Scholar
Marais, A, Adams, B, Ringsmuth, AK, Ferretti, M, Gruber, JM, Hendrikx, R, Schuld, M, Smith, SL, Sinayskiy, I, Kruger, TPJ, Petruccione, F and Van Grondelle, R (2018) The future of quantum biology. Journal of the Royal Society, Interface 15, 20180640.Google Scholar
Mohseni, M, Omar, Y, Engel, GS and Plenio, MB (eds) (2014) Quantum Effects in Biology. Cambridge: Cambridge University Press.Google Scholar
Mouritsen, H (2018) Long-distance navigation and magnetoreception in migratory animals. Nature 558, 50–59.Google Scholar
Mouritsen, H, Janssen-Bienhold, U, Liedvogel, M, Feenders, G, Stalleicken, J, Dirks, P and Weiler, R (2004) Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proceedings of the National Academy of Sciences, USA 101, 14294–14299.Google Scholar
Mouritsen, H, Feenders, G, Liedvogel, M, Wada, K and Jarvis, ED (2005) Night-vision brain area in migratory songbirds. Proceedings of the National Academy of Sciences, USA 102, 8339–8344.Google Scholar
Müller, P and Ahmad, M (2011) Light-activated cryptochrome reacts with molecular oxygen to form a flavin-superoxide radical pair consistent with magnetoreception. Journal of Biological Chemistry 286, 21033–21040.Google Scholar
Nielsen, MA and Chuang, IL (2010) Quantum Computation and Quantum Information. New York: Cambridge University Press.Google Scholar
Nielsen, C, Kattnig, DR, Sjulstok, E, Hore, PJ and Solov'yov, IA (2017) Ascorbic acid may not be involved in cryptochrome-based magnetoreception. Journal of the Royal Society, Interface 14, 20170657.Google Scholar
Niessner, C, Denzau, S, Gross, JC, Peichl, L, Bischof, HJ, Fleissner, G, Wiltschko, W and Wiltschko, R (2011) Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLoS One 6, e20091.Google Scholar
Niessner, C, Denzau, S, Stapput, K, Ahmad, M, Peichl, L, Wiltschko, W and Wiltschko, R (2013) Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds. Journal of the Royal Society, Interface 10, 20130638.Google Scholar
Niessner, C, Denzau, S, Peichl, L, Wiltschko, W and Wiltschko, R (2014) Magnetoreception in birds: i. Immunohistochemical studies concerning the cryptochrome cycle. Journal of Experimental Biology 217, 4221–4224.Google Scholar
Niessner, C, Gross, JC, Denzau, S, Peichl, L, Fleissner, G, Wiltschko, W and Wiltschko, R (2016) Seasonally changing cryptochrome 1b expression in the retinal ganglion cells of a migrating passerine bird. PLoS One 11, e0150377.Google Scholar
Ritz, T, Adem, S and Schulten, K (2000) A model for photoreceptor-based magnetoreception in birds. Biophysical Journal 78, 707–718.Google Scholar
Ritz, T, Wiltschko, R, Hore, PJ, Rodgers, CT, Stapput, K, Thalau, P, Timmel, CR and Wiltschko, W (2009) Magnetic compass of birds is based on a molecule with optimal directional sensitivity. Biophysical Journal 96, 3451–3457.Google Scholar
Shannon, CE (1948) A mathematical theory of communication. Bell System Technical Journal 27, 379–423.Google Scholar
Shannon, CE (1959) Coding a discrete information source with a distortion measure. IRE National Convention Record 4, 142–163.Google Scholar
Sheppard, DMW, Li, J, Henbest, KB, Neil, SRT, Maeda, K, Storey, J, Schleicher, E, Biskup, T, Rodriguez, R, Weber, S, Hore, PJ, Timmel, CR and Mackenzie, SR (2017) Millitesla magnetic field effects on the photocycle of Drosophila melanogaster cryptochrome. Scientific Reports 7, 42228.Google Scholar
Solov'yov, IA and Schulten, K (2009) Magnetoreception through cryptochrome may involve superoxide. Biophysical Journal 96, 4804–4813.Google Scholar
Steiner, UE and Ulrich, T (1989) Magnetic field effects in chemical kinetics and related phenomena. Chemical Reviews 89, 51–147.Google Scholar
Thomas, RJ, Szekely, T, Cuthill, IC, Harper, DGC, Newson, SE, Frayling, TD and Wallis, PD (2002) Eye size in birds and the timing of song at dawn. Proceedings of the Royal Society B 269, 831–837.Google Scholar
Timmel, CR, Till, U, Brocklehurst, B, Mclauchlan, KA and Hore, PJ (1998) Effects of weak magnetic fields on free radical recombination reactions. Molecular Physics 95, 71–89.Google Scholar
Vitalis, KM and Kominis, IK (2017) Quantum-limited biochemical magnetometers designed using the Fisher information and quantum reaction control. Physical Review A 95, 032129.Google Scholar
Voter, AF (2007) Introduction to the kinetic Monte Carlo method. In Sickafus, KE, Kotomin, EA and Uberuaga, BP (eds), Radiation Effects in Solids. NATO Science Series, vol. 235. Dordrecht: Springer.Google Scholar
Warrant, EJ (1999) Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation. Vision Research 39, 1611–1630.Google Scholar
Wiltschko, W (1968) Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Zeitschrift fuer Tierpsychologie 25, 537–558.Google Scholar
Wiltschko, W and Wiltschko, R (1972) Magnetic compass of European robins. Science 176, 62–64.Google Scholar
Wiltschko, R and Wiltschko, W (1995) Magnetic Orientation in Animals. Berlin: Springer Verlag.Google Scholar
Worster, S, Mouritsen, H and Hore, PJ (2017) A light-dependent magnetoreception mechanism insensitive to light intensity and polarization. Journal of the Royal Society, Interface 14, 20170405.Google Scholar
Zapka, M, Heyers, D, Hein, CM, Engels, S, Schneider, NL, Hans, J, Weiler, S, Dreyer, D, Kishkinev, D, Wild, JM and Mouritsen, H (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461, 1274–1278.Google Scholar
Zapka, M, Heyers, D, Liedvogel, M, Jarvis, ED and Mouritsen, H (2010) Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. European Journal of Neuroscience 32, 619–624.Google Scholar
Supplementary material: PDF

Hiscock et al. supplementary material

Hiscock et al. supplementary material

Download Hiscock et al. supplementary material(PDF)
PDF 374.8 KB