On the optimality of the radical-pair quantum compass
Abstract: Quantum sensing enables the ultimate precision attainable in parameter estimation. Circumstantial evidence suggests that certain organisms, most notably migratory songbirds, also harness quantum-enhanced magnetic field sensing via a radical-pair-based chemical compass for the precise detection of the weak geomagnetic field. However, what underpins the acuity of such a compass operating in a noisy biological setting, at physiological temperatures, remains an open question. Here, we address the fundamental limits of inferring geomagnetic field directions from radical-pair spin dynamics. Specifically, we compare the compass precision, as derived from the directional dependence of the radical-pair recombination yield, to the ultimate precision potentially realisable by a quantum measurement on the spin system under steady-state conditions. To this end, we probe the quantum Fisher information and associated Cram\'er--Rao bound in spin models of realistic complexity, accounting for complex inter-radical interactions, a multitude of hyperfine couplings, and asymmetric recombination kinetics, as characteristic for the magnetosensory protein cryptochrome. We compare several models implicated in cryptochrome magnetoreception and unveil their optimality through the precision of measurements ostensibly accessible to nature. Overall, the comparison provides insight into processes honed by nature to realise optimality whilst constrained to operating with mere reaction yields. Generally, the inference of compass orientation from recombination yields approaches optimality in the limits of complexity, yet plateaus short of the theoretical optimal precision bounds by up to one or two orders of magnitude, thus underscoring the potential for improving on design principles inherent to natural systems.
- C. L. Degen, F. Reinhard, and P. Cappellaro, Quantum sensing, Rev. Mod. Phys. 89, 035002 (2017).
- V. Giovannetti, S. Lloyd, and L. Maccone, Quantum-enhanced measurements: Beating the standard quantum limit, Science 306, 1330–1336 (2004).
- S. J. Asztalos et al., SQUID-based microwave cavity search for dark-matter axions, Phys. Rev. Lett. 104, 041301 (2010).
- P. J. Hore and H. Mouritsen, The radical-pair mechanism of magnetoreception, Annu. Rev. Biophys. 45, 299–344 (2016).
- C. T. Rodgers and P. J. Hore, Chemical magnetoreception in birds: The radical pair mechanism, Proc. Natl. Acad. Sci. U. S. A. 106, 353–360 (2009).
- K. Schulten, C. E. Swenberg, and A. Weiler, A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion, Z Phys. Chem. 111, 1–5 (1978).
- H. Mouritsen, Long-distance navigation and magnetoreception in migratory animals, Nature 558, 50–59 (2018).
- K. J. Lohmann, Magnetic-field perception, Nature 464, 1140–1142 (2010).
- R. Wiltschko and W. Wiltschko, Magnetoreception in birds, J. R. Soc. Interface 16, 20190295 (2019).
- G. C. Nordmann, T. Hochstoeger, and D. A. Keays, Magnetoreception—A sense without a receptor, PLOS Biol. 15, 1–10 (2017).
- W. Wiltschko and R. Wiltschko, Migratory orientation of European robinss is affected by the wavelength of light as well as by a magnetic pulse, J. Comp. Physiol. A 177, 363–369 (1995).
- T. Ritz, S. Adem, and K. Schulten, A model for photoreceptor-based magnetoreception in birds, Biophys. J. 78, 707–718 (2000).
- J. Xu et al., Magnetic sensitivity of cryptochrome 4 from a migratory songbird, Nature 594, 535–540 (2021).
- M. Procopio and T. Ritz, The reference-probe model for a robust and optimal radical-pair-based magnetic compass sensor, J. Chem. Phys. 152, 065104 (2020).
- J. Cai, F. Caruso, and M. B. Plenio, Quantum limits for the magnetic sensitivity of a chemical compass, Phys. Rev. A 85, 040304 (2012).
- I. A. Solov’yov and K. Schulten, Magnetoreception through cryptochrome may involve superoxide, Biophys. J. 96, 4804–4813 (2009).
- P. Mondal and M. Huix-Rotllant, Theoretical insights into the formation and stability of radical oxygen species in cryptochromes, Phys. Chem. Chem. Phys. 21, 8874–8882 (2019).
- P. Müller and M. Ahmad, Light-activated cryptochrome reacts with molecular oxygen to form a flavin–superoxide radical pair consistent with magnetoreception, J. Biol. Chem. 286, 21033–21040 (2011).
- N. S. Babcock and D. R. Kattnig, Radical scavenging could answer the challenge posed by electron–electron dipolar interactions in the cryptochrome compass model, JACS Au 1, 2033–2046 (2021).
- R. H. Keens, S. Bedkihal, and D. R. Kattnig, Magnetosensitivity in dipolarly coupled three-spin systems, Phys. Rev. Lett. 121, 096001 (2018).
- N. S. Babcock and D. R. Kattnig, Electron–electron dipolar interaction poses a challenge to the radical pair mechanism of magnetoreception, J. Phys. Chem. Lett. 11, 2414–2421 (2020).
- D. R. Kattnig and P. J. Hore, The sensitivity of a radical pair compass magnetoreceptor can be significantly amplified by radical scavengers, Sci. Rep. 7, 1–12 (2017).
- D. R. Kattnig, Radical-pair-based magnetoreception amplified by radical scavenging: Resilience to spin relaxation, J. Phys. Chem. B 121, 10215–10227 (2017).
- F. Schuhmann, D. R. Kattnig, and I. A. Solov’yov, Exploring post-activation conformational changes in pigeon cryptochrome 4, J. Phys. Chem. B 125, 9652–9659 (2021).
- M. Liedvogel and H. Mouritsen, Cryptochromes—a potential magnetoreceptor: What do we know and what do we want to know?, J. R. Soc. Interface 7, S147–S162 (2010).
- S. L. Braunstein and C. M. Caves, Statistical distance and the geometry of quantum states, Phys. Rev. Lett. 72, 3439 (1994).
- A. Holevo, Probabilistic and statistical aspects of quantum theory (Edizioni della Normale Pisa, 2011).
- R. A. Fisher, Theory of Statistical Estimation, Math. Proc. Cambridge Philos. Soc. 22, 700–725 (1925).
- H. Cramér, Mathematical methods of statistics (PMS-9) (Princeton University Press, 1946).
- 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).
- Y. Tiwari and V. S. Poonia, Quantum coherence enhancement by the chirality-induced spin selectivity effect in the radical-pair mechanism, Phys. Rev. A 107, 052406 (2023).
- 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).
- T. P. Le and A. Olaya-Castro, Basis-independent system-environment coherence is necessary to detect magnetic field direction in an avian-inspired quantum magnetic sensor, arXiv: 2011.15016 (2020).
- J. Cai and M. B. Plenio, Chemical compass model for avian magnetoreception as a quantum coherent device, Phys. Rev. Lett. 111, 230503 (2013).
- H. J. Hogben, T. Biskup, and P. J. Hore, Entanglement and sources of magnetic anisotropy in radical pair-based avian magnetoreceptors, Phys. Rev. Lett. 109, 220501 (2012).
- L. D. Smith, J. Deviers, and D. R. Kattnig, Observations about utilitarian coherence in the avian compass, Sci. Rep. 12, 1–10 (2022a).
- 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).
- M. G. Paris, Quantum estimation for quantum technology, Int. J. Quantum Inf. 7, 125–137 (2009).
- C. W. Helstrom, Quantum detection and estimation theory, J. Stat. Phys. 1, 231–252 (1969).
- R. Bhatia and P. Rosenthal, How and Why to Solve the Operator Equation AX-XB = Y, Bull. London Math. Soc. 29, 1–21 (1997).
- D. Šafránek, Simple expression for the quantum Fisher information matrix, Phys. Rev. A 97, 042322 (2018).
- J. S. Sidhu and P. Kok, Geometric perspective on quantum parameter estimation, AVS Quantum Sci. 2, 014701 (2019).
- D. R. Kattnig, I. A. Solov’yov, and P. J. Hore, Electron spin relaxation in cryptochrome-based magnetoreception, Phys. Chem. Chem. Phys. 18, 12443–12456 (2016a).
- A. T. Dellis and I. K. Kominis, The quantum Zeno effect immunizes the avian compass against the deleterious effects of exchange and dipolar interactions, Biosystems 107, 153–157 (2012).
- I. K. Kominis, Quantum Zeno effect explains magnetic-sensitive radical-ion-pair reactions, Phys. Rev. E 80, 056115 (2009).
- Y. Tiwari and V. S. Poonia, Role of chiral-induced spin selectivity in the radical pair mechanism of avian magnetoreception, Phys. Rev. E 106, 064409 (2022).
- J. Luo and P. J. Hore, Chiral-induced spin selectivity in the formation and recombination of radical pairs: Cryptochrome magnetoreception and EPR detection, New J. Phys. 23, 043032 (2021).
- J. L. Ramsay and D. R. Kattnig, Magnetoreception in cryptochrome enabled by one-dimensional radical motion, AVS Quantum Sci. 5, 22601 (2023).
- N. Ozturk, Phylogenetic and functional classification of the photolyase/cryptochrome family, Photochem. Photobiol. 93, 104–111 (2017).
- A. Sancar, Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors, Chem. Rev. 103, 2203–2237 (2003).
- J. Glatthard and L. A. Correa, Bending the rules of low-temperature thermometry with periodic driving, Quantum 6, 705 (2022).
- A. R. Mirza and A. Z. Chaudhry, Improving the estimation of the environment parameters via a two-qubit scheme, arXiv: 2305.12278 (2023).
- V. V. Krylov and E. A. Osipova, Molecular biological effects of weak low-frequency magnetic fields: Frequency–amplitude efficiency windows and possible mechanisms, Int. J. Mol. Sci. 24, 10989 (2023).
- H. Zadeh-Haghighi and C. Simon, Magnetic field effects in biology from the perspective of the radical pair mechanism, J. R. Soc. Interface 19, 20220325 (2022a).
- H. Zadeh-Haghighi and C. Simon, Radical pairs can explain magnetic field and lithium effects on the circadian clock, Sci. Reports 2022 121 12, 1–12 (2022b).
- P. J. Hore, K. L. Ivanov, and M. R. Wasielewski, Spin chemistry, J. Chem. Phys. 152, 120401 (2020).
- Y. Kim et al., Quantum biology: An update and perspective, Quantum Reports 3, 80–126 (2021).
- A. Marais et al., The future of quantum biology, J. R. Soc. Interface 15, 20180640 (2018).
Paper Prompts
Sign up for free to create and run prompts on this paper using GPT-5.
Top Community Prompts
Collections
Sign up for free to add this paper to one or more collections.