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arXiv:2401.02923 · Quantum Science and Technology

On the optimality of the radical-pair quantum compass

Luke D. Smith, Jonas Glatthard, Farhan T. Chowdhury, Daniel R. Kattnig

Published May 8, 2024• 11 citations
arXivHTMLPDF

Abstract

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 Cramér–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 levels off 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.

DOI
10.1088/2058-9565/ad48b4

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The radical pair (RP) based compass is considered as one of the principal models of avian magnetoreception. Different from the conventional approach where the sensitivity of RP based compass is described by the singlet yield, we introduce the quantum Fisher information (QFI), which represents the maximum information about the magnetic field's direction extracted from the RP state, to quantify the sensitivity of RP based compass. The consistency between our results and experimental observations suggests that the QFI may serve as a measure to describe the sensitivity of RP based compass. Besides, within the framework of quantum metrology, we give two specific possible measurement schemes and find that the conventional singlet yield is corresponding to the measurement of total angular momentum. Moreover, we show that the measurement of fluctuation of the total magnetic moment is much more accurate than the singlet yield measurement, and is close to the optimal measurement scheme. Finally, the effects of entanglement and decoherence are also discussed in the spirit of our approach.

Scientific Reports•Jul 13, 2017•10 citations
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 Cramér–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 levels off 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.
The quantum control of spin-correlated radical pairs (SCRPs) holds promise for the targeted manipulation of magnetic field effects (MFEs), with potential applications ranging from the design of noise-resilient quantum information processors to genetically encodable quantum sensors. However, achieving precise handles over the intricate interplay between coherent electron spin dynamics and incoherent relaxation processes in photo-excited radical-pair reactions requires tractable approaches for numerically obtaining controls for large, complex open quantum systems. To that end, we realise optimal control of SCRPs in the low-magnetic-field regime, through first generalising the gradient-ascent pulse engineering (GRAPE) paradigm to allow for optimising time-integral reaction yields for coherent control of SCRP spin dynamics. We then explore how interradical interactions which are unavoidable in a biophysical setting, such as electron-electron dipolar and exchange couplings, alongside driving resulting from intrinsic structural motion, can push the precision of the proposed radical pair quantum compass in cryptochrome closer to approaching the quantum Cram\'{e}r-Rao bound. Remarkably, this approach to optimality is amplified under environmental noise and persists with increasing complexity of the spin system, suggesting that perturbations inherent to such natural systems have enabled them to operate closer to the quantum limit to more effectively extract information from the weak geomagnetic field. Bolstered by these findings, we furthermore demonstrate how a control engineering approach based on the Pontryagin Maximum Principle (PMP) can offer a more computationally feasible route towards realising not only coherent, but also incoherent control, of noisy SCRP open-system spin dynamics. This raises prospects for experimental realisation of spin control of actual radical-pair systems in ambient magnetic fields, by suppressing or boosting radical reaction yields using purpose-specific radio-frequency wave forms, paving the way for inspiring more noise-robust quantum magnetometry via chemical reaction-yield-dependence, and potentially applications of quantum control to physiologically relevant radical-pair reaction intermediates.
It is hypothesised that the avian compass relies on spin dynamics in a recombining radical pair. Quantum coherence has been suggested as a resource to this process that nature may utilise to achieve increased compass sensitivity. To date, the true functional role of coherence in these natural systems has remained speculative, lacking insights from sufficiently complex models. Here, we investigate realistically large radical pair models with up to 21 nuclear spins, inspired by the putative magnetosensory protein cryptochrome. By varying relative radical orientations, we reveal correlations of several coherence measures with compass fidelity. Whilst electronic coherence is found to be an ineffective predictor of compass sensitivity, a robust correlation of compass sensitivity and a global coherence measure is established. The results demonstrate the importance of realistic models, and appropriate choice of coherence measure, in elucidating the quantum nature of the avian compass.
Magnetosensitive spin-correlated radical pairs offer a promising platform for noise-robust quantum metrology; however, unavoidable interradical interactions, such as electron-electron dipolar and exchange couplings, alongside deleterious perturbations resulting from intrinsic radical motion, typically degrade their potential as magnetometers. In contrast, we show how structured molecular motion modulating interradical interactions in a chemical sensor in cryptochrome can, in fact, increase sensitivity and, moreover, push precision in estimating magnetic field directions closer to the quantum Cramér-Rao bound. The latter is evident both on average over the magnetoreceptor array and, to an even greater extent, for the subset of best-performing magnetoreceptors, thus suggesting near-optimal metrological performance. Remarkably, this approach to optimality is amplified under environmental noise and persists with increasing complexity of the spin system, suggesting that perturbations inherent to such natural systems have enabled them to operate closer to the quantum limit to more effectively extract information from the weak geomagnetic field. This insight opens the possibility of channeling the underlying physical principles of motion-induced modulation of electron spin-spin interactions toward devising efficient handles over emerging molecular quantum information technologies.
Sensing of the geomagnetic field direction by many living organisms is commonly thought to involve radical pairs, such as those formed photochemically between the flavin and tryptophan radicals in the cryptochrome proteins. Previous theoretical studies have shown that strongly axial hyperfine couplings in the cryptochrome radicals greatly enhance the formation of a signaling state of the protein when the magnetic field is directed perpendicular to the hyperfine axis of either of the radicals. However, further analysis led to the conclusion that sharpness of detecting those magnetic directions is strongly suppressed by the inter-radical electron spin coupling. Here, we perform theoretical simulations of the compass function for a set of arrangements of the intra- and inter-radical spin couplings in the idealized cryptochrome radical pair, and find certain arrangements that preserve the sharpness in detecting the direction of the geomagnetic field. One particular arrangement, with the hyperfine axes of the radicals orthogonal to the symmetry axis of inter-radical coupling, provides even sharper field-direction sensitivity than that contributed solely by the anisotropy of the hyperfine coupling.
The chemical compass model, based on radical pair reactions, is an idea to explain avian magnetoreception. At present, to the best of our knowledge, questions concerning the key ingredients responsible for the high sensitivity of a chemical compass and the possible role of quantum coherence and decoherence remain unsolved. Here, we investigate the optimized hyperfine coupling for a chemical compass in order to achieve the best magnetic field sensitivity. We show that its magnetic sensitivity limit can be further extended by simple quantum control and may benefit from additional decoherence. With this, we clearly demonstrate how quantum coherence can be exploited in the functioning of a chemical compass. The present results also provide routes toward the design of a biomimetic weak magnetic field sensor.
The radical pair (RP) based compass is considered as one of the principal models of avian magnetoreception. Different from the conventional approach where the sensitivity of RP based compass is described by the singlet yield, we introduce the quantum Fisher information (QFI), which represents the maximum information about the magnetic field's direction extracted from the RP state, to quantify the sensitivity of RP based compass. The consistency between our results and experimental observations suggests that the QFI may serve as a measure to describe the sensitivity of RP based compass. Besides, within the framework of quantum metrology, we give two specific possible measurement schemes and find that the conventional singlet yield is corresponding to the measurement of total angular momentum. Moreover, we show that the measurement of fluctuation of the total magnetic moment is much more accurate than the singlet yield measurement, and is close to the optimal measurement scheme. Finally, the effects of entanglement and decoherence are also discussed in the spirit of our approach.