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Freezing revisited: coordinated autonomic and central optimization of threat coping

Abstract

Animals have sophisticated mechanisms for coping with danger. Freezing is a unique state that, upon threat detection, allows evidence to be gathered, response possibilities to be previsioned and preparations to be made for worst-case fight or flight. We propose that — rather than reflecting a passive fear state — the particular somatic and cognitive characteristics of freezing help to conceal overt responses, while optimizing sensory processing and action preparation. Critical for these functions are the neurotransmitters noradrenaline and acetylcholine, which modulate neural information processing and also control the sympathetic and parasympathetic branches of the autonomic nervous system. However, the interactions between autonomic systems and the brain during freezing, and the way in which they jointly coordinate responses, remain incompletely explored. We review the joint actions of these systems and offer a novel computational framework to describe their temporally harmonized integration. This reconceptualization of freezing has implications for its role in decision-making under threat and for psychopathology.

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Fig. 1: Ascending and descending control systems involved in freezing.
Fig. 2: Neuromodulation of autonomic balance during freezing and the switch to action.
Fig. 3: Information processing and control-theoretic considerations pertaining to freezing.
Fig. 4: Measuring freezing in humans.

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Acknowledgements

K.R. was supported by a consolidator grant from the European Research Council (ERC_CoG-2017_772337). P.D. was supported by the Max Planck Society and the Alexander von Humboldt Foundation. The authors thank A. Cleeremans, R. Cools, F. Klumpers, D. Mobbs, O. Robinson and T. Wise for their most helpful comments on an earlier draft, and S. Sara and L. de Voogd for discussions.

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Roelofs, K., Dayan, P. Freezing revisited: coordinated autonomic and central optimization of threat coping. Nat Rev Neurosci 23, 568–580 (2022). https://doi.org/10.1038/s41583-022-00608-2

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