Roelofs, K., Dayan, P.
Nat Rev Neurosci 23, 568–580 (2022).
https://doi.org/10.1038/s41583-022-00608-2
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.
Conclusions and future directions
Considering the post encounter threat state from neural, psychological and computational perspectives has shown how the most obvious external characteristic of this state — a particular form of active freezing arising from co-activation of the normally opposed sympathetic and parasympathetic branches of the ANS — could have various advantages from the viewpoints of both information processing and fast Pavlovian or instrumental action. Descending control of this state is quite well understood, and the potential benefits of expending effort on enhancing unbiased, bottom-up, sensory processing and engaging in planning are easy to observe. However, the roles of ascending neuromodulators in engaging these forms of appropriate information processing are less clear. Certainly, various of the modes of action of ACh and NA in the CNS are in a position to achieve some of this; but much remains to be discovered by precisely recording and manipulating the candidate circuits within the timeframes of the detection, evaluation and action stages.
One important source of ideas is evolutionary theory. For instance, the polyvagal theory of the phylogeny of the ANS suggests that it progressed in three stages. The first, associated with an unmyelinated vagus nerve, allowed metabolic activity to be depressed in response to threat and also controlled aspects of digestion. The second stage was associated with the sympathetic nervous system, which organized energized behaviour for fight or flight. The third stage was associated with a myelinated vagus nerve and allowed for more flexible and sophisticated responding. It has been suggested that the last stage is particularly involved in the evolution of somatic regulation in a social context; but the evolutionary layering of the competition and cooperation between the inhibitory and activating aspects of the different branches of the ANS is notable. It would be interesting to understand the parallel evolution of cholinergic and noradrenergic neuromodulation in the CNS.
Note: We are primates subject to the principles of biology and evolution.
