Freezing revisited: coordinated autonomic and central optimization of threat coping

Abstract

Animals have sophisticated mechanisms for coping with dangers. 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 sympathetic and parasympathetic branches of the autonomic nervous system. However, the interactions between autonomic systems and the brain during freezing, and the way that 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. [H1] IntroductionAnimals are endowed with elaborate repertoires of defensive actions that allow them to respond as optimally as possible to the dangers they face. Successfully responding to a threat involves a cascade of potential behavioural responses that are organized according to its perceived immediacy 1-4 . Beyond 'safety' (the stage at which no threat is present) three stages in this cascade are traditionally distinguished 5-8 . 'Pre-encounter threat' responses are associated with the possibility, but no immediate evidence, that a predator might be present. For instance, a grazing deer, upon hearing a noise in the forest, will raise its head and scan the environment to ascertain the possible presence of a wolf. 'Postencounter threat' responses arise upon detection of a not-yet-attacking predator. Here, the deer will usually and strikingly 'freeze', remaining as immobile as possible. Finally, 'circa-strike' responses are the responses prey take when actually confronted with an immediate threat (often referred to as 'flight, fight or fright' responses). Most likely, our deer will shoot off as fast as possible to escape.Traditional views conceptualized threat anticipatory freezing merely as a passive fear state 9-11 . However, there is increasing acknowledgement that this behaviour is not passive and may differ from the fright-related immobility that is observed after the dreaded thing has happened 1,7,12,13 . In this article, we propose that post-encounter freezing involves complex cognitive operations aimed at assessing the nature of the threat and planning for appropriate responses, as well as complex somatic processes geared towards action preparation. Crucial aspects of such preparation are that bodily

I did not scream. I could not; I was terrified. I just followed them…I blocked my mind. Then they all raped me: A narrative inquiry on the onset of tonic immobility among women rape victims in Nigeria

“…The accompanying feeling of inescapability ignites a TI like state (43) when the attacker physically confronts their victim. Participants narrated how they were frozen with fear, their bodies going limp (P1, 26-30; P2, 26-30; P3, [31][32][33][34][35], characteristics that agree with Marks' definition of TI (68). Being confronted by an armed attacker created extreme fear in the victims due to the anticipated consequences of being attacked and injured by someone who was clearly physically stronger than they were and had every intention of harming them (69,70,44).…”

“…On the other hand, for (30), the onset of TI is shown by a rape-induced paralysis, the two actions denote the same phenomenon. This lack of clarity as a standard for TI may have implications in decisionmaking towards developing appropriate intervention algorithms (31). It was stressed by (16) that understanding these concepts leads to tangible means of preventing maladaptive behaviours as consequences.…”

Missing pieces in decoding the brain oxytocin puzzle: Functional insights from mouse brain wiring diagrams

“…Alternatively, the freezing response may occur, which puts on hold the flight or fight response-activated mainly through the vagal pathway from the DMX by inhibiting sympathetic activation (Roelofs, 2017;Roelofs and Dayan, 2022).…”

“…The skeletal muscle activation for fight and attack is mediated through the periaqueductal gray (PAG) whereas visceromotor output (for example, increasing cardiac output) is mediated via the dorsal motor nucleus of the vagus nerve (DMX) ( Kozlowska et al, 2015 ; Deng et al, 2016 ). Alternatively, the freezing response may occur, which puts on hold the flight or fight response- activated mainly through the vagal pathway from the DMX by inhibiting sympathetic activation ( Roelofs, 2017 ; Roelofs and Dayan, 2022 ).…”

Stimulation of the ventromedial prefrontal cortex blocks the return of subcortically mediated fear responses

“…Given that the vmPFC has been ascribed a pivotal role in the consolidation and retrieval of extinction memory, we hypothesized that an anodal transcranial direct current stimulation targeting the vmPFC during extinction memory retrieval would facilitate extinction recall and prevent a subsequent return of fear. Since the vmPFC has found to exhibit such fear-attenuating effects by top-down inhibition of the amygdala, we further expected that these effects would be particularly pronounced for amygdala-dependent indicators of defensive responding (i.e., skin conductance, fear potentiated startle and fear bradycardia) [ 33 , 41 , 43 , 55 ]. On the other hand, we did not expect similar inhibitory effects for cognitive indices of fear activation, which have been suggested to be mediated by various cortical and hippocampal areas [ 35 , 37 , 42 ].…”