Upon increasing levels of threat, animals activate qualitatively different defensive modes, including freezing and active fight-or-flight reactions. Whereas freezing is a form of behavioural ...inhibition accompanied by parasympathetically dominated heart rate deceleration, fight-or-flight reactions are associated with sympathetically driven heart rate acceleration. Despite the potential relevance of freezing for human stress-coping, its phenomenology and neurobiological underpinnings remain largely unexplored in humans. Studies in rodents have shown that freezing depends on amygdala projections to the brainstem (periaqueductal grey). Recent neuroimaging studies in humans have indicated that similar brain regions may be involved in human freezing. In addition, flexibly shifting between freezing and active defensive modes is critical for adequate stress-coping and relies on fronto-amygdala connections. This review paper presents a model detailing these neural mechanisms involved in freezing and the shift to fight-or-flight action. Freezing is not a passive state but rather a parasympathetic brake on the motor system, relevant to perception and action preparation. Study of these defensive responses in humans may advance insights into human stress-related psychopathologies characterized by rigidity in behavioural stress reactions. The paper therefore concludes with a research agenda to stimulate translational animal–human research in this emerging field of human defensive stress responses.
This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.
Testosterone is an important regulator of social–motivational behavior and is known for its dominance-enhancing and social-anxiolytic properties. However, to date no studies have systematically ...investigated the causal effect of testosterone on actual social approach–avoidance behavior in humans. The present study sets out to test the effects of testosterone administration in healthy female volunteers using an objective implicit measure of social motivational behavior: the social Approach–Avoidance Task, a reaction time task requiring participants to approach or avoid visually presented emotional (happy, angry, and neutral) faces. Participants showed significantly diminished avoidance tendencies to angry faces after testosterone administration. Testosterone did not affect approach–avoidance tendencies to social affiliation (happy) faces. Thus, a single dose testosterone administration reduces automatic avoidance of social threat and promotes relative increase of threat approach tendencies in healthy females. These findings further the understanding of the neuroendocrine regulation of social motivational behavior and may have direct treatment implications for social anxiety, characterized by persistent social avoidance.
•We applied single dose testosterone administration in a placebo-controlled design.•The Approach–Avoidance Task requires participants to respond to emotional faces.•Testosterone diminished avoidance tendencies to angry faces but not happy faces.•Testosterone induced a direct shift from social avoidance to social approach action.•These findings may have direct treatment implications for social psychopathologies.
Anxious individuals consistently fail in controlling emotional behavior, leading to excessive avoidance, a trait that prevents learning through exposure. Although the origin of this failure is ...unclear, one candidate system involves control of emotional actions, coordinated through lateral frontopolar cortex (FPl) via amygdala and sensorimotor connections. Using structural, functional, and neurochemical evidence, we show how FPl-based emotional action control fails in highly-anxious individuals. Their FPl is overexcitable, as indexed by GABA/glutamate ratio at rest, and receives stronger amygdalofugal projections than non-anxious male participants. Yet, high-anxious individuals fail to recruit FPl during emotional action control, relying instead on dorsolateral and medial prefrontal areas. This functional anatomical shift is proportional to FPl excitability and amygdalofugal projections strength. The findings characterize circuit-level vulnerabilities in anxious individuals, showing that even mild emotional challenges can saturate FPl neural range, leading to a neural bottleneck in the control of emotional action tendencies.
When dealing with emotional situations, we often need to rapidly override automatic stimulus-response mappings and select an alternative course of action
1, for instance, when trying to manage, ...rather than avoid, another's aggressive behavior. The anterior prefrontal cortex (aPFC) has been linked to the control of these social emotional behaviors
2, 3. We studied how this control is implemented by inhibiting the left aPFC with continuous theta burst stimulation (cTBS;
4). The behavioral and cerebral consequences of this intervention were assessed with a task quantifying the control of social emotional actions and with concurrent measurements of brain perfusion. Inhibition of the aPFC led participants to commit more errors when they needed to select rule-driven responses overriding automatic action tendencies evoked by emotional faces. Concurrently, task-related perfusion decreased in bilateral aPFC and posterior parietal cortex and increased in amygdala and left fusiform face area. We infer that the aPFC controls social emotional behavior by upregulating regions involved in rule selection
5 and downregulating regions supporting the automatic evaluation of emotions
6. These findings illustrate how exerting emotional control during social interactions requires the aPFC to coordinate rapid action selection processes, the detection of emotional conflicts, and the inhibition of emotionally-driven responses.
► Inhibiting the anterior prefrontal cortex (aPFC) causes impulsive social behavior ► aPFC disruption leads to loss of control over automatic emotional tendencies ► aPFC disruption increases amygdala activity during social emotional actions
Active adaptation to acute stress is essential for coping with daily life challenges. The stress hormone cortisol, as well as large scale re-allocations of brain resources have been implicated in ...this adaptation. Stress-induced shifts between large-scale brain networks, including salience (SN), central executive (CEN) and default mode networks (DMN), have however been demonstrated mainly under task-conditions. It remains unclear whether such network shifts also occur in the absence of ongoing task-demands, and most critically, whether these network shifts are predictive of individual variation in the magnitude of cortisol stress-responses.
In a sample of 335 healthy participants, we investigated stress-induced functional connectivity changes (delta-FC) of the SN, CEN and DMN, using resting-state fMRI data acquired before and after a socially evaluated cold-pressor test and a mental arithmetic task. To investigate which network changes are associated with acute stress, we evaluated the association between cortisol increase and delta-FC of each network.
Stress-induced cortisol increase was associated with increased connectivity within the SN, but with decreased coupling of DMN at both local (within network) and global (synchronization with brain regions also outside the network) levels.
These findings indicate that acute stress prompts immediate connectivity changes in large-scale resting-state networks, including the SN and DMN in the absence of explicit ongoing task-demands. Most interestingly, this brain reorganization is coupled with individuals’ cortisol stress-responsiveness. These results suggest that the observed stress-induced network reorganization might function as a neural mechanism determining individual stress reactivity and, therefore, it could serve as a promising marker for future studies on stress resilience and vulnerability.
•Acute stress prompts changes in connectivity of the salience and default mode networks in the absence of external task demands.•Following stress, intra-network connectivity of the salience network was increased, while both intra-network and global connectivity of the default mode network was decreased.•This brain reorganization was coupled with the magnitude of individual cortisol stressresponses.
Summary Animal studies suggest a relationship between blunted HPA-axis stress reactivity and increased stress-induced food intake in chronically stressed animals. Such a relationship can potentially ...explain the underlying mechanisms of emotional eating in humans. However, no studies have experimentally tested the relationship between stress-induced cortisol responses and acute food intake in high and low emotional eaters. We studied these effects in 46 female students that were preselected on the basis of extremely high (HEE) or low (LEE) scores on an emotional eating questionnaire. Using a within subject design we measured the difference of actual food intake after a control or a stress task (Trier Social Stress Test). The HEE and LEE groups did not differ in their cortisol stress reactivity but emotional eating significantly moderated the relationship between cortisol stress reactivity and the difference of food intake after stress vs control. Whereas HEE participants with a blunted cortisol stress response ate more food after distress than those with an elevated cortisol stress response, LEE participants showed no such relationship. These findings support the relevance of an animal based model on the relationship between a blunted cortisol stress response and increased stress-induced food intake for human high emotional eaters.
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.
Threatening situations ask for rapid and accurate perceptual decisions to optimize coping. Theoretical models have stated that psychophysiological states, such as bradycardia during ...threat-anticipatory freezing, may facilitate perception. However, it's unclear if this occurs via enhanced bottom-up sensory processing or by relying more on prior expectations. To test this, 52 (26 female) participants completed a visual target-detection paradigm under threat-of-shock (15% reinforcement rate) with a manipulation of prior expectations. Participants judged the presence of a backward-masked grating (target presence rate 50%) after systematically manipulating their decision criterion with a rare (20%) or frequent (80%) target presence rate procedure. Threat-of-shock induced stronger heart rate deceleration compared to safe, indicative of threat-anticipatory freezing. Importantly, threat-of-shock enhanced perceptual sensitivity but we did not find evidence of an altered influence of the effect of prior expectations on current decisions. Correct target detection (hits) was furthermore accompanied by an increase in the magnitude of this heart rate deceleration compared to a missed target. While this was independent of threat-of-shock manipulation, only under threat-of-shock this increase was accompanied by more hits and increased sensitivity. Together, these findings suggest that under acute threat participants may rely more on bottom-up sensory processing versus prior expectations in perceptual decision-making. Critically, bradycardia may underlie such enhanced perceptual sensitivity.
Successful responding to acutely threatening situations requires adequate approach-avoidance decisions. However, it is unclear how threat-induced states-like freezing-related bradycardia-impact the ...weighing of the potential outcomes of such value-based decisions. Insight into the underlying computations is essential, not only to improve our models of decision-making but also to improve interventions for maladaptive decisions, for instance in anxiety patients and first-responders who frequently have to make decisions under acute threat. Forty-two participants made passive and active approach-avoidance decisions under threat-of-shock when confronted with mixed outcome-prospects (i.e., varying money and shock amounts). Choice behavior was best predicted by a model including individual action-tendencies and bradycardia, beyond the subjective value of the outcome. Moreover, threat-related bradycardia (high-vs-low threat) interacted with subjective value, depending on the action-context (passive-vs-active). Specifically, in action-contexts incongruent with participants' intrinsic action-tendencies, stronger bradycardia related to diminished effects of subjective value on choice across participants. These findings illustrate the relevance of testing approach-avoidance decisions in relatively ecologically valid conditions of acute and primarily reinforced threat. These mechanistic insights into approach-avoidance conflict-resolution may inspire biofeedback-related techniques to optimize decision-making under threat. Critically, the findings demonstrate the relevance of incorporating internal psychophysiological states and external action-contexts into models of approach-avoidance decision-making.
The steroid hormone testosterone has been associated with behavior intended to obtain or maintain high social status. Although such behavior is typically characterized as aggressive and competitive, ...it is clear that high social status is achieved and maintained not only through antisocial behavior but also through prosocial behavior. In the present experiment, we investigated the impact of testosterone administration on trust and reciprocity using a double-blind randomized control design. We found that a single dose of 0.5 mg of testosterone decreased trust but increased generosity when repaying trust. These findings suggest that testosterone may mediate different types of status-seeking behavior. It may increase competitive, potentially aggressive, and antisocial behavior when social challenges and threats (i.e., abuse of trust and betrayal) need to be considered; however, it may promote prosocial behavior in the absence of these threats, when high status and good reputation may be best served by prosocial behavior.
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