Dissociable neural signatures of passive extinction and instrumental control over threatening events

Wanke, Nadine; Schwabe, Lars

doi:10.1093/scan/nsaa074

Cited by 11 publications

(18 citation statements)

References 40 publications

(60 reference statements)

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“…Interestingly, during the presentation of the indicator (i.e., anticipation without stress), participants showed more activation in the vmPFC when an uncontrollable trial was signalled, but under stress they subsequently displayed enhanced vmPFC recruitment when they knew they could terminate the stressor. Although the former finding replicates results by Wanke & Schwabe (2020b), the apparent reversal in vmPFC recruitment induced by aversive stimulation encourages further research into timingdependent effects.…”

Section: Neuroimaging Resultssupporting

confidence: 60%

“…The overall down-regulatory effect that stress exerts on the vmPFC may well have prevented putative differences from reaching suprathreshold levels. In fact, studies that have found the expected condition-dependent connectivity patterns in humans have largely focused on anticipatory responses rather than investigating blood-oxygen-level-dependent (BOLD) signalling under acute stress (Kerr et al, 2012; Wanke & Schwabe, 2020b). Because the fixation phase in our design captures participants’ neural responses just before they were prompted to terminate the stressor, it effectively also constitutes an anticipatory phase, albeit under acute stress.…”

Section: Discussionmentioning

confidence: 99%

“…Others observed diminished stress effects on the vmPFC only if threats were both controllable and predictable (Wood et al, 2015). Using a fear conditioning paradigm, Wanke & Schwabe (2020b) directly contrasted instrumental control with passive extinction and found more pronounced fear reduction in the former condition. However, they noted increased activation of the vmPFC under uncontrollable stress, but not under instrumental control.…”

Section: Introductionmentioning

confidence: 99%

“…Inconsistencies in results may at least in part be explained by differences in experimental designs (e.g., between- vs. within-subject) and the type of stressor used (e.g., electric shocks, thermal stimulation, noise, or social-evaluative stress). Many have studied aversive stimuli which are signalled by a cue and can be avoided (Diener et al, 2009; Kerr et al, 2012; Wanke & Schwabe, 2020b; Cremers et al, 2020). However, we feel that researchers should also investigate controllability-dependent responses in human behaviour and brain function under acute stress.…”

Section: Introductionmentioning

confidence: 99%

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Don’t Stress, It’s Under Control: Neural Correlates of Stressor Controllability in Humans

Meine

Meier

Meyer

et al. 2021

Preprint

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Animal research has repeatedly shown that experience of control over an aversive event can protect against the negative consequences of later uncontrollable stress. Neurobiologically, this effect is assumed to correspond to persistent changes in the pathway linking the ventromedial prefrontal cortex (vmPFC) and the dorsal raphe nucleus. However, it remains unclear to what extent these findings translate to humans. During functional magnetic resonance imaging, we subjected participants to controllable and uncontrollable aversive but non-painful electric stimuli, as well as to a control condition without aversive stimulation. In each trial, a symbol signalled whether participants could terminate the stressor through correct performance in a button-matching task or whether the stressor would be randomly terminated, i.e., uncontrollable. Along with neural responses, we assessed participants' accuracy, reaction times, and heart rate. To relate neural activations and subjective experience, we asked participants to rate perceived control, helplessness, and stress. Results were largely in line with our hypotheses. The vmPFC was generally deactivated by stress, but this effect was attenuated when participants could terminate the stressor compared to when their responses had no effect. Furthermore, activation in stress-responsive regions, including the bilateral insula, was reduced during controllable trials. Under uncontrollable stress, greater vmPFC recruitment was linked to reduced feelings of helplessness. An investigation of condition-dependent differences in vmPFC connectivity yielded no significant results. Our findings further corroborate animal research and emphasise the role of the vmPFC in controllability-dependent regulation of stress responses. Based on the results, we discuss future directions in the context of resilience research and mental health promotion.

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Section: Neuroimaging Resultssupporting

confidence: 60%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Don’t Stress, It’s Under Control: Neural Correlates of Stressor Controllability in Humans

Meine

Meier

Meyer

et al. 2021

Preprint

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“…For example, participants make finger key-pressing responses to control icons on a monitor that are unrelated to the participants' bodily self. While some of the studies demonstrated the fear alleviating effect of active avoidance (Boeke et al, 2017;Delgado, Jou, LeDoux, & Phelps, 2009;Hartley et al, 2019Hartley et al, , 2014Wanke & Schwabe, 2020), the role of actual body movements awaits direct examination. Body movements are still well-required to defend against various real-life threats even in the modern human world -such as violent persons, looming vehicles, and various natural disasters.…”

Section: Introductionmentioning

confidence: 99%

Fear in action: Fear conditioning and alleviation through body movements

Alemany-González

Wokke

Chiba

et al. 2022

Preprint

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Learning a predictive cue of a threat - threat conditioning - allows us to prevent direct contact with the threat. In animals, threat-conditioned cues induce fear-like body movements such as freezing. Interestingly, training animals with alternative bodily defenses to avoid harm could reduce conditioned fear-like responses, suggesting that the physical capacity to actively defend against a threat could help overcome passively induced fear. However, evidence for the role of body movements in acquisition and alleviation of human fear is scarce. In the present study, human participants showed a deviation of multidimensional body movement patterns as threat conditioning progressed in a naturalistic virtual setting. The subsequent training to exert defensive body movements to prevent harm weakened the conditioned body movements and resulted in a long-term (24 hrs) reduction of the physiological responses and subjective fear toward the conditioned cues. Unlike the passive extinction procedure, the training of defensive body movements was resistant to spontaneous recovery of a fear response. The alleviating effect of the active defense training was observed when participants physically defended themselves but not when they merely observed another person vicariously defending against a threat on their behalf. These results suggest the critical role of body movements in both acquisition and reduction of conditioned fear among humans. Further investigations may leverage more embodied procedures to advance mechanistic understandings and clinical interventions of human fear memories.

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