Fear Without Context: Acute Stress Modulates the Balance of Cue-Dependent and Contextual Fear Learning

Simon-Kutscher, Kathrin; Wanke, Nadine; Hiller, Carlo; Schwabe, Lars

doi:10.1177/0956797619852027

Cited by 30 publications

(14 citation statements)

References 37 publications

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“…8,[32][33][34]41 Possibly, we were not able to demonstrate the fast and immediate effect of acute stress in the current study, due to the relatively long delay between the acute stressor and fear acquisition (Figure 3). In the present study, fear contextualization was measured between 40 and 70 min after acute stress exposure onset (in the immediate-stress group), which is later than in earlier published studies 8,[33][34][35] and slightly overlaps with potential delayed effects. This is a limitation of our design (see "No Time-Dependent Effect of Psychosocial Stress on Fear Contextualization" section) which was optimized to investigate the delayed effects of stress, since these (as opposed to immediate actions) are heavily understudied.…”

Section: No Time-dependent Effect Of Psychosocial Stress On Fear Contmentioning

confidence: 85%

“…This would be in line with the findings of Antov et al in a cued-fear conditioning paradigm, 58 but contrasts with earlier studies that identified a direct relation between context-dependency of emotional information and cortisol-responses following hydrocortisone administration 8,31 or psychosocial stress. 35 Importantly, these studies used different tasks to measure contextdependency of emotional information, including an episodic memory task 31 and fear conditioning tasks with skin conductance responses (SCR) 8,35,58 and FPS responses 8 as outcome measures. Since emotional episodic memory involves a different neurocircuit than fear conditioning 61 and SCR reflects different dimensions of fear learning than FPS responses, 62 it is likely that these tasks are also differentially affected by stress or cortisol.…”

Section: No Time-dependent Effect Of Psychosocial Stress On Fear Contmentioning

confidence: 99%

“…In agreement, two recent studies in humans showed that the immediate effects of acute stress impair contextual fear conditioning (up to 30-min post-stress) in men and women. 34,35 A previous study with exogenous hydrocortisone administration immediately before acquisition reported impairing effects on context-dependent fear expression in women but enhancing effects on contextualization in men. 8 These sex differences could originate from the interaction between stress and sex hormones in fear acquisition and generalization processes.…”

Section: Introductionmentioning

confidence: 98%

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No Time-Dependent Effects of Psychosocial Stress on Fear Contextualization and Generalization: A Randomized-Controlled Study With Healthy Participants

et al. 2019

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The formation of context-dependent fear memories (fear contextualization) can aid the recognition of danger in new, similar, situations. Overgeneralization of fear is often seen as hallmark of anxiety and trauma-related disorders. In this randomizedcontrolled study, we investigated whether exposure to a psychosocial stressor influences retention of fear contextualization and generalization in a time-dependent manner. The Trier Social Stress Test was used to induce psychosocial stress. Healthy male participants (n ¼ 117) were randomly divided into three experimental groups that were subjected to the acquisition phase of the Fear Generalization Task: (1) without stress, (2) immediately after acute stress, or (3) 2 h after acute stress. In this task, a male with neutral facial expression (conditioned stimuli) was depicted in two different contexts that modulated the conditioned stimuli-unconditioned stimuli (¼shock) association (threat, safe). Salivary alpha-amylase and cortisol levels were measured throughout the experiment. After a 24-h delay, context-dependency of fear memory was investigated with an unannounced memory test consisting of the threat and safe contexts alternated with a novel context (the generalization context). Multilevel analyses revealed that participants showed increased fear-potentiated startle responses to the conditioned stimuli in the threat compared to the safe context, at the end of the acquisition phase, indicating adequate fear contextualization. Directly after acquisition, there were no time-dependent effects of psychosocial stress on fear contextualization. Context-dependency of fear memories was retained 24 h later, as fear-potentiated startle responding was modulated by context (threat > safe or novel). At that time, the context-dependency of fear memories was also not influenced by the early or late effects of the endogenous stress response during acquisition. These results with experimental stress deviate in some aspects from those earlier obtained with exogenous hydrocortisone administration, suggesting a distinct role for stress mediators other than cortisol.

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Section: No Time-dependent Effect Of Psychosocial Stress On Fear Contmentioning

confidence: 85%

Section: No Time-dependent Effect Of Psychosocial Stress On Fear Contmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

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No Time-Dependent Effects of Psychosocial Stress on Fear Contextualization and Generalization: A Randomized-Controlled Study With Healthy Participants

et al. 2019

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“…Two of the most prominent stress mediators are glucocorticoids and noradrenaline, both of which are known to be major modulators of learning and memory in general (Diamond, Campbell, Park, Halonen, & Zoladz, 2007 ; Joels, Fernandez, & Roozendaal, 2011 ; Quaedflieg & Schwabe, 2018 ; Roozendaal, Okuda, de Quervain, & McGaugh, 2006 ; Sandi & Pinelo-Nava, 2007 ; Schwabe, Joels, Roozendaal, Wolf, & Oitzl, 2012 ). Moreover, there also is evidence that stress affects fear learning processes (Jackson, Payne, Nadel, & Jacobs, 2006 ; Merz, Elzinga, & Schwabe, 2016 ; Simon-Kutscher, Wanke, Hiller, & Schwabe, 2019 ), presumably also driven by glucocorticoids and noradrenergic arousal (Krugers, Zhou, Joels, & Kindt, 2011 ; Merz, Hamacher-Dang, Stark, Wolf, & Hermann, 2018 ). Prefrontal and medial-temporal brain areas critically involved in fear generalization (Greenberg et al, 2013 ; Lissek, Bradford, et al, 2014 ; Lopresto et al, 2016 ; Onat & Büchel, 2015 ) are known to be particularly sensitive to stress and stress mediators (de Kloet, Joels, & Holsboer, 2005 ; Krugers, Karst, & Joels, 2012 ; Roozendaal et al, 2006 ).…”

Section: Introductionmentioning

confidence: 99%

Acute stress leaves fear generalization in healthy individuals intact

Kausche

Zerbes

Kampermann

et al. 2021

Cogn Affect Behav Neurosci

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Because threatening situations often occur in a similar manner, the generalization of fear to similar situations is adaptive and can avoid harm to the organism. However, the overgeneralization of fear to harmless stimuli is maladaptive and assumed to contribute to anxiety disorders. Thus, elucidating factors that may modulate fear (over)generalization is important. Based on the known effects of acute stress on learning, which are at least partly due to noradrenergic arousal, we investigated whether stress may promote fear overgeneralization and whether we could counteract this effect by reducing noradrenergic arousal. In a placebo-controlled, double-blind, between-subjects design, 120 healthy participants underwent a fear-conditioning procedure on Day 1. Approximately 24 hours later, participants received orally either a placebo or the beta-adrenergic receptor antagonist propranolol and were exposed to a stress or control manipulation before they completed a test of fear generalization. Skin conductance responses as well as explicit rating data showed a successful acquisition of conditioned fear on Day 1 and a pronounced fear generalization 24 hours later. Although physiological data confirmed the successful stress manipulation and reduction of noradrenergic arousal, the extent of fear generalization remained unaffected by stress and propranolol. The absence of a stress effect on fear generalization was confirmed by a second study and a Bayesian analysis across both data sets. Our findings suggest that acute stress leaves fear generalization processes intact, at least in a sample of healthy, young individuals.

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“…Two participants did not return for the second experimental day and were excluded from the analysis. The target sample size was based on experience from previous studies on stress and memory processes(Schönfeld, Ackermann, & Schwabe, 2014;Simon-Kutscher, Wanke, Hiller, & Schwabe, 2019;Zerbes & Schwabe, 2019). While no prior research targeted retroactive memory enhancements specifically through social stress, our research design in this experiment was inspired by the study byDunsmoor et al (2015).…”

mentioning

confidence: 99%

On the search for a selective and retroactive strengthening of memory: repeated failure to find category-specific behavioral tagging

Kalbe¹,

Schwabe²

2020

Preprint

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Storing motivationally salient experiences preferentially in long-term memory is generally adaptive. While such relevant experiences are often immediately obvious, a problem arises when the relevance of initially ambiguous events becomes evident sometime after encoding. Is there a mechanism that enables the retroactive enhancement of specific memories? Recent evidence suggests the existence of such a mechanism that selectively strengthens weak memories for neutral stimuli from one category when their respective category gains motivational significance later. While such a selective retroactive memory enhancement has considerable implications for adaptive memory, evidence for this phenomenon is based on only two studies. Here, we report data from five failed attempts to produce category-specific retroactive memory enhancements in the context of aversive or reward learning. Experiments 1A, 1B, and 1C aimed to closely replicate findings of category-specific retroactive memory enhancements for neutral stimuli from a category that was later predictive of aversive electric shocks. Experiment 2 was designed to broaden the scope of these experiments by replacing electric shocks with an ecologically more valid psychosocial stress procedure. Finally, in Experiment 3, we aimed to replicate findings of category-specific retroactive memory enhancement in the context of instrumental reward learning. Although our data showed enhanced memory for the arousing stimuli themselves as well as related subsequent stimuli, none of our experiments provided any evidence for category-specific retroactive memory enhancement. Thus, our data cast doubt on the proposed selective retroactive enhancement of initially weak memory.

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Fear Without Context: Acute Stress Modulates the Balance of Cue-Dependent and Contextual Fear Learning

Cited by 30 publications

References 37 publications

No Time-Dependent Effects of Psychosocial Stress on Fear Contextualization and Generalization: A Randomized-Controlled Study With Healthy Participants

No Time-Dependent Effects of Psychosocial Stress on Fear Contextualization and Generalization: A Randomized-Controlled Study With Healthy Participants

Acute stress leaves fear generalization in healthy individuals intact

On the search for a selective and retroactive strengthening of memory: repeated failure to find category-specific behavioral tagging

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