The influence of acute stress on the regulation of conditioned fear

Raio, Candace M.; Phelps, Elizabeth A.

doi:10.1016/j.ynstr.2014.11.004

Cited by 91 publications

(70 citation statements)

References 221 publications

(297 reference statements)

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“…By contrast, animals that are able to express an active strategy recruit PFC IL to toggle amygdala output pathways—control is shifted from CeA outputs that mediate freezing to the BA outputs that mediate active avoidance. Connections between medial PFC and the amygdala in humans have been implicated in other aspects of emotion regulation in the face of stress 228, 229 . A treatment that is able to suppress excessive CeA-mediated reactions might be very useful in facilitating the acquisition of active coping skills in those predisposed towards passive coping.…”

Section: Therapeutic Implicationsmentioning

confidence: 99%

The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm

et al. 2016

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Research on avoidance conditioning began in the late 1930s as a way to use laboratory experiments to better understand uncontrollable fear and anxiety. Avoidance was initially conceived of as a two-factor learning process in which fear is initially acquired through Pavlovian aversive conditioning (so-called fear conditioning), and then behaviors that reduce the fear aroused by the Pavlovian conditioned stimulus are reinforced through instrumental conditioning. Over the years, criticisms of both the avoidance paradigm and the two-factor fear theory arose. By the mid 1980s, avoidance had fallen out of favor as an experimental model relevant to fear and anxiety. However recent progress in understanding the neural basis of Pavlovian conditioning has stimulated a new wave of research on avoidance. The new work has fostered new insights into contributions of not only Pavlovian and instrumental learning, but also habit learning, to avoidance, and has suggested that the reinforcing event underlying the instrumental phase should be conceived in terms of cellular and molecular events in specific circuits rather than in terms of vague notions of fear reduction. In our approach, defensive reactions (freezing), actions (avoidance) and habits (habitual avoidance) are viewed as being controlled by unique circuits that operate non-consciously in the control of behavior, and that are distinct from the circuits that give rise to conscious feelings of fear and anxiety. These refinements, we suggest, overcome older criticisms, justifying the value of the new wave of research on avoidance, and offering a fresh perspective on the clinical implications of this work.

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Section: Therapeutic Implicationsmentioning

confidence: 99%

The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm

et al. 2016

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“…The effects of stress on the ability to regulate defensive behaviors have been detailed using Pavlovian threat (fear) conditioning tasks in humans and laboratory animals (7)(8)(9). Much of this research has focused predominately on how acute and chronic stress impairs threat extinction to conditioned stimuli (CS) or contexts via structural and functional changes in the neural circuitry involved in the learning (10), consolidation (11), and retrieval (12) of extinction memories (see ref.…”

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confidence: 99%

Stress promotes generalization of older but not recent threat memories

Dunsmoor

Otto

Phelps

2017

Proc. Natl. Acad. Sci. U.S.A.

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Stress broadly affects the ability to regulate emotions and may contribute to generalization of threat-related behaviors to harmless stimuli. Behavioral generalization also tends to increase over time as memory precision for recent events gives way to more gist-like representations. Thus, acute stress coupled with a delay in time from a negative experience may be a strong predictor of the transition from normal to generalized fear expression. Here, we investigated the effect of a single-episode acute stressor on generalization of aversive learning when stress is administered either immediately after an aversive learning event or following a delay. In a betweensubjects design, healthy adult volunteers underwent threat (fear) conditioning using a tone-conditioned stimulus paired with an electric shock to the wrist and another tone not paired with shock. Behavioral generalization was tested to a range of novel tones either on the same day (experiment 1) or 24 h later (experiment 2) and was preceded by either an acute stress induction or a control task. Anticipatory sympathetic arousal [i.e., skin conductance responses (SCRs)] and explicit measures of shock expectancy served as dependent measures. Stress administered shortly after threat conditioning did not affect behavioral generalization. In contrast, stress administered following a delay led to heightened arousal and increased generalization of SCRs and explicit measures of shock expectancy. These findings show that acute stress increases generalization of older but not recent threat memories and have clinical relevance to understanding overgeneralization characteristics of anxiety and stress-related disorders.stress | Pavlovian conditioning | associative learning | generalization | memory A number of anxiety and stress-related disorders can be characterized by an inability to discriminate threat from safety. For instance, a core symptom of trauma-and stressrelated disorders [e.g., posttraumatic stress disorder (PTSD)] is persistent and widespread fear and avoidance of myriad harmless cues that act as reminders of the trauma, often referred to as overgeneralization (1). A key component of overgeneralization in anxiety and stress-related disorders may hinge on stress-induced changes in neural circuitry underlying the ability to discriminate threat from safety and regulate emotional responses (2-4). Behavioral generalization also tends to increase over time, as memory precision for recent events gives way to more gist-like representations (5, 6). It then follows that stress-induced impairments in discriminating threat from safety coupled with a loss of memory precision might jointly influence the transition away from normal fear (i.e., highly specific to a known threat) toward overgeneralized fear. Here, we investigate how acute stress and the time between learning and test impacts fear generalization in humans.The effects of stress on the ability to regulate defensive behaviors have been detailed using Pavlovian threat (fear) conditioning tasks in humans and labo...

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“…Norepinephrine (NE), which is released widely in the brain during situations involving stress, emotional arousal, attention, and alertness (for reviews, see Rodrigues et al 2009;Sara and Bouret 2012;Raio and Phelps 2015) is one of the key neuromodulators that regulate the degree of learning and memory (Roozendaal et al 2009;Joëls et al 2011;McEwen 2012). The amygdala receives direct noradrenergic innervation from the locus coeruleus (LC) (Uematsu et al 2015), and β-adrenergic receptors (βARs) are highly expressed in LA (Farb et al 2010).…”

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confidence: 99%

Characterization of the amplificatory effect of norepinephrine in the acquisition of Pavlovian threat associations

et al. 2017

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The creation of auditory threat Pavlovian memory requires an initial learning stage in which a neutral conditioned stimulus (CS), such as a tone, is paired with an aversive one (US), such as a shock. In this phase, the CS acquires the capacity of predicting the occurrence of the US and therefore elicits conditioned defense responses. Norepinephrine (NE), through β-adrenergic receptors in the amygdala, enhances threat memory by facilitating the acquisition of the CS-US association, but the nature of this effect has not been described. Here we show that NE release, induced by the footshock of the first conditioning trial, promotes the subsequent enhancement of learning. Consequently, blocking NE transmission disrupts multitrial but not one-trial conditioning. We further found that increasing the time between the conditioning trials eliminates the amplificatory effect of NE. Similarly, an unsignaled footshock delivered in a separate context immediately before conditioning can enhance learning. These results help define the conditions under which NE should and should not be expected to alter threat processing and fill an important gap in the understanding of the neural processes relevant to the pathophysiology of stress and anxiety disorders.

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The influence of acute stress on the regulation of conditioned fear

Cited by 91 publications

References 221 publications

The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm

The birth, death and resurrection of avoidance: a reconceptualization of a troubled paradigm

Stress promotes generalization of older but not recent threat memories

Characterization of the amplificatory effect of norepinephrine in the acquisition of Pavlovian threat associations

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