Elsevier

Neurobiology of Learning and Memory

Volume 113, September 2014, Pages 149-156
Neurobiology of Learning and Memory

Stressor controllability modulates fear extinction in humans

https://doi.org/10.1016/j.nlm.2013.12.003Get rights and content

Abstract

Traumatic events are proposed to play a role in the development of anxiety disorders, however not all individuals exposed to extreme stress experience a pathological increase in fear. Recent studies in animal models suggest that the degree to which one is able to control an aversive experience is a critical factor determining its behavioral consequences. In this study, we examined whether stressor controllability modulates subsequent conditioned fear expression in humans. Participants were randomly assigned to an escapable stressor condition, a yoked inescapable stressor condition, or a control condition involving no stress exposure. One week later, all participants underwent fear conditioning, fear extinction, and a test of extinction retrieval the following day. Participants exposed to inescapable stress showed impaired fear extinction learning and increased fear expression the following day. In contrast, escapable stress improved fear extinction and prevented the spontaneous recovery of fear. Consistent with the bidirectional controllability effects previously reported in animal models, these results suggest that one’s degree of control over aversive experiences may be an important factor influencing the development of psychological resilience or vulnerability in humans.

Introduction

Instrumental control over an aversive experience, or the ability to influence its intensity, duration, onset, or termination, has long been recognized as a critical factor determining its behavioral and physiological impact on an organism (Brady, 1958, Mineka and Hendersen, 1985, Rotter, 1966, Seligman and Maier, 1967). The importance of stressor controllability was initially evidenced by the demonstration that exposure of an animal to inescapable shocks yielded impairment in subsequent avoidance learning that was not observed in animals exposed to identical but escapable shocks (Seligman & Maier, 1967). Subsequent studies revealed that uncontrollable stress exposure results in a host of other behavioral and physiological consequences including neophobia, reduced social interaction, decreased social dominance and aggression, heightened immobility in a forced swim task, decreased food and water consumption, formation of ulcers, and the potentiation of fear conditioning (see Maier & Watkins, 2005 for a review). As many of these behaviors mirror the symptoms of depression and anxiety, it has been proposed that exposure to uncontrollable stress may play an important role in the etiology of these disorders (Maier and Watkins, 2005, Weiss and Simson, 1986). While studies of uncontrollable stress reveal a broad array of deleterious effects, an equally striking result is that controllable stress yields none of these consequences, but in contrast, appears to promote behavioral resilience.

Stressor controllability effects are typically studied using a triadic design. One group of subjects is exposed to aversive reinforcement (such as electric shock) that they are able avoid or escape via the performance of an instrumental avoidance response. A second group is yoked to the first group, receiving reinforcement that is identical in intensity and duration, but that they cannot control through any action of their own. A third control group receives no exposure to the stressor. All three groups then take part in an identical generalization task through which the effects of prior experience are assessed. Importantly, this design enables the distinction between effects of stress exposure and the degree to which controllability modulates these effects. A host of recent studies employing this design have found that subjects exposed to escapable stress exhibit performance in the generalization task comparable or even superior to that of unstressed controls (Maier & Watkins, 2010). These findings suggest that the ability to exercise control over a stressor blunts its detrimental effects. Furthermore, several studies report that animals exposed to escapable stress fail to show the typical neurochemical and behavioral consequences of later inescapable stress (Amat et al., 2010, Amat et al., 2006, Williams and Maier, 1977), suggesting that escapable stress yields long-lasting neurobiological changes that immunize an organism to subsequent aversive experiences. Thus, contrary to the conventional notion that stress is physiologically harmful, these studies indicate that stressful experience may actually play a critical role in fostering resilience, provided that it is controllable.

Recent studies in rodents suggest that stressor controllability powerfully influences the expression of conditioned fear (Baratta et al., 2007, Cain and LeDoux, 2007, Rau et al., 2005). In one such study (Baratta et al., 2007), inescapable stress potentiated and escapable stress mitigated subsequent conditioned fear expression during fear acquisition, fear extinction learning, and a test of extinction retrieval, with respect to unstressed control animals. These findings suggest a mechanism by which individual variation in life experiences may modulate the expression of learned threat and safety associations; however, such effects have not presently been demonstrated in humans. In this study, we explore whether stressor controllability in humans yields the bidirectional effects on conditioned fear expression previously observed in animal models. As dysregulated fear expression is proposed to play a mechanistic role in the etiology of anxiety disorders (Lissek et al., 2005, Milad and Quirk, 2012, Mineka and Zinbarg, 2006), such a finding would implicate stressor controllability as an important experiential mechanism underlying psychological resilience or vulnerability.

Section snippets

Participants

Participants in both experiments were recruited at New York University. All participants gave their informed consent to take part in the study and were paid for their participation.

Experiment 1: One hundred and two participants (75 female), aged 18–50 (mean age = 22.8) were randomly assigned to one of three experimental conditions, an escapable stress (ES) condition, a yoked inescapable stress (IS) condition, or a control condition. Twenty-five participants in the ES condition who did not learn

Effects of variable shock level and number on fear expression

A yoked design ensured that each participant in an escapable stress (ES) and inescapable stress (IS) yoked pair received the same number of shocks during the stressor task. However, each individual was able to set the shock at a level that they deemed to be subjectively uncomfortable, and differences in these levels could potentially modulate fear expression. A one-way ANOVA revealed no significant group differences in shock levels (F(2,56) = .223; p = .801) between control (M = 41.1 V, SD = 9.03), ES (M

Discussion

Our data suggest that degree of instrumental control over a stressor modulates subsequent fear expression in humans. Consistent with reported findings in animal models (Baratta et al., 2007), we observed evidence of bidirectional effects of stressor controllability, with inescapable stress (IS) potentiating and escapable stress (ES) diminishing conditioned fear expression one week later. Whereas ES participants exhibited successful extinction and an absence of fear recovery, fear expression in

Acknowledgments

This work was supported by funding from the National Institute of Mental Health grants to E.A.P (Grant numbers MH062104 and MH080756) and by a National Science Foundation Graduate Research Fellowship to C.A.H. We thank Catherine Stevenson for assistance with participant testing.

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