Sleep promotes consolidation and generalization of extinction learning in simulated exposure therapy for spider fear

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Abstract

Simulated exposure therapy for spider phobia served as a clinically naturalistic model to study effects of sleep on extinction. Spider-fearing, young adult women (N = 66), instrumented for skin conductance response (SCR), heart rate acceleration (HRA) and corrugator electromyography (EMG), viewed 14 identical 1-min videos of a behaving spider before a 12-hr delay containing a normal night's Sleep (N = 20) or continuous daytime Wake (N = 23), or a 2-hr delay of continuous wake in the Morning (N = 11) or Evening (N = 12). Following the delay, all groups viewed this same video 6 times followed by six 1-min videos of a novel spider. After each video, participants rated disgust, fearfulness and unpleasantness. In all 4 groups, all measures except corrugator EMG diminished across Session 1 (extinction learning) and, excepting SCR to a sudden noise, increased from the old to novel spider in Session 2. In Wake only, summed subjective ratings and SCR to the old spider significantly increased across the delay (extinction loss) and were greater for the novel vs. the old spider when it was equally novel at the beginning of Session 1 (sensitization). In Sleep only, SCR to a sudden noise decreased across the inter-session delay (extinction augmentation) and, along with HRA, was lower to the novel spider than initially to the old spider in Session 1 (extinction generalization). None of the above differentiated Morning and Evening groups suggesting that intervening sleep, rather than time-of-testing, produced differences between Sleep and Wake. Thus, sleep following exposure therapy may promote retention and generalization of extinction learning.

Introduction

Abnormal expression of fear, as occurs in anxiety disorders such as post-traumatic stress disorder (PTSD) and specific phobia, may result from abnormally strong fear conditioning (Armfield, 2006; Lissek et al., 2005; Mineka and Oehlberg, 2008; Orr et al., 2000), deficiency of inhibitory mechanisms that normally moderate fear expression (Craske et al., 2008; Hofmann, 2008; Milad et al., 2006), or both. Key among such inhibitory processes is extinction — learning that a once-feared object or event is no longer dangerous (Milad et al., 2006). Rather than erasing a fearful memory, extinction forms a new ”safety memory” that competes with the fear memory when the once-feared object or event is re-encountered (Hermans et al., 2006; Quirk and Mueller, 2008).

Formation of such therapeutic extinction memories is the neurocognitive basis for the efficacy of exposure therapy, a first-line behavioral treatment for anxiety disorders (Craske et al., 2008; McNally, 2007). In order for exposure therapy to be successful, consolidation and retention of extinction learning acquired during therapy is essential (Craske et al., 2008). In addition, such learning must generalize in order to ensure that the reduction of fearful responding to specific cues in treatment will extend to stimuli encountered outside the therapist's office (Rowe and Craske, 1998; Vansteenwegen et al., 2007).

Using an experimental fear-conditioning paradigm (Milad et al., 2007), normal sleep has been shown to promote the generalization of extinction memories (Pace-Schott et al., 2009). However, unlike such experimentally induced de-novo fears, anxiety disorders are associated with long-standing fears that have complex, multi-factorial origins and perpetuating factors (Armfield, 2006). Specific phobias, such as spider phobia, are highly prevalent, mild anxiety disorders (LeBeau et al., 2010; Lissek et al., 2007) in which treatment strategies, such as exposure therapy, can be studied in a non-clinical setting (e.g., Vansteenwegen et al., 2007).

Sleep enhances consolidation of emotional memory (reviewed in Walker, 2009). Here we characterize the effect of sleep on the retention and generalization of a specific emotional memory-- the extinction of spider fear produced by simulated exposure therapy. We hypothesized that sleep following simulated exposure therapy in spider-phobic subjects would lead to greater retention of fear extinction for the spider to which they were repeatedly exposed. In addition, we predicted that sleep would enhance generalization of this extinction memory to a novel spider.

Section snippets

Participants

Participants were 66 females (18–28 yrs, mean = 19.9) with significant fear of spiders operationally defined using thresholds of 80 on the Fear of Spiders Questionnaire [FSQ (Szymanski and O'Donohue, 1995)] and 15 on the Spider Phobia Questionnaire [SPQ (Klorman et al., 1974)]. Previous research has determined that these thresholds reflect significant fear of spiders (Muris and Merckelbach, 1996; Rodriguez et al., 1999; Guastella et al., 2007; Vansteenwegen et al., 2007). The FSQ was included

Comparison of group characteristics

As shown in Table 1 and Supplementary results, the four groups showed highly similar spider fear, habitual sleep and psychological trait measures. All groups averaged above 100 on the FSQ and 20 on the SPQ (Table 1) indicative of a highly spider-fearful sample (Muris and Merckelbach, 1996). Notably, when Group main effects were present (NEO-PI-R Extraversion, sleep duration on night before S1), this reflected one control group differing from the remaining groups rather than differences between

Discussion

In spider-fearing young adult women, simulated exposure therapy acutely diminished both subjective and physiological measures of negative affect. Following a 12-hr delay, those exposed in the evening, who then slept, showed better extinction retention and generalization when tested in the morning than those exposed in the morning who remained awake until tested in the evening. The majority of findings remained unchanged after exclusion of participants with potentially confounding factors (see

Conclusions

A period of sleep following simulated exposure therapy resulted in better retention and generalization of subjective and physiological responses to phobic stimuli. Sleep may confer protection from sensitization to such stimuli. Findings encourage further clinical investigation into the timing of exposure therapy in relation to sleep.

Role of funding source

NIA R00AG029710 provided salary support for Edward F. Pace-Schott and Rebecca M.C. Spencer, Ph.D. as well as equipment and materials support for the study. NIMH R21MH090357 provided salary support for Edward F. Pace-Schott.

Contributors

Edward F. Pace-Schott designed experiments, designed stimuli, collected and analyzed data, and wrote manuscript. Patrick W. Verga collected and analyzed data. Tobias S. Bennett designed stimuli and collected and analyzed data. Rebecca M.C. Spencer analyzed data and wrote manuscript.

Conflict of interest

None of the authors report any potential conflicts of interest.

Acknowledgments

The authors thank Scott Orr, Ph.D. scientific and technical advice, Philip Cusimano for technical advice, and Shanzay Haider, Shannon McKeon, Joanna Hong, Jessica Green and Lana Kim for research assistance.

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