Abstract
Although exposure-based treatments appear to be efficacious for the treatment of anxiety-related disorders, many individuals experience a renewal of the original fear response at follow-up. In an effort to prevent fear renewal, researchers have begun to use exposure of the conditioned stimulus in different contexts during extinction. Although studies continue to accumulate, showing that conducting exposure in multiple contexts buffers against the renewal of distress responses to fear-relevant stimuli, it remains unclear how conducting exposure in multiple contexts affects the renewal of distress responses to disgust-relevant stimuli. In the present study, participants (N = 52) were randomized to repeated presentations of disgust stimuli (vomiting in a toilet) in a single context or multiple contexts. Results revealed that those in the single context condition reported less distress after the exposure manipulation compared with the multiple context condition. Although there were no significant group differences in distress toward a novel disgust stimulus, the single context condition reported greater distress renewal than the multiple context condition. Furthermore, individuals in the multiple context condition showed significant reductions in distress at 1-week follow-up whereas distress in the single context condition remained stable. Subsequent analyses also provided moderate evidence for an effect of the disgust context manipulation on physiological arousal and disgust propensity, but not disgust-related behavioral avoidance. These findings offer preliminary evidence that renewal of distress toward disgust cues can be attenuated by conducting extinction in multiple contexts.
Disgust was initially described by Darwin (1872/1965) as “something revolting, primarily in relation to the sense of taste, as actually perceived or vividly imagined; and secondarily to anything which causes a similar feeling, through the sense of smell, touch and even of eyesight (p. 137).” Like many other emotions, disgust is recognizable across cultures (Eckman, 1992) with distinct facial expressions and specific cognitive, physiological, and behavioral manifestations (Eckman & Friesen, 1975; Izard, 1971). Although initially thought to facilitate the rejection of tainted foods (Rozin & Fallon, 1987), disgust has evolved to serve a broader defensive function. For example, the disease-avoidance model posit that certain stimuli (e.g., small animals, blood) have acquired an association with the spread of disease or contamination and this association leads to heightened disgust toward the object and subsequent avoidance (Matchett & Davey, 1991). Thus, whereas fear may function to prevent physical harm (Barlow, 2000, 2002), disgust appears to function largely to prevent the acquisition of disease (Haidt, McCauley, & Rozin, 1994; Rozin & Fallon, 1987).
Personality research has shown that there are marked individual differences in the extent to which disgust is experienced (Haidt et al., 1994). Clinical research has extended this work to show that “disgust propensity,” the personality trait characterized by the tendency to experience disgust in various contexts, may operate as a risk factor for anxiety-related disorders, including spider phobia (Matchett & Davey, 1991), snake phobia (Klieger & Siejak, 1997), blood-injection-injury (BII) phobia (Olatunji, Lohr, Sawchuk, & Westendorf, 2005), obsessive-compulsive disorder (OCD; Tolin, Worhunsky, & Maltby, 2006), health anxiety (Olatunji, 2009), posttraumatic stress disorder (Engelhard, Olatunji, & de Jong, 2011), and eating disorders (Davey, Buckland, Tantow, & Dallos, 1998). Although cognitive and behavioral treatments of these anxiety disorders have had remarkable success, many individuals do not achieve clinically significant improvement, with 33% to 50% experiencing a relapse of fear at follow-up (Boschen, Neumann, & Waters, 2009). These less than optimal outcomes may be partially due to the observation that exposure-based interventions are designed to target fear and not necessarily disgust. Theoretical conceptualizations contend that while disgust is easily acquired, it is not easily extinguished (Rozin & Fallon, 1987; Rozin, Haidt, & McCauley, 2000; Woody & Teachman, 2000). Indeed, research examining spider phobic (Smits, Telch, & Randall, 2002) and BII phobic individuals (Olatunji, Lohr, Sawchuk, & Tolin, 2007) found that while phobic individuals showed significant declines in fear and disgust during repeated exposure, the decay slope for fear was significantly greater than for disgust. This finding suggests that disgust may be more resistant to extinction than fear. Therefore, the inclusion of exposure trials designed specifically to desensitize disgust may yield better treatment outcomes for anxiety disorders (Woody & Teachman, 2000).
Targeting disgust more efficiently during treatment may require some consideration of its renewal effect. Renewal refers to the phenomenon in which a change of context after extinction can cause a robust return of conditioned responding (Boschen et al., 2009; Bouton & Bolles, 1979; Bouton & King, 1983). For example, Bouton and Ricker (1994) found that when acquisition and extinction took place in the same context, introduction of the conditioned stimuli in a novel context resulted in a return of conditioned responding. This finding suggests that the retrieval of extinction is context dependent such that simply leaving the therapeutic context may be sufficient to evoke a return of phobic responding even after successful exposure. To prevent the renewal of fear, researchers have begun to use exposure of the conditioned stimulus in different contexts during extinction. It has been posited that conducting exposure in multiple contexts maximizes the generalizability of habituation (Bouton, 2002). It is now widely accepted that repeated exposure to a stimulus does not simply overwrite or destroy the original fear learning (Bouton, Garcia-Gutierrez, Zilski, & Moody, 2006; Rescorla, 2001). Instead, individuals learn new meanings of the feared stimulus (Lang, Craske, & Bjork, 1999) or how to inhibit or suppress fear itself (Bouton, 2002; Bouton et al., 2006). Thus, by varying the context in which exposure takes place, “inhibition learning” is strengthened by promoting the learning of multiple retrieval cues for coping. In support of this notion, Rowe and Craske (1998) showed that while spider-phobic individuals who were exposed to a single spider during exposure had a return of fear when presented with a novel spider, this return was reduced when multiple stimulus examples were used during exposure.
Although studies continue to accumulate showing that conducting exposure in multiple contexts buffers against the renewal of phobic responding to fear-relevant stimuli (Vansteenwegen et al., 2007), it is unclear how conducting exposure in multiple contexts affects the renewal of distress responses to disgust-relevant stimuli. Given prior research implicating heightened generalized disgust sensitivity in several anxiety-related disorders (see Olatunji & Sawchuk, 2005, for a review), exposure-based interventions which provide multiple retrieval cues that promote maximal generalizability to disgust-relevant stimuli could potentially result in better outcomes. Accordingly, the present study examines the effects of repeated exposure to disgust-relevant stimuli in multiple contexts versus a single context on reductions in distress, behavioral avoidance, and physiological arousal in an unselected sample. It was predicted that repeated exposure to a disgusting stimulus in a single context (e.g., same person vomiting in the same toilet) or multiple contexts (e.g., different people vomiting in different toilets) would reduce distress, behavioral avoidance, and physiological arousal. However, when confronted with a novel disgust stimulus, a stronger renewal effect would be observed for the single context group compared with the multiple context group. In addition, it was hypothesized that these effects would be observed at a 1-week follow-up.
Method
Participants
A total of 52 unselected undergraduates (90% female), with a mean age of 19.83 (SD = 1.28; range = 18-24), were recruited to participate. Participants were 73% Caucasian, 11% African American, 2% Asian/Pacific Islander, 10% Hispanic, and 4% identified themselves as multiethnic.
Measure
The Disgust Propensity and Sensitivity Scale–Revised (DPSS-R; van Overveld, de Jong, Peters, Cavanagh, & Davey, 2006) is a 16-item measure designed to assess the frequency of disgust experiences (Disgust Propensity) and the emotional impact of disgust experiences (Disgust Sensitivity). Participants rate their agreement with each item on a scale ranging from 1 (never) to 5 (always). The Disgust Propensity subscale, with alpha coefficients ranging from .71 to .73, was used in the present study.
Disgust Exposure Stimuli
Based on prior research (Olatunji, Haidt, McKay, & David, 2008), four clearly distinguishable videos containing people vomiting into toilets were selected to serve as disgust stimuli in the experiment. Vomit was selected for the present study given that such bodily secretions are the most widely reported elicitors of the disgust emotion (Curtis & Biran, 2001). In addition, previous research using a similar vomit induction paradigm reported significant increases in subjective experiences of disgust (Olatunji, Ciesielski, Wolitzky-Taylor, Wentworth, & Viar, 2012).
Behavioral Avoidance Task (BAT)
A BAT was administered to assess the emotional and behavioral features relating to disgust. The BAT consisted of two steps which participants were asked to complete. The first asked the participant to spit into a paper cup and the second step asked the participant to consume the spit from the cup. Participants could receive a score of 0 (no steps completed), 1 (only spit into the cup), or 2 (spit into the cup and consumed the spit). This task has been found to be associated with core disgust in previous research (Olatunji et al., 2008). Given that the disgust exposure stimuli (e.g., vomit videos) used in the present study also represents core disgust (Chapman & Anderson, in press; Olatunji et al., 2008), it was deemed an appropriate behavioral measure of disgust proneness to match the exposure stimuli. The oral focus symmetry between the exposure stimuli (vomit) and behavioral outcome (spit) may also lead to great sensitivity to the experimental manipulation.
Physiological Assessment
Previous research examining the effects of multiple contexts on habituation (Vansteenwegen et al., 2007) found that skin conductance responses (SCRs) were sensitive to attenuated renewal as a function of extinction in multiple contexts. Accordingly electrodermal activity was also assessed in the present study. Assessment of electrodermal activity was also used to provide an assessment of the hypothesized renewal effect beyond just self-report. Electrodermal activity in the current study was recorded using unshielded 8-mm Ag-AgCl electrodes filled with isotonic gel and attached to the middle phalanx of the index and middle fingers of the right hand. Signals were recorded at 200 Hz using the Biopac MP35 system with Acknowledge software (BIOPAC Systems Inc., 2007). The SCRs were also analyzed using Acknowledge software.
Procedure
Following the informed consent process, participants completed the Propensity subscale of the DPSS-R and were randomly assigned to a single context (n = 26) or multiple context (n = 26) condition. All participants received 14 presentations of a 30-s video clip with intertrial intervals (ITIs) of 30 s (blank screen). Participants were instructed to carefully watch the videotapes. During the ITI, participants indicated on two 100-point rating scales how anxious the video made them feel and how disgusted the video made them feel. For all participants, the first presentation included a person vomiting in Context A (pretest trial). Then the single context group received 11 presentations of the same Context A video, whereas participants in the multiple context group received three presentations of Context A video, four Context B videos, and four Context C videos in the following order: BBACBACCCBA. This sequence was determined randomly and was the same for all participants in the multiple context condition. Following the exposure trials, all participants were presented with the Context A video (posttest trial) and then a novel Context D video (Week 1 novel trial). Skin conductance (SC) was collected during presentation of the video clips. Following the video exposures, participants completed the measure of disgust propensity and the BAT. At the 1-week follow-up, participants were presented with the same novel Context D video as a retention trial (Week 2 novel retention). Following the Week 2 novel retention trial, participants completed the measure of disgust propensity and BAT. An overview of the course of the exposure phase as well as a scheme of the course of one trial is presented in Figure 1.

The course of all trials (upper panel) and a single trial (lower panel) during the experiment for the single context and multiple context groups.
Results
Participant Characteristics and Distress Ratings
As shown in Table 1, there were no significant group differences in age, gender, ethnicity, or self-report measures. Given significantly high correlations between verbal ratings of anxiety and disgust ratings taken during the exposure ITIs for the pretest trial (r = .80), posttest trial (r = .78), Week 1 novel trial (r = .67), and the Week 2 novel retention trial (r = .77), these ratings were averaged to form a composite distress rating.
Group Means (Standard Deviations) of Study Measures Among Single Context and Multiple Context Participants
Note: BAT = behavioral avoidance task.
Effect of Context on Distress Reduction
Distress reduction was defined by group differences at post exposure. Given the unexpected significant group differences in distress ratings during the pretest trial, pretest distress was entered as a covariate. An ANCOVA revealed significantly lower distress among the single context group (M = 25.90, SD = 23.80) at post exposure compared with the multiple context condition (M = 33.12, SD = 25.00); F(1, 48) = 11.31, p < .003, partial η2 = .19.
Effect of Context on Distress Renewal
Distress renewal was defined by the change in ratings from posttest (Video Context A) to a novel context (Video Context D). A 2 (time; Week 1 post vs. Week 1 novel) × 2 (condition: single context vs. multiple context) ANCOVA was then conducted for distress ratings with pretest distress as a covariate. As depicted in Figure 2, results yielded a significant main effect of time, F(1, 48) = 5.99, p < .03, partial η2= .11, and condition, F(1, 48) = 8.15, p < .007, partial η 2 = .15, that was qualified by a significant time by condition interaction, F(1, 48) = 4.31, p < .05, partial η2= .08. Paired t tests revealed a significance increase from Week 1 post to Week 1 novel for the single context group, t(24) = 4.95, p = 001, and the multiple context group, t(25) = 3.54, p = 002. However, follow-up tests comparing the magnitude of change (as index by a difference score from Week 1 post to Week 1 novel) from Week 1 post to Week 1 novel revealed that renewal of distress was significantly greater among the single context group (M = 20.66, SD = 20.87) compared with the multiple context condition (M = 9.13, SD = 13.14), t(49) = 2.37, p < .03.

Renewal of distress from Week 1 posttest trial to Week 1 novel test trial with pretest distress rating as a covariate
Effect of Context on Distress Retention
Distress retention was defined by the change in ratings from Week 1 novel trial (Video Context D) to Week 2 novel retention trial (Video Context D). A 2 (time; Week 1 novel trial vs. Week 2 novel retention trial) × 2 (condition: single context vs. multiple context) ANCOVA was then conducted with pretest distress rating as a covariate. As depicted in Figure 3, results yielded only a significant time by condition interaction, F(1, 48) = 7.17, p = .01, partial η2= .13. Paired t tests revealed no significant change in the level of distress reported by the single context group, t(24) = .59, p = .55. However, the multiple context group reported significantly less distress from Week 1 novel to Week 2 novel, t(25) = 3.91, p < .002. Follow-up analyses comparing the magnitude of change (as index by a difference score from Week 1 novel to Week 1 novel) from Week 1 novel to Week 2 novel also revealed a significant reduction in distress for the multiple context group (M = −12.98, SD = 16.91) compared with the single context group (M = −1.96, SD = 16.46); t(49) = 2.36, p < .03.

Change in distress ratings for same Context D novel video at Week 1 and 1-week follow-up among single context and multiple context conditions
Effect of Context on Physiological Arousal
In accordance with previous research examining the effect of context on physiological arousal (Vansteenwegen et al., 2007), SCRs were visually inspected and corrected for movement artifacts before they were analyzed statistically. The “tonic” SC value, the average SC across full exposure presentation (~810 s), was calculated for each participant to serve as a baseline (SC0). To calculate phasic fluctuations of SC as a function of exposure (e.g., Galvanic Skin Conductance [GSR]), the baseline (SC0) was subtracted from the mean SC of each 30-s trial (SC1). This raw GSR was range-corrected using the largest and smallest responses observed during all video presentations (Lykken, Rose, Luther, & Maley, 1966; Lykken & Venables, 1971). The corrected responses were then subjected to a square root transformation to normalize the distribution prior to statistical analysis. SCR means are shown in Figure 4. 1 Change scores were computed for the full sample and planned comparisons revealed only a significant between-group difference from Week 1 post to Week 1 novel, t(45) = −2.14, p < .05, suggesting that the single context group experienced a greater increase in arousal in response to the novel video whereas the multiple context showed no change.

Mean amplitudes of the skin conductance responses (SCRs) at pretest, posttest, novel context, and Week 2 novel retention trial for the single context and multiple context groups
Effects of Context on Disgust Propensity
A 3 (time; preexposure, postexposure, Week 2 follow-up) × 2 (condition: single context vs. multiple context) mixed-model ANOVA with the propensity subscale of the DPSS-R as the outcome variable was then conducted to assess change in disgust proneness as a function of the exposure manipulation. The results yielded a significant main effect of time, F(2, 50) = 4.97, p = .009, partial η2= .80, that was qualified by a significant Time × Condition interaction, F(2, 50) = 6.01, p = .003, partial η2= .87. Follow-up tests revealed a significant increase in disgust propensity for the single context group from preexposure to postexposure, t(25) = −3.05, p < .004, but no significant difference from postexposure to Week 2 (p < .05). In contrast, the multiple context group showed no significant change in disgust propensity from preexposure to postexposure or from postexposure to Week 2 (ps > .05).
Effect of Context on Behavioral Avoidance
A 2 (time; Week 1, Week 2) × 2 (condition: single context vs. multiple context) mixed-model ANOVA was conducted to examine the effect of context on behavioral avoidance. Results did not yield a significant main effect of time, F(1, 50) = 1.30, p = .26, partial η2= .03, or condition, F(1, 50) = .89, p = .35, partial η2= .02.
Discussion
Although disgust has been implicated in the etiology and maintenance of several anxiety-related disorders (Olatunji & Sawchuk, 2005), much remains unknown about how disgust operates in the context of exposure-based treatments. Prior research has shown that disgust may be less resistant to extinction than fear during repeated exposure (Olatunji, Lohr, Sawchuk, & Tolin, 2007; Smits et al., 2002), potentially making it more likely to return even after successful treatment. There is experimental evidence suggesting the exposure to the conditioned stimulus in different contexts during extinction may prevent the renewal of distress in response to fear-relevant stimuli (Bouton, 2002). However, it is unclear whether varying the context of exposure during extinction may also prevent the renewal of distress in response to disgust-relevant stimuli disgust. To address this gap in the literature, the present investigation examined the effect of varying the context in which disgust stimuli is presented during repeated exposure on habituation in an unselected sample. The findings revealed significantly lower ratings of distress at posttest for the single context condition compared with the multiple context condition. This finding is not particularly surprising given that the single context group is presented with twelve 30-s trials of the target stimulus whereas the multiple context condition is exposed to only four 30-s trials of the target stimulus. With the presentation of different stimuli during extinction, there is less repeated presentation of the same stimulus needed for habituation.
Despite less emotional reactivity to the disgust stimulus at posttest, the present study hypothesized that the single context condition would experience more renewal (a return of the original distress response), compared with the multiple context condition, when confronted with a novel disgust stimulus. The findings revealed that although both groups reported an increase in distress ratings when presented with a novel disgust stimulus, those in the multiple context condition showed less renewal than those in the single context condition. This finding is consistent with previous research on animals and humans examining the effectiveness of using multiple contexts to reduce fear renewal (Bouton, 2002; Vansteenwegen et al., 2007). Although the two experimental groups showed no significant differences in distress ratings for the novel context trial, the greater shift in distress ratings experienced by the single context group may have important clinical implications. For example, it is now well accepted that exposure does not simply overwrite the original affective response but rather produces a new “inhibition” pathway in which the individuals learn to inhibit the original response (Boschen et al., 2009). Thus, greater renewal or reactivity may cause a reinstatement of the original affective response thereby weakening the fragile structure of the new inhibitory pathway. The large shift in distress to the disgust-relevant stimuli may trigger reinstatement through a variety of mechanisms including increased salience in disgust responding.
The present study also found that those in the multiple context condition showed a significant reduction in distress levels during presentation of the same novel context video at a 1-week follow-up, whereas those in the single context condition reported no change in their distress ratings. According to Schmidt and Bjork (1992), the effectiveness of learning is dependent on how well the learning is retained and generalized to related contexts. Variation of context during exposure may result in less distress at follow-up by requiring retrieval and organization of different information with the presentation of each new disgust stimulus. The finding that the benefit of varying the context in which disgust stimuli is presented is mostly observed at follow-up rather than immediately following extinction learning may be partially accounted for by means of reconsolidation. The reconsolidation hypothesis suggests that memories are strengthened each time they are retrieved making the memory easier to recall (Dudai, 2006; Sara & Hars, 2006). In the current study, the use of multiple contexts during extinction provides multiple disgust retrieval cues following exposure. Thus, each time one of these multiple cues is encountered in a different context, the new inhibitory memory may be retrieved and reconsolidated, reinforcing the newly learned pathway.
The current study also examined the effect of context variation on disgust propensity and behavioral avoidance. Although the context manipulation did not have any observed effect on behavioral avoidance, significant group differences did emerge for disgust propensity. Disgust propensity has been described as a personality trait that is relatively stable (Olatunji & Cisler, 2009; Olatunji, Cisler, Deacon, Connolly, & Lohr, 2007; van Overveld et al., 2006). However, the present study found that those in the single context condition reported an increase in disgust propensity following the exposure manipulation whereas the multiple context condition reported no change. Although these findings suggest that disgust propensity may be variable under some circumstances, the mechanisms that may account for this effect are unclear. For example, it is unclear in the present study whether exposure to disgust stimuli in a single context increases disgust proneness or whether exposure to disgust stimuli in multiple contexts protects against an increase in disgust propensity. The moderate decrease in physiological reactivity among the multiple context group coupled with slightly less renewal during exposure and reduced distress at follow-up, lend some evidence that the latter explanation may be more viable. If the assumption that context variation during disgust exposure protects against an increase in disgust propensity is confirmed in future research, it may be possible to provide early interventions that prevent the emergence of anxiety disorders in which disgust propensity has been implicated.
The current investigation is among the first to examine whether varying context facilitates habituation to disgust-relevant stimuli. Results show promising effects for reducing renewal of distress toward disgust-relevant stimuli when using multiple contexts during repeated exposures. Animal models and preliminary work with humans (Bouton & Ricker, 1994; Rowe & Craske, 1998) posit that learning that takes place during extinction may not generalize to occasions outside the therapeutic context. Accordingly, Bouton and Swartzentruber (1991) encouraged an expanded view of “context” by including any background event or stimulus in which target learning and memory events are embedded (e.g., time, location, stimulus features). This definition implies that the stimulus itself may serve as a contextual retrieval cue, such that when the stimulus itself changes, renewal can occur (Rowe & Craske, 1998). The present findings are largely consistent with this operational definition of context. Indeed, variation of the disgust stimulus itself served as the manipulation of context in the current study and this manipulation was quite subtle (different young males vomiting in different toilets). Even with such a conservative context manipulation, greater renewal (and retention of that renewal a week later) was observed among the single context condition. Therefore, simply varying features of disgust-relevant stimuli during the extinction process may have therapeutic effects.
The present findings complement previous research on fear renewal by offering preliminary evidence that renewal of disgust can also be attenuated by conducting extinction in multiple contexts. However, there are several notable limitations. Although significant effects of context variation were revealed despite the subtle manipulation, future studies should use a wider range of contexts with great diversity to optimize these effects. More specificity in assessment modality may also reveal more robust context effects. For example, SCRs may not be an ideal physiological marker for disgust responding, especially given that disgust may be more reflective of parasympathetic activation (Levenson, 1992). Indeed, the SC findings of the present study were much more modest than those of the verbal report indices. Prior research has shown that facial electromyography (EMG) appears to correlate well with disgust responding (Olatunji et al., 2008), and this physiological parameter may ultimately yield more sensitivity to exposure-based context effects.
One interpretation of the present findings is that varying context does not influence behavioral indices of disgust. However, the restricted range of the BAT is also a limitation of the present study. Indeed, participants completed nearly all the steps of the BATs at preassessment, making it insensitive to detecting exposure-based context effects on behavior. Future research along these lines should use BATs that allow for detecting greater variability in behavioral responding as well as BATs that assess a broader range of disgust domains. Such assessment considerations may facilitate examination of the benefits of context variation during exposure among patients with anxiety disorders. Recent research suggests that targeting disgust may be therapeutic in the treatment of some anxiety disorders (Olatunji, Tart, Ciesielski, McGrath, & Smits, 2011). Varying the context of disgust during exposure may be a useful approach for facilitating disgust tolerance in anxiety disorders that are marked by excessive disgust sensitivity.
Footnotes
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
Preparation of this manuscript was supported in part by a training grant from the National Institute of Mental Health (T32-MH018921-21A1).
