1 s2.0 S0272735808001347 Main

Clinical Psychology Review 29 (2009) 34–46
Contents lists available at ScienceDirect
Clinical Psychology Review
Disgust, fear, and the anxiety disorders: A critical review

Josh M. Cisler a,⁎, Bunmi O. Olatunji b, Jeffrey M. Lohr a
a
University of Arkansas, United States
b
Vanderbilt University, United States
a r t i c l e i n f o a b s t r a c t
Article history: Anxiety disorders have traditionally been conceptualized as reflecting the emotions of fear and anxiety. A
Received 2 January 2008 developing program of research demonstrates a relation between disgust and three specific anxiety
Received in revised form 22 June 2008 disorders: blood-injection-injury (BII) phobia, spider phobia, and contamination-related obsessive–
Accepted 19 September 2008
compulsive disorder (OCD). This review serves three purposes. First, the authors review the response
patterns predicted to be observed if the emotional response in these disorders involved disgust versus fear.
Keywords:
Fear
The review suggests specific response patterns that characterize disgust and fear in the domains of heart rate,
Disgust facial expression, neural activity, and cognitive processes. Second, the authors review extant research
Contamination fear employing measures of these domains in spider phobia, BII phobia, and contamination-related OCD. The
Spider phobia evidence suggests that both fear and disgust characterize each of these disorders, but the magnitude at
Blood-injection-injury which the emotions characterize the disorders may depend on the response domain measured. For example,
disgust may be more involved in spider phobia in appraisals and facial expression, but less involved in neural
correlates or heart rate domains. Third, the authors suggest guidelines for future research, including
concurrent use of specific measures as well as examining whether the different emotions in different
response domains respond to similar interventions (e.g., exposure).
© 2008 Elsevier Ltd. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
2. Distinguishing disgust from fear . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
2.1. Theoretical background of operational definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
2.2. Heart rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
2.3. Neural correlates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
2.4. Facial expression. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
2.5. Cognitive processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
2.6. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
3. A critical review of disgust-related anxiety research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
3.1. Spider phobia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.1.1. Facial expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.1.2. Heart rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.1.3. Neural substrate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.1.4. Cognitive processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.1.5. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
3.2. BII phobia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
3.2.1. Facial expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
3.2.2. Heart rate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
3.2.3. Neural substrate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
3.2.5. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
3.3. Contamination-related OCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
3.3.1. Facial expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
⁎ Corresponding author. 216 Memorial Hall, Psychology Department, University of Arkansas, 72701, United States.
E-mail address: [email protected] (J.M. Cisler).
0272-7358/$ – see front matter © 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cpr.2008.09.007
J.M. Cisler et al. / Clinical Psychology Review 29 (2009) 34–46 35
3.3.2. Heart rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42

3.3.3. Neural substrate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
3.3.5. Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
3.4. General summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
4. Future directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
4.1. Concurrent use of emotion indicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
4.2. Investigate whether fear and disgust across response domains respond to similar types of interventions . . . . . . . . . . . . . . . . 44
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
Acknowledgement. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
1. Introduction maintained. Fourth, this line of inquiry may begin to suggest

therapeutic techniques to enhance treatment efficacy. For example,
An anxiety disorder is typically conceptualized as an interrelated extant treatments of specific phobia are efficacious (Choy, Fyer, &
pattern of responding that reflects two emotions; fear and anxiety Lipsitz, 2007; Wolitzky-Taylor, Horowitz, Powers, & Telch, 2008), yet
(Barlow, 2002, 2000; Rosen & Schulkin, 1998). Recent research effect sizes tend to be variable (Wolitzky-Taylor et al., 2008). If disgust
suggests that fear is an organism's defensive response to a present does play a prominent role in these anxiety disorders, the inclusion of
threat, whereas anxiety is an organism's preparatory response to procedures to target disgust may lead to more consistent treatment
contexts in which a threat may occur (Barlow, 2002; Davis, 2006; effects.
Lang, Davis, & Öhman, 2000; Quinn & Fanselow, 2006; Walker & Davis, The purpose of the current review is to examine the relative
1997). Although research investigating the etiology and maintenance contributions of fear and disgust in spider phobia, BII phobia, and
processes of particular anxiety disorders has focused primarily on contamination-related OCD. This purpose is specifically pursued by
these two emotions, recent research suggests that some anxiety examining the degree to which the emotional response towards
disorders (e.g., spider phobia, contamination-related obsessive– disorder-relevant stimuli in these anxiety disorders is characteristic of
compulsive disorder, blood-injury-injection phobia) may be asso- disgust or fear. For example, to what degree does the emotional
ciated with an additional emotion, disgust (Woody & Teachman, response towards spiders in spider phobia resemble a disgust
2000). Indeed, in clinical (McKay, 2006; Olatunji & Sawchuk, 2005; response? To what degree does the emotional response towards
Woody & Teachman, 2000) and basic research (Rozin & Fallon, 1987; spiders in spider phobia resemble a fear response? The review focuses
Rozin, Fallon, & Augustoni-Ziskind, 1984; Rozin, Fallon, & Mandell, on the relative contributions of disgust and fear in the emotional
1984), interest on disgust has grown immensely over the past response of these disorders because of the common conceptualization
20 years, prompting McNally (2002) to announce ‘disgust has arrived.’ of these disorders as fear and anxiety based (e.g., Antony & Barlow,
Given the wealth of data collected on disgust and fear in spider 2002; Rachman, 2006). Moreover, treatments of these disorders based
phobia, blood-injection-injury (BII) phobia, and contamination-related on fear and anxiety conceptualizations do not include procedures to
obsessive–compulsive disorder (OCD), it is necessary to examine the target disgust (e.g., see Öst et al.'s treatments for spider and BII phobia;
relative contributions of disgust and fear in these disorders. Elucidating Öst, Fellenious, & Sterner, 1991; Öst, 1997). If disgust is indeed a part of
the magnitude to which disgust and fear contribute to these anxiety the emotional response in these disorders, conceptualizations and
disorders will serve several purposes. First, this line of inquiry critically treatments of the disorders may need to be modified in order to
examines the growing program of research on disgust and certain account for disgust. The current review does not examine the relative
anxiety disorders (e.g., Olatunji & McKay, 2007; Olatunji & Sawchuk, contributions of disgust and fear in the etiology of these anxiety
2005; Woody & Teachman, 2000). If disgust functions in anxiety disorders. Although the role of disgust in the etiology of these
disorders to a comparable magnitude as fear, this growing program of disorders is theoretically interesting in its own right (see, for example,
research may develop into a viable paradigm by which particular an interesting study by Muris et al., 2008), the literature on the role of
anxiety disorders (e.g., spider phobia) are conceptualized. Second, this disgust in the etiology of these anxiety disorders is currently limited
line of inquiry critically examines previous assertions that disgust may and conclusions would be difficult to derive. The review is focused on
play a minor role compared to fear in these anxiety disorders (Edwards spider phobia, BII phobia, and contamination-related OCD because
& Salkovskis, 2006; Rachman, 2006; Thorpe & Salkovskis, 1998). For they have received the most empirical and theoretical attention
example, Edwards and Salkovskis (2006) found that presenting vomit (Olatunji & Sawchuk, 2005; Woody & Teachman, 2000).
(i.e., a disgust stimulus) during exposure therapy for spider phobia did There are three sections to the current review. First, elucidating the
not lead to a return of self-reported anxiety towards spiders. These relative contributions of disgust and fear necessitates an elucidation of
authors concluded that “although disgust clearly can be part of the the specific response topographies expected to be observed if the
emotional reaction to some phobic stimuli, the presents results suggest emotional response is fear or disgust. These specific response
that this reaction may be secondary to fear” (p. 69). Critical examination components then directly facilitate an examination of the relative
of this competing assertion is important in the development of the contributions of disgust and fear. That is, if the emotional response
disgust program of research. Third, this line of inquiry would facilitate involves disgust, it follows that disgust specific response domains
the development of theories by which these disorders are developed would be observed; if the emotional response involves fear, it follows
and maintained. For example, Antony and Barlow's (2002, p.408) model that fear specific response domains would be observed. Second,
of the development of specific phobia does not, at least explicitly, research employing specific measures of disgust and fear in spider
include a component of disgust. Conversely, Armfield's (2006) recent phobia, BII phobia, and contamination-related OCD is critically
theory of cognitive vulnerabilities towards developing fear posits that examined in order to elucidate the relative magnitude to which the
perceptions of disgust are a pivotal factor in the development of fear emotional response reflects fear and disgust. Finally, guidelines for
towards particular objects/situations. Elucidation of the relative con- future research investigating the relation between disgust and
tributions of disgust and fear in these disorders would facilitate anxiety-related pathology are put forward to facilitate a progressive
comprehensive models of how these disorders are developed and program of investigation.
36 J.M. Cisler et al. / Clinical Psychology Review 29 (2009) 34–46
2. Distinguishing disgust from fear produce specific response topographies: physiology, neural substrate,
facial expressions, and appraisals/cognitive processes. The following
2.1. Theoretical background of operational definitions sections review basic research on the distinctness of the topography of
disgust and fear responses in the domains of heart rate, neural
Fear is characterized by an organism's defensive response to substrate, facial expression, and appraisals/cognitive processes. Again,
imminent threat (Barlow, 2002, 2000; Quinn & Fanselow; 2006). At the purpose of the review is to elucidate the expected response
the phenomenological level, fear is typically defined by three response topographies if the emotion is fear or disgust (e.g., what is the
systems (Kozak & Miller, 1982; Lang, 1968; Lipp, 2006): overt behavior, expected heart rate topography if the emotion is disgust?).
verbal-cognitive, and physiological. For example, an individual's fear
of spiders may be exhibited by inhibited approach towards a spider in 2.2. Heart rate
a behavioral approach task (i.e., overt behavioral system), verbally
reported subjective units of distress (SUDs) ratings in the presence of Ekman, Levenson, and Friesen (1983) directed participants to
spiders or attentional bias towards spiders (i.e., verbal-cognitive contort their face into emotional configurations (i.e., directed facial
system), and a heightened heart rate in the presence of spiders (i.e., action task) or asked participants to relive particularly salient
physiological system). emotional experiences in their past (i.e., relived emotions task).
Disgust is characterized by a revulsion response towards potential Regardless of task, results revealed greater heart rate acceleration for
contamination (Olatunji & Cisler, 2008; Olatunji & Sawchuk, 2005; fear compared to happiness, and heart rate deceleration for disgust
Rozin & Fallon, 1987; Rozin, Haidt, & McCauley, 2000). At the compared to all other emotions. The authors did not report if the
phenomenological level, researchers studying disgust typically define deceleration for disgust was significantly different from zero (i.e.,
disgust in the same three systems as fear (Olatunji & Cisler, 2008; disgust results in heart rate deceleration compared to baseline and not
Woody & Teachman, 2000). Woody and Teachman (2000) differenti- just to other emotions). These results suggest that a particular pattern
ate fear and disgust along the dimensions of behavioral intentions, of autonomic nervous system (ANS) activity can differentiate fear from
appraisal, and physiological processes. They argue that avoidance disgust: fear results in heart rate acceleration relative to positive
characterizes both fear and disgust, but for different reasons: “fear- emotions; disgust results in heart rate deceleration compared to
motivated avoidance protects the person from perceived danger, positive emotions. The differentiation of fear and disgust based on
while disgust-motivated avoidance may be more often linked to heart rate has since been replicated. For example, Levenson, Ekman,
sensation or imagery” (p. 293). The authors do not provide a means to and Friesen (1990) found that participants engaged in a directed facial
differentiate the reasons for avoidance, and consequently researchers action task or relived emotions task displayed heart rate acceleration
are left with the same indicator of avoidance to define both fear and for fear, but “unchanged or small decelerations in heart rate during
disgust. One problem with using avoidance to define both fear and disgust” (p. 380). Levenson, Carstensen, Friesen, and Ekman (1991)
disgust is that the topographical form of the avoidance is similar for found greater heart rate acceleration among elderly adults during fear
both fear and disgust. For example, if disgust motivates avoidance on a compared to disgust emotion-eliciting activities, but disgust was not
behavioral approach task (BAT), it will result in a low score on the BAT. associated with a decrease in heart rate. The finding of heart rate
If fear motivates avoidance on a BAT, it will also result in a low BAT acceleration for fear is consistent with much research and theory (see
score. Even if one emotion (e.g., fear) results in a lower BAT score than e.g., Barlow, 2002; Lang, 1968; Lipp, 2006), and as a result, the review
the other emotion (e.g., disgust), the fact that the scores are in the will focus on the physiological correlates of disgust.
same metric leads to the possibility that disgust did not really The Ekman et al. (Ekman et al., 1983; Levenson et al., 1991, 1990)
motivate avoidance; rather what was labeled ‘disgust’ was really a studies are limited in that they reveal differential heart rate
subdued fear response. Given that the topographical features of responding between fear and disgust only during two emotion
avoidance for disgust and avoidance for fear are apparently quite eliciting activities (see Boiten, 1996 for a critique of the directed facial
similar, the observation of avoidance cannot differentiate disgust from action task). Other research, however, has found heart rate decelera-
fear. Avoidance, then, does not appear to be a useful means to examine tion towards ecologically valid stimuli. Olatunji, Haidt, McKay, and
the relative contributions of disgust and fear. David (2008) found that scores on a measure of the propensity to
Woody and Teachman (2000) state that “appraisals of a stimulus as respond with disgust were negatively correlated with heart rate
potentially threatening or dangerous is associated with a fear responding during videos depicting vomit or blood draws. Impor-
response… but disgust appraisals seem to focus more specifically on tantly, that a similar decrease was found across two types of disgust
the threat of contamination” (p. 295). Appraisals/cognitive processes stimuli suggests that the heart rate deceleration may be robust across
of disgust and fear may be topographically distinct and appear to be types of disgust stimuli. Stark, Walter, Schienle, and Vaitl (2005)
useful in examining the relative contributions of disgust and fear. presented non-selected individuals with neutral, disgusting, or
Physiological systems also appear to offer a viable indicator to mutilation pictures and found heart rate deceleration for the
differentiate fear and disgust. Woody and Teachman (2000) suggest disgusting and mutilation pictures compared to neutral pictures.
that heart rate acceleration characterizes fear, whereas heart rate Also, they found that the deceleration of heart rate correlated
deceleration characterizes disgust, indicating that physiology can positively with the subjective ratings of disgust for the pictures.
differentiate fear from disgust. The topography of heart rate response Thus, greater heart rate deceleration accompanies greater subjective
is distinct for fear and disgust, which suggests that heart rate response experiences of disgust. Klorman, Weissberg, and Wiesenfeld (1977)
is a useful indicator to examine the relative contribution of disgust and found greater heart rate deceleration among females during mutila-
fear. tion slides compared to neutral slides. Klorman and Ryan (1980),
Emotion theorists offer a perspective of identifying and measuring however, found that males did not differ in heart rate response to
emotions that extends the popular three systems model of fear (e.g., mutilation compared to neutral slides. Hare, Wood, Britain, and
Lang, 1968, Lipp, 2006). Izard (1993, 1992) suggests that basic Shadman (1970) found greater heart deceleration among non-selected
emotions are characterized by unique neural substrates and expres- male individuals during pictures of homicide scenes compared to
sive components. Ekman (1992a) argues that basic emotions can be picture of nude models or neutral scenes. Lang, Greenwald, Bradley,
differentiated based on the signal of the emotion (e.g., facial and Hamm (1993) found decreased heart rate towards disgust
expression) and physiology. Based on Ekman (1992b), Izard (1993, compared to fear and neutral pictures among non-selected indivi-
1992), and Woody and Teachman's (2000) analyses, there are four duals. Finally, Rohrmann and Hopp (2008) found decreased heart rate
response domains where disgust and fear would be expected to during an amputation film compared to a neutral film.
The results of physiological studies examining heart rate suggest a (i.e., the anterior insula) is activated by disgust facial expressions
robust heart rate deceleration for disgust compared to fear, and a strongly suggests that this region may be a critical neural substrate
moderately consistent heart rate deceleration for disgust compared to underlying disgust (also see Calder, Lawrence, and Young, 2001). The
neutral stimuli with only two studies yielding no differences between finding of amygdala activation in response to fear stimuli is consistent
disgust and neutral (Klorman & Ryan, 1980; Levenson et al., 1991). The with a large body of data implicating the amygdala in the fear
finding of slower heart rate for disgust compared to neutral stimuli is response (Calder et al., 2001; LaBar & Cabeza, 2006; LeDoux, 2000;
important in that it suggests that the heart rate component of the Phan, Wager, Taylor, & Liberzon, 2004, 2002; Phelps & LeDoux, 2005).
disgust response does not resemble a fear response of smaller The studies mentioned above (Phillips et al., 1998, 1997; Williams
magnitude. Instead, the disgust response likely involves a decreased et al., 2005) are limited to revealing specificity of the insula only for
heart rate compared to neutral stimuli, whereas fear involves an facial expressions as stimuli, which limits the degree to which the
increase. The finding of heart rate deceleration for disgust has been results suggest that the insula is involved in experiencing disgust, as
theorized to reflect parasympathetic activation (Page, 1994). Rohr- opposed to merely being involved in recognizing disgust. However,
mann and Hopp (2008) found support for this assertion, but also the finding of anterior insula activation specificity towards disgust
found mild evidence for sympathetic activation during disgust facial expressions has been replicated using ecologically valid types of
inductions. Future research is necessary to clarify the autonomic disgust stimuli. Wright, He, Shapira, Goodman, and Liu (2004)
nervous processes underlying disgust. compared neural activation between contamination, mutilation, and
There have been two studies showing heart rate acceleration fear-related pictorial stimuli among non-clinical participants. Results
towards disgust stimuli compared to neutral stimuli (Prkachin, revealed greater anterior insula activation for both contamination and
Williams-Avery, Zwaal, & Mills, 1999; Vrana, 1993), but these studies mutilation stimuli compared to neutral stimuli and the insula did not
used guided imagery as opposed to pictorial stimulus presentation. respond to fear pictures. Adding further evidence, Fitzgerald et al.
According to McKay and Tsao (2005), “the studies reporting increased (2004) found that participants asked to recall and re-experience
sympathetic activation relied on imagery, which may better address recent disgusting situations exhibited insula activation but not
anticipatory reactions. In this case participants may label the amygdala activation. These data further support the hypothesis that
anticipatory reaction as anxiety, leading to sympathetic activation, the insula is a specific neural substrate for the experience of disgust
while live exposure more likely produces the diphasic reaction, with and not just the perception of disgust faces.
parasympathetic arousal then occurring as well” (p. 356; italics The double dissociation hypothesis has not, however, been
added). The interpretation of heart rate acceleration towards consistently supported. For example, Schienle et al. (2002) found
particular disgust stimuli explains the data in a manner that does activation of the insula and the amygdala in response to various
not contradict the findings of heart rate deceleration towards disgust disgusting stimuli (e.g., maggots, cadavers, dirty toilets, vomit). They
stimuli. This differential pattern of heart rate suggests that if the also found activation of the insula in response to fear stimuli. An
emotion of disgust is present, it could be expected that a heart rate important inconsistency across studies investigating the neural
deceleration would be observed; if fear is present, it could be expected regions underlying fear and disgust is that the region of the insula
that heart acceleration would be observed. under investigation is not reported in all studies. For example, Phillips
et al. (1997) and Wright et al. (2004) report specificity of the anterior
2.3. Neural correlates insula for disgust, but some studies revealing non-specificity of the
insula do not report the region of the insula investigated (Schienle et
Calder, Keane, Manes, Antoun, and Young (2000) reported data on al., 2002; Schafer et al., 2005; Stark et al., 2004). These inconsistencies
a neurological patient with a lesion largely specific to the insula. This make their results difficult to interpret. In fact, recent meta-analyses
individual had selective deficits in recognizing disgust, but not other of positron emission tomography (PET) and fMRI studies (Murphy,
emotions (e.g., fear). Moreover, this individual's deficits in recognizing Nimmo-Smith, & Lawrence, 2003; Phan et al., 2004, 2002) lend
disgust extended across sensory modalities. The patient also scored support to the double dissociation hypothesis. Although these studies
low relative to controls on an individual difference measure of the found that both the amygdala and insula can respond to either fear or
propensity to experience disgust. This case study implicates the insula disgust stimuli, a high percentage of studies support specificity (e.g.,
as a neurological substrate necessary for both disgust perception and disgust and the insula; fear and the amygdala) compared to the
experience. percentage of studies suggesting non-specificity. Thus, there is a
Neuroimaging techniques have also been employed to test the higher probability of observing anterior insula activation in response
neural substrates underlying disgust and fear. Phillips et al. (1997) to disgust stimuli compared to amygdala activation (also see Cisler &
presented individuals with pictures of fearful, disgusting, or neutral Olatunji, 2008 for a recent review of neuroimaging studies of disgust).
faces. Functional magnetic resonance imaging (fMRI) revealed greater Accordingly, anterior insula activation would be expected if the
activation of the amygdala for fear faces compared to neutral faces, emotion was disgust, and amygdala activation would be expected if
and greater activation of the anterior insula for disgust faces compared the emotion was fear. One limitation of using anterior insula activation
to neutral faces. The insular cortex is heterogeneous in function as an indicator of disgust is that the anterior insula has also been
(Augustine, 1996), thus it is important that Phillips and colleagues implicated in interoceptive processes (Critchley, Wiens, Rotshtein,
found activation for disgust faces in a specific region of the insula (i.e., Öhman, & Dolan, 2004). Accordingly, disgust responding would be
the anterior insula). Phillips and colleagues also found that the expected to produce anterior insula activation, but generic inter-
amygdala did not respond to disgust faces, and the insula did not oceptive awareness may also produce anterior insula activation. As
respond to fear faces. Phillips et al. (1998) replicated these results in a with the other response domains, conclusions based on neural
subsequent study. Williams et al. (2005) similarly presented indivi- activation must be made with caution.
duals with fear and disgust faces and found amygdala activation
towards fear faces and insula activation towards disgust faces. These 2.4. Facial expression
results suggest a double dissociation between neural substrate and
stimulus type, which is consistent with the theory of basic emotions Yartz and Hawk (2002) presented individuals with fear, disgust,
(Ekman, 1992a,b; Izard, 1992, 1993), which posit unique neural positive, and neutral pictures and found greater levator labii and
substrates for the basic emotions. Given that the function of disgust corrugator muscle activation based on electromyogram (EMG)
is theorized to be avoidance of contamination (Rozin & Fallon, 1987), recordings for disgust compared to all other picture types, and less
the finding that a neural region associated with gustatory perception corrugator muscle activation for fear compared to all other muscle
picture types. Vrana (1994, 1993) asked individuals to imagine disgust, of contagion and similarity. Teachman (2006) expanded on the disgust
anger, or neutral scenarios and found that activation in the levator appraisal processes theorized in Woody and Teachman (2000) and
labii was greater during disgust compared to anger and neutral proposed an interesting analogy to Salkovskis' (1996) discussion of
imagery, and activation in the corrugator was greater for disgust primary and secondary appraisals in OCD. Teachman theorized that
compared to neutral stimuli. Lang et al. (1993) did not measure levator primary appraisals in disgust reflect beliefs about 1) disgusting
labii activation but found greater corrugator muscle activation in properties of an object (e.g., ‘that spider is gross’), or 2) the degree
response to disgust pictures compared to fear, but not neutral pictures. to which a situation or object will elicit disgust (e.g., ‘that spider will
Findings regarding specificity of the corrugator to disgust, however, make me feel disgusted’). Secondary appraisals in disgust reflect
are not consistent. Several studies have found increased corrugator individuals' beliefs about the perceived consequences if the primary
muscle activation in response to fear compared to pleasant or neutral appraisals are true (e.g., ‘if I feel disgusted, I won't be able to cope or
emotions (Dimberg, 1990, 1986; Schwartz, Ahern, & Brown, 1979; manage’). The important concept common to Teachman et al. (2006)
Sinha & Parsons, 1996, see for a review). Given that both fear and and Woody and Teachman's (2000) analyses that is relevant to the
disgust are associated with increased corrugator activation, the current review is that the primary appraisals for disgust and fear are
observation of increased corrugator activation does not appear able likely to be where differences emerge. That is, primary appraisals of
to reliably differentiate fear from disgust. disgust (e.g., ‘that thing is gross,’ ‘that fly will contaminate my drink’)
More promising, however, is the levator labii. Only one study failed center on attributes of the stimulus/situation that are topographically
to find increased levator labii activation for disgust (Wolf et al., 2005), quite distinct from appraisals of fear (e.g., ‘that snake is dangerous,’ ‘I
compared to three studies (Vrana, 1994, 1993; Yartz & Hawk, 2002) might crash if I fly in a plane). Secondary appraisals of disgust and fear
across different sensory modalities that did find increased levator labii may be similar and both revolve around individuals’ beliefs in whether
activation for disgust. Moreover, Yartz and Hawk found that fear stimuli they can cope if their primary appraisals are true.
did not result in levator labii activation. The observation of levator labii Research and theory on cognitive processes suggest three manners
activation in response to a stimulus, then, seems to indicate the emotion in which disgust and fear differ: 1) disgust involves the law of
of disgust and not fear. Consequently, it would be predicted that if a contagion, 2) disgust involves the law of similarity, and 3) disgust
stimulus elicits disgust, then levator labii muscle activation is likely to primary appraisals involve beliefs about the object/situation as
be observed. Additionally, the levator labii is a muscle used in raising disgusting, contaminating, or able to elicit the feeling of disgust.
the upper lip, which is involved in rejecting food from the mouth and Fear appraisals, in contrast, center on estimations of danger/harm.
consistent with the evolutionary function of disgust in protecting from However, appraisals do suffer from one limitation in regards to
disease/contagion (Rozin & Fallon, 1987; Rozin et al., 2000). their specificity. Woody and Teachman (2000) discuss what they refer
to as the Imprecise Emotional Label model, in which the link between
2.5. Cognitive processes fear and disgust is caused by the confusion of fear and disgust. Thus,
even if an individual appraises a stimulus as dangerous, the actual
There has been limited research on normative cognitive processes emotion eliciting the appraisal may be disgust, but the individual
in disgust (Williams et al., 2008). Moreover, there has been limited merely confuses the emotion and uses the wrong linguistic appraisal.
research comparing the cognitive processes of disgust and fear. The Conversely, even if an individual appraises a stimulus as contaminat-
limited research on cognitive processes in disgust is included in this ing, the actual emotion eliciting the appraisal may be fear, but the
review in light of the importance of appraisals (Armfield, 2006; individual merely confuses the emotion and uses the wrong linguistic
Teachman, 2006; Woody & Teachman, 2000) and cognitive processes appraisal. Similarly, verbally reported levels of disgust or fear (i.e.,
in general (Mathews & MacLeod, 2005) in understanding disgust and subjective units of distress [SUDs] ratings for the emotion of disgust or
fear. This section outlines the empirical evidence of possible cognitive fear) also have been used to measure the cognitive system of disgust
processes in disgust, and then describes existing theories that and fear in analogue-clinical populations (Olatunji, Smits, Connolly,
differentiate cognitive processes of disgust and fear. Willems, & Lohr 2007; Sawchuk, Lohr, Westendorf, Meunier, & Tolin,
Rozin, Millman, and Nemeroff (1986) presented participants 2002; Smits Telch, & Randall, 2002). A SUDs rating of disgust could be
recruited from either a university or the community with two glasses conceptualized as a primary appraisal of disgust1 (i.e., a SUDs rating
of different juices. A dead and sterilized cockroach was then dropped measures individuals' beliefs that the object/situation has disgust
into one of the glasses and then removed. Participants were notified eliciting properties). Research has shown that SUDs ratings of disgust
that the cockroach was sterilized and perfectly safe. Participants rated are highly correlated with SUDs ratings of fear (also see Olatunji &
their desire of drinking the ‘roached’ juice significantly less after the Cisler, 2008), with reported r values of .68 (Olatunji et al., 2007), .83
‘roaching.’ Similarly, Rozin, Markwith, and McCauley (1994) found in a (Sawchuk et al., 2002), .86 (Smits et al., 2002; BAT 2), .89 (Olatunji &
questionnaire study that college students were less willing to wear a Deacon, 2008), and .90 (Smits et al., 2002; BAT 1). Consequently, the
thoroughly laundered sweater after it had been worn by a man with observation of elevated SUDs ratings for one emotion could actually be
AIDS compared to a man without AIDS. These studies illustrate the law due to causally prior elevations of the other emotion. Although
of contagion; that is, the disgust-related appraisal that ‘once in appraisals and SUDs of disgust and fear are topographically distinct
contact, always in contact’ (Rozin & Fallon, 1987). and therefore useful in examining the relative contributions of disgust
Rozin et al. (1986) presented participants with fudge shaped to and fear, there appear to be slight problems with specificity.
resemble dog feces and rubber fake vomit. Participants were less Accordingly, appraisals and SUDs will be used in the current review,
willing to eat the fudge shaped to resemble dog feces relative to the but conclusions must be tempered by these limitations.
same type of fudge shaped into a disc, and participants were less
willing to place the rubber fake vomit in their lips relative to a rubber 2.6. Summary
stopper. This study illustrates the law of similarity; that is, the disgust-
related appraisal that the images resembling a noxious object are also There appear to be four response domains in which the specific
noxious (Rozin & Fallon, 1987). topographies for disgust and fear are expected to differ. If the stimulus
Woody and Teachman (2000) suggest that disgust appraisals differ
from fear appraisals in that disgust appraisals center on the threat of 1
An alternative conceptualization of SUDs ratings is simply as self-reported
contamination, whereas fear appraisals may be more centered on emotional experiences. SUDs ratings will be considered appraisals in this paper in
broad estimations of danger. These authors' reasoning derives from order to 1) be consistent with Teachman's (2006) theory of appraisals in disgust, and 2)
Rozin et al.'s (Rozin et al., 1986; Rozin et al., 1994) research on the laws provide another indicator of possible cognitive processes in disgust and fear.
elicits disgust, it follows that heart rate deceleration, anterior insula on danger will be observed. These response topographies also
activation, levator labii activation, and appraisals centering on converge well with the theorized evolutionary function of fear —
disgusting properties or transmission of contagion will be observed. avoiding/escaping danger (e.g., Öhman & Mineka, 2001). Note,
Importantly, these response topographies generally converge well however, that there may not be a specific facial expression indicator
with the theorized evolutionary function of disgust — avoidance/ for fear (Kring & Bachorowski, 1999). Given that the reliability of any
rejection of contagions. That is, the levator labii is a muscle involved in one measure is questionable (e.g., Klorman & Ryan, 1980; Levenson
rejecting food from the mouth, the anterior insula is involved in et al., 1991; Schienle et al., 2002; Wolf et al., 2005; Woody &
gustatory processes (Calder et al., 2001), and implausible beliefs about Teachman, 2000), future research investigating whether disgust
the transmission of contagion (e.g., ‘once in contact always con- operates in anxiety disorders should include multiple indicators
taminated’) and appraisals of objects as disgusting all appear related (e.g., heart rate and facial muscle tension) in order to most accurately
to the similar function of avoiding harmful disease or contagion account for the presence and absence of both emotions.
carrying substances. It is difficult to explain why disgust would be
associated with a decrease in heart rate. Analogously, Page (1994) 3. A critical review of disgust-related anxiety research
suggested that the fainting response in BII phobia may actually not
have an evolutionary advantage. It may also be the case that a heart The previous sections identified specific indicators of disgust and
rate deceleration is a correlate of disgust and not functionally involved fear across four response systems. The following sections review extant
in achieving the evolutionary purpose of disgust. Alternatively, Stark research employing these specific measures among spider phobia, BII
et al. (2005) suggested that decreased heart rate in disgust may be phobia, and contamination-related OCD. The review is limited to
intertwined with increased attention towards disgust stimuli, given studies using these emotion indicators to examine emotional respond-
that increased attention is also associated with heart rate decrease. ing towards disorder-relevant stimuli. This limitation is to keep the
Future research and theory on this issue is needed. review focused on examining the relative magnitude to which disgust
The review suggests that if the stimulus elicits fear, it follows that and fear characterize the emotional response in these disorders. A
heart rate acceleration, amygdala activation, and appraisals centering summary of the review is provided in Table 1.
Table 1
Summary of neural correlate, facial expression, heart rate and appraisal responses towards disorder-relevant stimuli among spider phobia, BII phobia, and contamination-related OCD
Disorder Emotion indicator Author Stimulus type Disgust Fear

Spider phobia Neural substrate Larson et al. (2006) Disorder-relevant pictures n.a. +
Neural substrate Straube et al. (2006) Disorder-relevant pictures + +
Neural substrate Goossens et al. (2007) Disorder-relevant pictures + +
Facial expression de Jong et al. (2002) Disorder-relevant pictures + −
Facial expression Vernon and Berenbaum (2002) Disorder-relevant object + +
Heart rate Hare (1973) Disorder-relevant pictures − +
Heart rate Fredrikson et al. (1995) Disorder-relevant pictures − +
Heart rate Sarlo et al. (2002) Disorder-relevant pictures + +
Cognitive de Jong and Muris (2002) Disorder-relevant scripts + +
Cognitive Huijding and de Jong (2007) Disorder-relevant pictures + +
Cognitive van Overveld et al. (2006) Disorder-relevant pictures + +
Cognitive Mulkens et al. (1996) Disorder-relevant object + n.a.
Cognitive Woody et al. (2005) Disorder-relevant objects + n.a.
Cognitive Olatunji and Deacon (2008) Disorder-relevant objects + +
Cognitive Vernon and Berenbaum (2002) Disorder-relevant objects + +
Cognitive Sawchuk et al. (2002) Disorder-relevant pictures + +
Cognitive Tolin et al. (1997) Disorder-relevant pictures + +
Cognitive Thorpe and Salkovskis (1998) Disorder-relevant pictures + +
Cognitive de Jong and Peters (2007a) Disorder-relevant pictures + −
Cognitive Teachman et al. (2001) Disorder-relevant pictures + +
BII phobia Neural substrate Herman et al. (2007) Disorder-relevant pictures − +⁎
Facial expression Lumley and Melamed (1992) Disorder-relevant + −
Heart rate Öst et al. (1984) Disorder-relevant film + +
Heart rate Ritz et al. (2005) Disorder-relevant film − +
Heart rate Vogele et al. (2003) Disorder-relevant film + +
Heart rate Sarlo et al. (2002) Disorder-relevant film + +
Heart rate Dahllof and Öst (1998) Disorder-relevant film + +
Cognitive Sawchuk et al. (2002) Disorder-relevant pictures + +
Cognitive Tolin et al. (1997) Disorder-relevant pictures + +
Cognitive de Jong and Peters (2007b) Disorder-relevant pictures + +
Contamination fear Neural substrate Breiter et al. (1996) Contaminated object + +
Neural substrate Phillips et al. (2000) Disorder-relevant pictures + −
Neural substrate Shapira et al. (2003) Generally disgusting pictures + −
Neural substrate McGuire et al. (1994) Disorder-relevant objects − −
Neural substrate van den Heuvel et al. (2004) Disorder-relevant pictures − +
Neural substrate Rauch et al. (1994) Disorder-relevant objects − −
Facial expression No available studies
Heart rate Hornsveld et al. (1979) ‘Dirty’ objects − −
Cognitive Tolin et al. (2004) Disorder-relevant object + n.a.
Cognitive Connolly et al. (in press) Disorder-relevant pictures + +
Cognitive Cougle et al. (2007) None + +
Note. A ‘+’ in the ‘disgust’ or ‘fear’ column indicates that the emotion indicator suggests the emotion of disgust or fear, respectively; a ‘−’ indicates the emotion measure did not
indicate the emotion. The neuroimaging OCD studies are limited to studies using homogeneous contamination fear OCD samples (i.e., the contamination concerns were the primary
obsession or compulsion), except for Rauch et al. (1994) whose sample consisted of 75% pure contamination fear participants (i.e., 6 out of the 8 participants). ‘⁎’ indicates a marginally
significant finding. ‘n.a.’ = not available.
3.1. Spider phobia fear and disgust are present in spider phobia, but that the fear
response may be automatic, whereas the disgust response may not.
3.1.1. Facial expression One limitation to these studies is that they did not document that
de Jong, Peters, and Vanderhallen (2002) assessed facial muscle insula cortex activation was specific to the anterior insula, thus it is
activation during spider-related guided imagery and disgust-related difficult to discern what function of the insula the significant
imagery among spider fearful and control women. Results revealed activation actually indicates.
greater levator labii muscle activation during both disgust and spider-
related guided imagery compared to another muscle region, and 3.1.4. Cognitive processes
importantly, the spider phobic group displayed greater levator labii A few studies demonstrate that individuals with spider phobia
muscle tension during spider-related imagery compared to the control exhibit the ‘law of contagion’ appraisal towards spiders. Mulkens, de
group. Vernon and Berenbaum (2002) measured facial expression Jong and Merckelbach (1996) found that women with spider phobia
during BAT towards a live tarantula through coding videotapes of were significantly less likely to eat a cookie after a spider had walked
participants' reactions during the BAT. Spider fearful individuals across it compared to women without spider phobia. Importantly, the
exhibited greater disgust (e.g., raised upper lip, which indicates two groups did not differ in their likelihood of drinking a
levator labii muscle activation) and fear (e.g., brow raised, lips tense) contaminated cup of tea, suggesting that there were no differences
facial expressions compared to non-fearful individuals. There were no between the groups in general sensitivity to dirtiness. This study
differences in the frequency of disgust and fear facial expressions. illustrates that spider phobia may be characterized by appraisals of
disgust, specifically the law of contagion (i.e., ‘once in contact, always
3.1.2. Heart rate in contact’). Other studies have since replicated this law of contagion
Hare (1973) found that subclinical spider fearful participants effect in spider phobia (de Jong and Muris, 2002; Woody, McLean, &
displayed heart rate acceleration towards spider-related pictures but Klassen, 2005). One limitation of these studies is that they do not offer
not towards neutral stimuli, and also that a control group did not an appropriate comparison for fear-related cognitive processes, thus
display heart rate acceleration towards spider-related pictures. This the relative contributions of disgust and fear cannot be compared.
finding of heart rate acceleration among spider fearful individuals has Some studies have used experimental tasks (Implicit Association
been replicated (Fredrikson, Wik, Annas, & Ericson, 1995; Sarlo, Tasks [IAT], expectancy bias paradigm) that assess whether spider
Palomba, Angrilli, & Stegagno, 2002; see Table 1). Sarlo et al. (2002) phobic individuals associate spiders with disgust-related stimuli or
observed an initial heart rate increase followed by a statistically fear-related stimuli. These experimental designs provide some
significant decrease among spider phobics during viewing of a spider evidence of whether the cognitive processes in spider phobia involve
film. This pattern is notably similar to the diphasic heart rate response disgust and/or fear. For example, associating spiders with disgust
in BII phobia (see section BII phobia below), which has been theorized outcomes provides evidence, albeit indirectly, that spiders are
to reflect parasympathetic activity and the emotion of disgust (Page, appraised as disgusting. Importantly, these studies assess associa-
1994). Importantly, Sarlo and colleagues found that sustained tions/expectancies for both fear and disgust related stimuli, thus
sympathetic activity predicted the heart rate response across time in allowing an estimate of the relative contributions of fear and disgust.
spider phobics, but the relation between sympathetic activity and Teachman, Gregg, and Woody (2001) used an IAT with pictures of
heart rate response among BII phobics became weaker across time spiders as the target stimuli and disgust attributes (e.g., gross) and fear
and during the second phase heart rate decline. Thus, the heart rate attributes (e.g., harm) as separate categories. Results revealed that
pattern among spider phobics in this study appears to reflect spider fearful individuals associated spiders with both disgust and fear
sympathetic activity, and consequently fear, as opposed to parasym- attributes to a greater degree than an anxious control group. Huijding
pathetic activity and disgust. and de Jong (2007) employed an IAT with pictures of spiders as the
target stimuli and disgust attributes (e.g., ‘dirty’) and fear attributes
3.1.3. Neural substrate (e.g., ‘attacking’) as separate categories. Results revealed that
Several studies have examined neural responses to disorder individuals with spider phobia associated spiders with both fear and
relevant stimuli in spider phobia (see Table 1). Goossens, Sunaert, disgust attributes to a greater degree than did non-phobic individuals.
Peeters, Griez, and Schruers (2007) found greater amygdala activation The magnitude of disgust associations did not appear to differ from
towards spider stimuli compared to a control group, but this the magnitude of fear associations. van Overveld, de Jong, and Peters
difference disappeared after exposure therapy. However, the results (2006) asked participants to rate whether they expected pictures of
also demonstrated greater insula cortex activation compared to spiders, maggots, dogs, and rabbits to be followed by disgust
control participants pre-treatment and this difference also disap- outcomes (i.e., drinking a distasteful fluid), fear outcomes (i.e., an
peared after treatment. These results suggest that fear and disgust electric shock), or no outcome. The authors found that high spider
may characterize spider phobia. Straube, Mentzel, and Miltner (2006) fearful individuals expected both disgust and fear outcomes to follow
found that spider phobics display amygdala and insula activation spiders to a greater degree than low spider fearful individuals. There
when attending to spider pictures, but only amygdala activation when was no difference between the magnitudes of expectancies for disgust
the spider pictures are present but not part of the primary or fear outcomes. However, expectancies of disgust outcomes
experimental task. The finding of amygdala activation when the following spiders significantly predicted self-reported spider fear,
spider was not part of the primary task suggests automaticity, such but fear-expectancies did not. Using a similar methodology, de Jong
that conscious control and effort were not necessary (Moors & de and Peters (2007a) found that spider fearful individuals expected a
Houwer, 2006). That fear appeared to be automatic whereas disgust disgust outcome to follow spider pictures, but did not expect a fear
did not suggests that the fear response may come first, which is later outcome to follow spider pictures.
followed by disgust. Automaticity of only the fear response also Some studies have also asked participants to rate how disgusted
demonstrates the comparative ease with which spiders elicit fear and frightened they feel during exposure to spiders/spider-related
relative to disgust. However, these interpretations must be tempered stimuli. These types of assessments provide some evidence of the
by the fact that they are based on one isolated study. Larson et al. types of primary appraisals individuals make about spiders and their
(2006) found that immediate amygdala activation in response to responses towards spiders. Olatunji and Deacon (2008) engaged
spider stimuli differentiated between spider phobics and control spider fearful and nonfearful individuals in a BAT task towards a
participants, which further suggests a key role of the amygdala, and realistic looking, but fake, tarantula. Spider fearful individuals self-
fear, in spider phobia. Overall, neuroimaging studies suggest that both reported significantly more fear and disgust compared to non-fearful
individuals. Spider fearful individuals reported more fear than disgust, activation. Results revealed that BII phobic individuals displayed more
but it was not reported whether this difference was significant. facial expressions of disgust compared to non-phobic individuals
Vernon and Berenbaum (2002) also found greater self-reported fear during the surgery films. These results suggest that BII phobic
and disgust during a BAT towards a live spider, but there was a trend individuals respond with the emotion of disgust during exposure to
for greater self-reported disgust compared to self-reported fear. disorder-relevant stimuli.
Sawchuk et al. (2002) presented spider fearful and nonfearful Some research has investigated facial expression in BII phobia
individuals with spider pictures, measured self-reported fear and towards disgusting stimuli (Schienle et al., 2005) and to neutral
disgust, and found greater fear and disgust in the spider fearful stimuli paired with disgusting stimuli (Schienle et al., 2001). However,
compared to non-fearful individuals. Spider fearful individuals also these studies do not demonstrate which type of facial expression BII
exhibited greater self-reported fear relative to disgust. Tolin, Lohr, phobics display towards disorder-relevant stimuli. Thus, these studies
Sawchuk, and Lee (1997) used a similar methodology and found that are not appropriate to test whether BII individuals respond pre-
spider fearful participants again rated more fear and disgust towards dominantly with fear or disgust.
spider pictures relative to non-fearful individuals, but there were no
differences in self-reported ratings between fear and disgust towards 3.2.2. Heart rate
spiders. Finally, Thorpe and Salkovskis (1998) also found that One of the most promising pieces of evidence for disgust in BII
individuals with spider phobia rated pictures of spiders as more phobia is the unique heart rate response to phobic-related stimuli. The
disgusting and frightening compared to non-phobic individuals; heart rate response to phobogenic stimuli in BII is characterized by a
differences between fear and disgust ratings were not reported. diphasic response (Page, 1994; Sarlo et al., 2002; Thyer, Himle, &
Curtis, 1985), in which there is a rapid acceleration of heart rate
3.1.5. Summary followed by a sharp decrease in heart rate. This heart rate response is
Facial expression data indicate both fear and disgust, but there is specific to disorder-relevant stimuli; BII phobic individuals do not
more consistent evidence for a disgust facial expression. Cognitive display a diphasic response while experiencing generic stress (Dahllof
measures generally implicate both disgust and fear, with a slight trend & Öst, 1998). The latter half of the diphasic reaction seems responsible
favoring disgust among the IAT/expectancy bias studies. In contrast, for the fainting response that sometimes occurs with BII phobia (Öst,
heart rate studies and neuroimaging studies generally suggest a Sterner, & Lindahl, 1984; see Page, 1994 for a detailed discussion). For
dominant role for fear and a less robust role for disgust. Moreover, one example, Öst et al. (Dahllof & Öst, 1998; Öst et al., 1984; see Table 1)
fMRI study (Straube et al., 2006) suggests automaticity of the fear presented BII phobics with surgery films and found an initial increase
response, but not the disgust response. The limitation that no studies in heart rate, followed by a rapid decline in heart rate. Similarly, Sarlo
have revealed specific activation of the anterior region of the insular et al. (2002) presented BII phobics with surgery films and also found
cortex further weakens the neuroimaging evidence for the role of an initial heart rate increase followed by a decrease. Sarlo and
disgust in the emotional response in spider phobia. As such, the colleagues found that sympathetic activation predicted the initial
evidence suggests that the degree to which the emotional response heart rate increase, but the influence of sympathetic activation
reflects fear or disgust may depend on the response domain became weaker over time. This suggests that the latter heart rate
measured. One possible theory explaining the dissociation between decrease is mediated by parasympathetic activation and disgust. Page
emotion observed and response domain measured is that spiders may (1994) argues that the unique heart rate response in BII phobia is
initially elicit fear in physiological domains (e.g., neural substrate, mediated by parasympathetic activity and suggests that the diphasic
heart rate), whereas disgust may emerge later during more controlled heart rate response in BII phobia reflects disgust. However, even if the
processes (i.e., appraisals, facial expression). Thus, it would be latter heart rate decrease is mediated by disgust and parasympathetic
predicted that amygdala and heart rate acceleration may be observed activity, the initial heart rate increase is likely mediated by
towards masked (i.e., not-consciously recognized) spider-stimuli, but sympathetic activity (Page, 1994; Sarlo et al., 2002), thus implicating
a disgust facial expression or evidence of the law of contagion would fear. As such, the diphasic heart rate response towards disorder-
only be expected to be observed towards consciously recognized relevant stimuli in BII phobia may reflect both fear and disgust.
spider stimuli. This dissociation may occur in order to motivate 1) The diphasic heart rate response has not, however, been
immediate escape from spiders given that some may be dangerous, consistently demonstrated in BII phobia. Ritz et al. (2005) found that
and 2) avoid future contact with objects in close proximity to spiders only 2 of 12 BII phobics demonstrated the diphasic heart rate response
given the possibility for contagion transmission (e.g., Matchett & during viewing of surgery films, although they failed to find a
Davey, 1991). Indeed, this would explain why fear may be auto- significant diphasic response among their entire BII phobia sample. It
matically elicited from spiders (i.e., to quickly avoid/escape) and is important to note that Ritz and colleagues' null results may be due
disgust may occur in more controlled domains (i.e., appraisals of to their strict definition of diphasic responding; they defined a
disgust and contamination may motivate passive avoidance of objects diphasic response as an increase in heart rate towards the BII film
touched by spiders). Future research concurrently measuring all compared to a generally unpleasant film and a subsequent decrease in
response domains is necessary to further explore how disgust and fear heart rate towards the BII film compared to a neutral film. These strict
differentially emerge across the response systems. Finally, the criteria may have minimized false positives but consequently also
observation that physiological measures indicate fear whereas more maximized false negatives. Similarly, Gerlach et al. (2006) observed a
controlled processes indicate disgust suggests that both emotions may rapid heart rate increase among BII phobics during an actual
need to be targeted during treatment, but possibly through distinct venopuncture but did not observe a subsequent heart rate decelera-
techniques (e.g., exposure for fear, re-appraisal for disgust). tion. A difference between this study and studies documenting a
diphasic response is the type of stimulus used. In previous studies the
3.2. BII phobia stimulus was a surgery film, but in the Gerlach study it was a
venopuncture. It may be the case that venopuncture stimuli are
3.2.1. Facial expression weaker elicitors of the diphasic response.
Lumley and Melamed (1992) videotaped BII phobic and non- The diphasic response may be specific to a subset of BII phobics.
phobic individuals' facial expressions while viewing surgery film clips Vogele et al. (2003) found a rapid increase in heart rate, followed by a
and neutral film clips. The facial expressions were rated by observers decrease in heart rate, during viewing of a surgery video only among
on whether the participants furrowed their eyebrows or raised their BII phobics with a history of fainting. BII phobics without a history of
upper lip; rising of the upper lip indicates levator labii muscle fainting did not display this diphasic heart rate response. A history of
fainting may explain previous null findings of the diphasic response, studies (Sawchuk et al., 2002; Tolin et al., 1997) found that the disgust
such that previous studies may have used samples with mostly non- appraisals were greater than the fear appraisals. Thus, data from facial
fainters. These latter results also suggest that the diphasic response expressions, heart rate, and appraisals all converge in suggesting a
may not be intrinsic to BII phobia per se, but rather only to the fainting dominant role of disgust and a minimal role of fear. One fMRI study
response. If this were true, it would call into question whether disgust failed to corroborate a role for either disgust or fear in BII phobia. In
is only relevant in BII phobics with a history of fainting. Further contrast to spider phobia, there is evidence for a role of disgust in BII
investigation of response specificity and the consistent role of disgust phobia across all response systems except for neural substrate, but this
is needed. conclusion must be tempered by the limited number of studies. One
theoretically interesting line of inquiry could be in investigating
3.2.3. Neural substrate Lumley and Melamed's (1992) assertion that what is feared in BII
Only one study presented BII phobic individuals with disorder phobia is responding with disgust. This assertion is consistent with
relevant study and examined neural substrate activation (see Table 1). the current findings that fear may emerge in more controlled
Hermann et al. (2007) found that BII phobic individuals display processes such as appraisals. It may be the case that the fear arises
diminished medial prefrontal cortex activity in response to disorder due to appraisals stating that feeling disgusted is bad/uncomfortable;
relevant pictures compared to the control group. They did not find as opposed to fear arising in response to the BII stimulus per se. Future
evidence of insula activation towards disorder-relevant pictures, but research is necessary to test possible interactions between fear and
found marginally significantly greater activation of the amygdala disgust in BII phobia.
towards disorder-relevant compared to neutral pictures. The medial
prefrontal cortex has been implicated in the down-regulation of 3.3. Contamination-related OCD
emotional processing (Bishop, 2007; Phelps & LeDoux, 2005), thus
suggesting that BII phobia may be characterized by a generalized 3.3.1. Facial expression
diminished ability to regulate negative emotions elicited from BII- No studies have examined facial muscle activity in contamination
relevant stimuli. As such, diminished medial prefrontal cortex activity fear.
could be consistent with either fear, disgust, or both underlying BII
phobia. 3.3.2. Heart rate
Only one study has investigated heart rate response in contamina-
3.2.4. Cognitive processes tion fear. Hornsveld, Kraaimaat, and Van Dam-Baggen (1979)
There are no studies testing whether individuals with BII phobia presented high contamination fear individuals and psychiatric
display appraisals related to the laws of contagion or similarity controls with in vivo ideographic stimuli selected to be ‘dirty.’ The
towards disorder-relevant objects. There have been some studies authors did not report examples of stimuli used. They found that the
investigating primary appraisals (i.e., self-reported fear and disgust) anticipation of touching a dirty stimulus resulted in greater heart rate
towards disorder-relevant materials. Sawchuk et al. (2002) presented acceleration compared to baseline among contamination fearful but
participants with surgery pictures and found that BII fearful not control participants. During actual touching of the stimuli, neither
individuals self-reported more fear and disgust relative to non-fearful group exhibited a change in heart rate compared to baseline. These
individuals. BII fearful individuals' self-reported disgust was greater results are difficult to interpret. On one hand, the contamination
than their self-reported fear. Tolin et al. (1997) similarly found that BII fearful individuals displayed a heart rate increase while anticipating
fearful individuals self-reported greater fear and disgust towards dirty stimuli, thus suggesting a fear response. On the other hand, this
surgery pictures compared to non-fearful individuals. Again, self- anticipatory response could be deemed anxiety about an impending
reported disgust was greater than self-reported fear. threatening situation (see McKay & Tsao, 2005 for a similar discussion
There has been one study examining the associations between BII- pertaining to disgust, heart rate, and anticipation). Additionally, if
related stimuli and disgust versus fear-related stimuli. de Jong and contamination fearful individuals respond with fear towards phobo-
Peters (2007b) presented BII phobic individuals and non-phobic genic stimuli, then it follows that a heart rate increase compared to
individuals with pictures of either neutral stimuli (e.g., rabbits) or baseline would be observed when touching the phobogenic stimuli.
disgust stimuli (e.g., pictures of blood-donations). Presentation of The results did not support this hypothesis. Thus, the results do not
these pictures was followed by one of three possible outcomes: a strongly suggest fear or disgust. It is difficult to discern what these
shock, drinking a disgusting fluid, and nothing. Results revealed that results say in regards to the questions underlying this review.
both high and low phobic individuals expected both a fear and
disgust-related outcome with equal probability. There were no 3.3.3. Neural substrate
differences between groups. Several studies have investigated the neural substrates underlying
contamination fear (see Table 1). Some studies suggest that disgust
3.2.5. Summary may be the predominant emotional response. For example, Phillips et
One facial expression study demonstrates disgust and not fear. al. (2000) presented individuals with contamination fears with
Heart rate data appear to suggest both disgust and fear. It is important disorder-relevant pictures and found heightened insula, but not
to note that the response pattern of the diphasic heart rate response in amygdala activation. Similarly, Shapira et al. (2003) found heightened
BII phobia begins with an increase (i.e., fear), which is followed by a insula and not amygdala activation towards generally disgusting
decrease (i.e., disgust). An alternative interpretation of the heart rate pictures among a contamination fear sample.
data in BII phobia is that the initial heart rate activation indicates Some studies suggest that both fear and disgust may underlie
anxiety about a pending disgust response (McKay & Tsao, 2005). contamination fears. Schienle, Schafer, Stark, Walter, and Vaitl (2005)
Indeed, Lumley and Melamed (1992) argue that “what may be feared used a heterogeneous OCD sample (i.e., not ‘pure’ contamination fear
[in BII phobia] is the highly uncomfortable feelings of nausea or OCD) and found enhanced insula activation while viewing disorder
faintness…” (pg. 433). When viewed in this light, the primary relevant pictures, but amygdala activation towards these pictures
emotional response is disgust and the initial heart rate activation is correlated positively with a self-report measure of contamination fear
merely anticipatory anxiety about the imminent disgust response. The as well as with the experience of disgust. Mataix-Cols et al. (2004),
evidence from both facial expression and heart rate data then appear however, used a heterogeneous OCD sample and found enhanced
to suggest a dominant role of disgust. Appraisal data suggests both amygdala activation during a contamination fear provocation task, but
disgust and fear in the emotional response of BII phobia, but two that insula activation correlated with a self-report measure of
contamination fear. Similarly, Breiter et al. (1996) found both insula data more strongly indicate disgust across the response systems that
and amygdala activation in response to contaminated objects among have been more thoroughly investigated (i.e., appraisals, neural
contamination fearful individuals. Finally, two studies found neither substrate). These data on contamination-related OCD is in contrast
insula nor amygdala activation towards disorder-relevant objects to Rachman's (2006, 2004) assertion that contamination-related OCD
(McGuire et al., 1994; Rauch et al., 1994), and one study found only is predominantly fear based, and not disgust based. Instead, the
amygdala, and not insula, activation towards disorder-relevant current data largely implicate disgust and minimally implicate fear. As
pictures (van den Heuvel et al., 2004). Thus, neuroimaging studies of with BII phobia, it may be the case that the fear component involved in
contamination fear generally indicate both disgust and fear, but may contamination-related OCD is best conceptualized as fear or dis-
indicate a more consistent and dominant role of disgust (see Table 1). comfort experiencing disgust (e.g., Cisler, Reardon, Williams, & Lohr,
However, inconsistent findings limit the degree of confidence placed 2007; Cougle et al., 2007). Alternatively, the fear could be associated
in this conclusion. with a fear of contracting an illness (Cougle et al., 2007), which is also
actually consistent with the evolutionary function of disgust (i.e.,
3.3.4. Cognitive processes motivating avoidance of disease/contagions). However, conclusions
One study has investigated the law of contagion appraisal in based on the current review are limited to a few neuroimaging and
contamination-related OCD. Tolin, Worhunsky, and Maltby (2004) appraisal studies. Further research across indicators is necessary to
asked individuals with contamination-related OCD, other anxiety corroborate the evidence from these response systems.
disorders, and non-anxious controls to identify the most contami-
nated object in the building. The experimenter then rubbed a new 3.4. General summary
pencil on the object and asked participants how contaminated the
pencil was. The experimenter then rubbed another new pencil on the The review of specific measures of disgust and fear in spider
previous pencil and again asked how contaminated this new pencil phobia, BII phobia, and contamination-related OCD largely suggests
was. This process was repeated for 12 pencils. Results revealed that that both fear and disgust are involved in the emotional response
the anxious and non-anxious controls evidenced nearly a 100% towards disorder-relevant stimuli in these disorders. Indeed, Table 1
decrease in appraisals of contamination across the 12 pencils, but demonstrates that many studies found evidence for both fear and
the contamination-related OCD group displayed only a 40% reduction. disgust in each of the disorders across many of the response domains.
The groups performed the same task on a non-threat object (i.e., a These data provide strong support for the growing program of
piece of candy) and all groups demonstrated nearly a 100% reduction research on disgust in anxiety disorders. However, the relative
in ‘candy contagion’ across the pencils. Thus, individuals with contribution of disgust and fear appears to differ across the disorders.
contamination-related OCD exhibit the law of contagion appraisal Spider phobia may be characterized by a fear response in more
uniquely towards possible sources of contamination. automatic response domains (e.g., neural activation) and a disgust
Connolly, Lohr, Olatunji, Hahn, and Williams (in press) used a response in more controlled response domains (e.g., facial expres-
covariation paradigm (i.e., a task in which the perceived covariation sion). BII phobia appears to be characterized most strongly by a
between a CS and different types of UCS's is measured) and found that disgust response, but cognitive processes may indicate both disgust
individuals with elevated contamination fear overestimated the and fear. Contamination-related OCD appears to be characterized
pairings of contamination-related pictures (e.g., vomit, dog feces) most strongly by a disgust response and the inconsistent evidence for
with pictures of fear facial expressions and disgust facial expressions fear may indicate a weaker role of fear in this disorder. The role of
to a greater degree than with neutral facial expressions. There were no disgust and fear may differ in these disorders because of the nature of
differences in the estimations of pairings between fear facial the disorder-stimuli. That is, spiders are moving objects in the
expressions and disgust facial expressions. Additionally, individuals environment. Accordingly, it may be adaptive to quickly increase
with elevated contamination fear exhibited greater estimations of physical distance away from the spider, thus necessitating a fear
pairings between the contamination pictures and the fear facial response and rapid physiological mobilization. Disgust may be
expressions compared to individuals with low contamination fear, but involved in order to motivate passive avoidance of stimuli that have
the two groups did not differ in associations between contamination come in contact with spiders. For BII phobia and contamination-
pictures and disgust facial expressions. related OCD, however, the stimuli are relatively static. The potential
Finally, Cougle et al. (2007) investigated primary threat appraisals for harm from these stimuli may be more related to disease or
of participants with elevated contamination fear on a self-report contagion possibility; thus, rapidly increasing the physical proximity
questionnaire. They found that 41% of their sample (N = 27) endorsed a from these stimuli may not be necessary. Instead, it may only be
primary contamination threat of being overwhelmed by feelings of necessary to prevent physical contact with these stimuli, thus
disgust and that 37% of the sample endorsed a primary threat of being necessitating a disgust response. Fear may be involved due to
concerned with illness or harm to the self. These data suggest that discomfort experiencing the aversive sensations of disgust. This line
contamination fearful individuals appraise contamination-related of reasoning would explain why the role of disgust and fear in the
situations as disgust eliciting (i.e., a disgust primary appraisal) and different response domains may differ across the disorders.
dangerous (i.e., a fear primary appraisal). The degree to which these A recurring theme in this section is the limited number of studies
primary threat appraisals covaried was not reported. employing specific measures of disgust and fear in spider phobia, BII
phobia, or contamination-related OCD samples. It is difficult to place
3.3.5. Summary confidence in conclusions drawn from such a limited number of
No studies have examined facial expression in contamination- studies. The current review also highlights another problem in
related OCD. One heart rate study (Hornsveld et al., 1979) suggests the establishing an integral role of disgust in anxiety. Some of the
emotion of disgust, but data from this study are difficult to interpret. research described above suggests that the emotion observed may be
Contamination-related OCD is generally associated with anterior dependent on the response domain measured. It is difficult to explain
insula activation towards disorder-relevant stimuli, although this why this may be the case. As noted above, it may be that this pattern
effect is not always consistent. Contamination-related OCD strongly indicates that fear or disgust may emerge in automatic or controlled
demonstrates the law of contagion appraisal (Tolin et al., 2004), but response domains, depending on the disorder. Even if this were true, it
two other studies suggest appraisals of both disgust and fear. It is is difficult to discern what this means about the role of disgust or fear
difficult to draw conclusions from such a limited number of studies, in these disorders. For example, if disgust only emerges in controlled
but the data overall suggest a dominant role of disgust. Moreover, the processes in spider phobia, does that mean that disgust is less
important or dominant than fear? This is not necessarily so and it more controlled processes. BII phobia and contamination-related OCD
could also be the case that the more controlled processes and disgust appear to be predominantly characterized by disgust across response
are better predictors of avoidance (e.g., Olatunji, Cisler, Meunier, systems, while fear also emerges in more controlled response systems.
Connolly, & Lohr 2008; Woody et al., 2005). Future research should An overarching finding from the review is the need for more research
compare the ability of fear and disgust in each of the response using specific measures, preferably employing concurrent use of these
domains to predict avoidance and distress during exposure. Research measures. Additionally, given that fear and disgust are both implicated
along this line would assist in developing theories about how disgust in these disorders, researchers need to test whether therapeutic
is functionally relevant in these disorders. procedures differentially affect fear versus disgust response domains.
4. Future directions Acknowledgement
4.1. Concurrent use of emotion indicators We thank Andrew Tomarken for helpful comments on an earlier
draft of this manuscript.
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Clinical Psychology Review 29 (2009) 34–46

Contents lists available at ScienceDirect

Clinical Psychology Review

Disgust, fear, and the anxiety disorders: A critical review

3.3.2. Heart rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42

1. Introduction maintained. Fourth, this line of inquiry may begin to suggest

Disorder Emotion indicator Author Stimulus type Disgust Fear

4. Future directions Acknowledgement

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