Inhibitory Learning Craske & Sewart 2020
Inhibitory Learning Craske & Sewart 2020
Inhibitory Learning
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Clinical Handbook of Fear and Anxiety: Maintenance Processes and Treatment Mechanisms,
J. S. Abramowitz and S. M. Blakey (Editors)
Copyright © 2020 by the American Psychological Association. All rights reserved.
265
266 Sewart and Craske
the unconditional threat response (UR) to the related US. These phenomena
can be translated to the real world, wherein clinically elevated anxiety can
become associated with fear-relevant situations and stimuli. As an example, a
young woman by the name of Taylor is taking a walk around her neighbor-
hood when—out of nowhere—she is attacked and bitten by a German
Shepherd. Taylor was previously unafraid of dogs, but after being bitten (US,
dog bite) Taylor begins to fear (CR) all dogs (CS) and to avoid public spaces in
which she may encounter them. This fear of dogs and its related avoidance
has caused Taylor clinically significant distress and impairment.
To reduce or eliminate the CR, the CS must now lessen its status as a pre-
dictor of the US. This is achieved by fear extinction, which involves repeatedly
presenting the CS without the US (CS–noUS, shape → / shock/noise). Impor-
tantly, the original CS–US relationship is not erased during extinction, but
rather, a secondary relationship wherein the CS no longer predicts the US
develops as a result of extinction. Under certain conditions, this CS–noUS
relationship can inhibit the original, excitatory nature of the CS–US relation-
ship (Bouton, 1993). In the previous dog bite example, Taylor’s fear of dogs is
extinguished by exposing her to dogs in the absence of being bitten (CS–
noUS). After systematically exposing Taylor to dogs, the notion of dogs being
predictive of dog bite is dampened by new, inhibitory learning that dogs are
not predictive of dog bite. This new, inhibitory learning has extinguished
Taylor’s fear of dogs.
The original excitatory CS–US association, however, can be uncovered in
several ways, including spontaneous recovery (Quirk, 2002)—the reemergence
of a previously extinguished conditioned response after a delay. For example,
after completion of exposure therapy, Taylor’s fear of dogs may return in a
seemingly inexplicable manner. Furthermore, because extinction learning is
limited by context, renewal of conditional fear may occur if the surrounding
context is changed between extinction and retest (i.e., context renewal; Bouton,
2002). This highlights the importance of context variability in exposure therapy,
discussed in further detail later in the chapter. Finally, reinstatement of condi-
tional fear occurs if unsignaled US presentations occur between extinction
and retest (Haaker, Golkar, Hermans, & Lonsdorf, 2014). Clinically translated,
adverse events following exposure therapy may lead to a return of fear of the
previously feared stimulus. Fourth, rapid reacquisition of the CR is seen if the
CS–US pairings are repeated following extinction (Ricker & Bouton, 1996), as
may occur in dangerous environments. In addition to offering an explanation
Inhibitory Learning 267
for return of fear following exposure therapy, these processes suggest possible
pathways through which exposure therapy can be optimized to reduce the
return of fear (Craske et al., 2014).
Traditional, habituation-based models of exposure therapy (see Chapter 14)
posit that fear reduction during and between exposure trials is required for
lasting changes in the perceived harm associated with a given phobic stimulus.
Thus, habituation-based exposure approaches have focused on fear reduction
within and between sessions as an index of treatment response and success (e.g.,
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Foa, Huppert, & Cahill, 2006; Foa & Kozak, 1986). However, our understanding
of the role of fear reduction—or habituation—in exposure has also evolved with
advances in associative learning theory. The amount that fear has been reduced
by the end of an exposure trial or series of exposure trials is not a reliable pre-
dictor of the fear level expressed at follow-up assessment (Baker et al., 2010;
Culver, Stoyanova, & Craske, 2012; Kircanski et al., 2012; Meuret, Seidel,
Rosenfield, Hofmann, & Rosenfield, 2012). Similar results have been found in
laboratory paradigms with animals and human samples (Plendl & Wotjak, 2010;
Prenoveau, Craske, Liao, & Ornitz, 2013; Rescorla, 2006). To combat return of
fear, inhibitory learning models of exposure do not emphasize fear reduction
during exposure trials and instead focus on optimizing the strength and dura-
bility of the CS–noUS relationship that occurs during extinction learning.
Numerous strategies translated from basic fear learning research can be
implemented during exposure to enhance inhibitory learning. These methods
include enhancing inhibitory learning through (a) expectancy violation,
(b) removal of safety signals, (c) attentional focus, (d) deepened extinction,
(e) stimulus variability, (f) occasional reinforced extinction, and enhancing
retrieval of inhibitory learning via (g) multiple contexts and (h) retrieval cues.
This chapter focuses on ways to implement and capitalize on these strategies
within treatment to achieve superior extinction learning.
IMPLEMENTATION
Expectancy Violation
As defined in the fifth edition of the Diagnostic and Statistical Manual of Mental
Disorders (American Psychiatric Association, 2013), anxiety disorders are
associated with the overprediction of aversive, negative outcomes. For exam-
ple, an individual with social anxiety may expect with absolute certainty that
if they were to attend a social gathering they would be rejected by peers.
Similarly, someone with panic attacks may expect with high confidence that
experiencing a rapid heart rate will result in a heart attack. Enhancing extinc-
tion learning during exposure requires that exposure exercises be designed to
maximally violate an individual’s elevated expectancies regarding the fre-
quency or intensity of predicted, aversive outcomes (Davey, 1992; Rescorla &
Wagner, 1972). Based in learning theory, expectancy violation posits that the
268 Sewart and Craske
was predicted and what occurred, and the degree of surprise from the expo-
sure practice (Craske et al., 2014). The phrase “test it out” is helpful to intro-
duce to patients when providing rationale for expectancy violation.
The end of an exposure trial is determined by conditions that violate
expectancies. Furthermore, exposures are continued for the duration deter-
mined to violate expectancies most effectively. An individual with social anx-
iety may avoid one-on-one conversations for fear of rejection. To determine
the duration of a related exposure exercise, the therapist should assess with
the patient how long the patient needs to participate in a one-on-one conversa
tion until they are convinced that rejection will occur. If the patient states with
certainty that rejection will occur after only 5 minutes of conversation, the
duration of the exposure practice should be constructed to last for more than
5 minutes to maximally violate this excitatory expectancy. Using an inhibi-
tory learning approach, graduated exposure may be used by clinicians to pro-
gressively modulate conditions in which the feared outcome is judged most
likely to occur. For example, one-on-one conversation exposure exercises for
social anxiety may be conducted at increasingly longer trials (e.g., 5 minutes,
10 minutes), regardless of the observed fear reduction, in an effort to further
violate expectancies and extinguish related fear. In several studies, failure to
habituate throughout exposure therapy was not associated with poorer out-
comes (e.g., Culver et al., 2012; Kircanski et al., 2012; Lang & Craske, 2000).
For most anxiety-related disorders, it is indisputable that the defined neg-
ative outcome has not occurred during a given exposure exercise. For exam-
ple, an individual predicts that experiencing panic-related symptoms (e.g.,
rapid heartbeat) will result in a heart attack. Testing out whether or not a heart
attack will occur during an interoceptive exposure practice is straightforward.
Similarly, determining whether or not a dog-phobic individual is actually bit-
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EXHIBIT 15.1
Prior to How likely is it that what I am most worried about will occur
Exposure: (0 = Not at All, 100 = Certain)?
After Did what I was most worried about occur? Yes ____ No ____
Exposure:
How do I know?
Imagine I repeated the same exposure practice. How likely is it that what I was
most worried about before will occur this time (0 = Not at All, 100 = Certain)?
____
Note. From the UCLA Anxiety and Depression Research Center. Reprinted with permission of
Jonathan S. Abramowitz and Shannon M. Blakey.
272 Sewart and Craske
All clinical case material has been altered to protect patient confidentiality.
1
Inhibitory Learning 273
Attentional Focus
One of the critical variables in modern associative learning models is the atten-
tional salience of presented CSs (Rescorla & Wagner, 1972). Thus, within an
inhibitory learning approach to exposure, increased salience of the CS (e.g.,
conspicuous, attention-grabbing; Pearce & Hall, 1980) enhances extinction
learning. To optimize salience and subsequent extinction, directing a patient’s
attention to excitatory CSs during all exposures trials is critical. Given that dis-
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Deepened Extinction
stroke. Joel has completed exposures for fear of light-headedness with chair spinning exer-
cises and confronted the fear of shortness of breath through straw breathing exercises.
Joel’s therapist may choose to deepen extinction learning by having Joel complete straw
breathing exercises while spinning in a chair.
Stimulus Variability
Research indicates that variable practice enhances the capacity for new learning
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(Bjork & Bjork, 1992, 2006). Variation results in effortful encoding of learning
resulting from exposure trials and gives rise to a schema that may be applied
across a range of fear-provoking situations (Bjork & Bjork, 1992). Importantly,
varied practice has been shown to increase the array of associated cues that
may be present during retrieval (Estes, 1955), making inhibitory associations
of CSs more accessible at a later time. The following example highlights the
importance of stimulus variability during exposure.
Logan presents for treatment of his fear of spiders. To extinguish his fear, Logan’s therapist
conducts multiple exposure trials with the same large tarantula. Logan now reports that
his fear of spiders and avoidance of places where he may encounter a spider has disap-
peared. He and his therapist then terminate treatment. Months later, while hiking, Logan
walks into a golden banana spider’s web. Logan’s fear and avoidance of spiders return.
In this example, when hiking, Logan was unable to access the inhibitory
associations he had developed with his therapist months earlier. This return
of fear is likely due to the fact that inhibitory learning was confined to a
specific type of spider, rather than extended to a general schema of spiders.
Developing multiple retrieval cues and a general inhibitory rule relating to
spiders requires that Logan be exposed to multiple spider types with varying
features.
Variability in exposures can also be applied to exposure duration, timing of
exposures, levels of emotional intensity, and expectancy levels. This approach
is in contrast to moving through exposures in a stepped, hierarchical fashion.
Emphasizing variability has been shown to attenuate fear renewal and result
in superior outcomes at follow-up (e.g., Kircanski et al., 2012; Rowe & Craske,
1998; Tsao & Craske, 2000). “Change it up” is a helpful phrase for presenting
the rationale behind stimulus variability.
Multiple Contexts
Retrieval Cues
OUTCOME INDICATORS
Given that fear expression during exposure is (a) incommensurate with fear
learning (see Craske et al., 2008) and (b) an unreliable predictor of treatment
outcomes, fear reduction (generally measured by subjective units of distress)
between and within sessions should not be used as an index of inhibitory
learning. Rather, expectancy ratings and their reduction pre- to postexposure
and across exposure trials with the same CSs provide a more appropriate
index of the potential for expectancy violation and extinction learning. Prior
to exposure, patients should give an expectancy rating for a given feared out-
come on a 0-to-100-point scale, where 0 represents the belief that the feared
outcome is not at all likely to happen and 100 is entirely certain the feared outcome
will happen. This rating can be assessed by asking the question “How likely is
it that what I am/you are most worried about will occur?” Using the same
rating anchors, the postexposure expectancy level can also be assessed by
asking, “Imagine you repeated the same exposure practice. How likely is it
that what I was/you were most worried about before will occur this time?”
Self-reported expectancy ratings may not provide a complete representa-
tion of achieved extinction learning during exposure therapy. Additional
measurement methods need to be developed and adopted for a more accurate
index of inhibitory learning that will aid therapists in clinical decision making.
Inhibitory Learning 277
EMPIRICAL SUPPORT
exposure trials and across studies (see Craske et al., 2014, for a more detailed
explanation). Although these results are currently inconsistent, the general
consensus remains that safety signals and behaviors should be removed sys-
tematically over the course of exposure therapy (Hermans et al., 2006).
Strategies that increase retrievability of extinction learning possess less
consistent results than strategies that enhance extinction learning. Multiple
contexts have been shown to offset context renewal in human laboratory
studies (e.g., Balooch & Neumann, 2011; Balooch, Neumann, & Boschen,
2012) and in a clinical analog study of exposure therapy (Vansteenwegen
et al., 2007). However, one conditioning study with rodents (Bouton, García-
Gutiérrez, Zilski, & Moody, 2006) and another conditioning study with humans
(Neumann, Lipp, & Cory, 2007) failed to demonstrate detectable benefits of
multiple contexts throughout extinction on context renewal, suggesting that
the effects may be unstable. Similarly inconsistent results have been observed
regarding retrieval cues. Mental reinstatement of prior extinction learning
was demonstrated to limit context renewal in spider-phobic individuals
(Mystkowski et al., 2006). The effects of retrieval cues, such as distinctive pen
and clipboard, were found to be very weak in one study for public-speaking-
phobic individuals (Culver, Stoyanova, & Craske, 2011).
In sum, findings from basic research and treatment studies largely support
methods that enhance inhibitory learning (e.g., deepened extinction, occa-
sional reinforcement). Strategies that are geared toward enhancing retrieval
of extinction learning currently show inconsistent results in a limited number
of studies. Overall, additional translational research in clinical samples is nec-
essary to examine the extent to which inhibitory learning-based exposure
strategies enhance treatment outcomes or outperform traditional habituation-
focused exposure therapy.
TROUBLESHOOTING
Avoidance
treatments are designed to help the patient approach situations that have been
avoided. Patients are likely to engage in avoidance behaviors during exposure
treatment, resulting in an insufficient response or nonresponse to exposure
therapy.
Avoidance of feared stimuli during exposure therapy may be conspicuous
and easily identified by the therapist. Most commonly, patients engaging in
avoidance return to session with unfinished exposure assignments. Similarly,
to reduce the likelihood of a given feared outcome, patients engaging in avoid-
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ance may only partially complete exposure assignments. For example, a patient
with panic disorder may be absolutely certain that hyperventilating for 1 minute
will result in a stroke. To violate this expectation, the patient’s therapist assigns
the patient to hyperventilate in 15-second intervals for 2 minutes as a take-
home exposure assignment. The patient returns next session reporting that they
completed the assignment but were able to hyperventilate for only 45 seconds.
In this example, the avoidance has reduced the potency of the learning expe-
rience because the patient did not exceed the duration that was defined to
result in a stroke (i.e., 1 minute). As a result, the patient’s new inhibitory
associations formed from the exposure were restricted and extinction learn-
ing suboptimal when compared with the initial planned exposure.
Patients may also engage in discreet avoidance or escape behaviors during
a given exposure trial. These behaviors may not be as easily observed and
therefore require therapists to watch attentively for their potential interfer-
ence. A common inconspicuous avoidance behavior often shown by patients
with anxiety disorders during an exposure is shifting attention away from
feared stimuli. In the absence of engagement with a feared stimulus, an indi-
vidual is likely to not notice whether or not the negative event they expected
even occurred. Unquestionably, this behavior compromises the development
of new inhibitory learning. Several studies in anxious adults have shown that
individuals who selectively attend toward threat (e.g., Price, Mehta, Tone, &
Anderson, 2011) or demonstrate greater difficulty disengaging from threaten-
ing stimuli (Barry, Sewart, Arch, & Craske, 2015) in laboratory tasks prior to
CBT show greater improvement of symptoms when compared to those who
show no bias or avoid threat.
For example, individuals with severe social anxiety may avoid eye contact
with other individuals as a safety behavior. As aforementioned, abstaining
from eye contact with others allows socially anxious persons to avoid salient
behavioral indicators of rejection, such as squinted eyes or a furrowed brow,
and may reduce distress associated with the event—which is likely to have an
added predictive value of rejection (e.g., “If I make eye contact, I will see
someone is judging me, which will make me anxious. This anxiety will lead
me to blush and stutter during the conversation. If I blush and stutter, people
will think I’m weird and reject me”). Thus, expectancy violation is limited
during an exposure in which avoidance of eye contact is employed by a
socially anxious patient. Individuals with specific phobia are likely to avoid
looking directly at phobic stimuli. Similarly, persons with panic disorder may
avoid internal physiological sensations related to panic by shifting their atten-
tion to other stimuli, internal or external.
280 Sewart and Craske
behaviors that may reduce expectancy and interfere with new learning.
When new avoidance behaviors are identified, therapist and patient should
discuss how to monitor, reduce, and eliminate their future occurrence.
After the conclusion of exposure therapy, the return of previously extin-
guished fear responses is not uncommon. However, return of fear posttreat-
ment is problematic only when accompanied by escape or avoidance
behaviors. Return of fear itself is a transient state with limited clinical impli-
cations (Craske et al., 2018). In the absence of escape or avoidance, return of
fear is followed by additional experience that provides extinction learning
and eventual fear reduction. Prior to the conclusion of exposure therapy,
therapists should highlight the inevitability of residual anxiety and stress to
patients that continued exposure practice to feared stimuli following treat-
ment is essential in maintaining treatment gains.
CONCLUSION
(Craske et al., 2008, 2014; Rescorla & Wagner, 1972). Development of CS–
noUS associations must occur to inhibit—not erase—existing excitatory asso-
ciations (CS–US) that are responsible for maladaptive fear responding and
anxiety (CR). To maximize treatment outcomes and maintain long-term
gains, this theoretical understanding of exposure therapy requires clinicians
to emphasize therapeutic strategies that increase inhibitory learning. Such
strategies translated from basic associative learning theory include expec-
tancy violation, immediate removal of safety behaviors and signals, stimulus
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