Download The Return of Extinguished Conditioned Behaviour in Humans: New

Griffith Research Online
https://research-repository.griffith.edu.au
The Return of Extinguished Conditioned
Behaviour in Humans: New Research and
Future Directions
Author
Neumann, David, Boschen, Mark, Waters, Allison
Published
2008
Book Title
Biological Psychology: New Research
DOI
http://books.google.com.au/
Copyright Statement
With permission from Nova Science Publishers Inc. The attached file is reproduced here in accordance
with the copyright policy of the publisher. Reprinted from: Biological Psychology: New Research,
Chapter 10, The Return of Extinguished Conditioned Behaviour in Humans: New Research and Future
Directions, pages 17-56, copyright 2008, and Neumann, et. al.
Downloaded from
http://hdl.handle.net/10072/23364
Link to published version
https://www.novapublishers.com/catalog/product_info.php?products_id=8447
The Return of Extinguished Conditioned Behaviour
Running head: Return of Extinguished Conditioned Behaviour
The Return of Extinguished Conditioned Behaviour in Humans: Research findings
and Clinical Implications
David L. Neumann, Mark J. Boschen, & Allison M. Waters
School of Psychology, Griffith University
1
The Return of Extinguished Conditioned Behaviour
2
ABSTRACT
The last five years has seen an explosion of interest in research on the return of
extinguished conditioned behaviour in humans. This interest has resulted from the
development of theoretical models of the phenomenon from non-human animal
research and the potential application that the research has to explaining relapse
following extinction-based treatments for psychological disorders. The recent
research conducted with human participants is reviewed. The main return of
conditioned behaviour phenomena are renewal, reinstatement, spontaneous recovery,
and reacquisition, although recent human research has tended to focus on only the
first two. Human research has employed three main paradigms in the laboratory: fear
conditioning procedures, a conditioned suppression task, and causal learning tasks.
The basic effects of renewal, reinstatement, and spontaneous recovery have been
demonstrated in these tasks and in psychophysiological, behavioural, and subjective
measures. However, research has also yielded some inconsistencies among measures
as well as differences between the results obtained with human participants and those
obtained with non-human animals. There may be some unique factors that mediate the
return of extinguished conditioned behaviour in humans. Clinical studies on anxiety
and substance dependence have also confirmed that renewal, reinstatement, and
spontaneous recovery are potentially important mechanisms that may underlie relapse
following extinction-based treatments. There is a clear need for future research to
understand the psychological mechanisms behind the return of extinguished
conditioned behaviour in humans and to develop ways to reduce its occurrence in
clinical treatment.
The Return of Extinguished Conditioned Behaviour
3
INTRODUCTION
The discovery that extinguished conditioned responses could reappear at a
later time was made by Pavlov (1927) when he observed spontaneous recovery in his
experiments with dogs. Research on other means by which conditioned responses can
return following extinction in animal subjects, such as renewal and reinstatement,
began to develop momentum in the late 1970’s (e.g., Bouton & Bolles, 1979;
Rescorla & Heth, 1975). However, it has only been recently that these phenomena
have been studied in humans. Despite the late start, human research is accelerating at
an astounding rate. The number of published reports on renewal, reinstatement, and
spontaneous recovery in humans numbered fewer than one per year between 1995 and
2000. In the years 2001 to 2005, this number increased to just over two per year. In
the years subsequent to 2005, there have been over 5 per year published reports to
date. The recent surge of work on the return of extinguished conditioned behaviour
indicates that it is a significant new direction in biological psychology research.
The reasons why the return of extinguished conditioned behaviour in humans
is attracting increasing interest are not hard to find. The most obvious is that it has
important implications for our theoretical understanding of the acquisition and
extinction of conditioned responses. For instance, the fact that extinguished
conditioned responses can reappear at a later time suggests that extinction does not
erase the original learning (e.g., Bouton, 2002; 2004; Bouton, Westbrook, Corcoran &
Maren, 2006). It also suggests that learning does not occur in a vacuum, but can be
influenced by a constellation of contextual factors ranging from the physical
environment, the passage of time, physical states, and psychological mood states.
Similarly, it suggests that our memories can be influenced by contextual cues that are
present during their formation or recall (Bouton, 1993). Research on the topic
The Return of Extinguished Conditioned Behaviour
4
facilitates cross-species comparisons of learning phenomena by determining the
extent to which the many discoveries made in experiments using non-human animals
applies to humans. There are important clinical implications because the fundamental
process of extinction has been applied in the treatment of psychological disorders
such as anxiety disorders and substance dependence disorders. Relapse remains as an
ever present danger when extinction is used in therapy and increasing our
understanding of what factors mediate the return of extinguished conditioned
behaviour has the potential to produce greater long-term benefits of therapy (Bouton,
2000; 2002).
The present chapter will present a review of the human research on the return
of extinguished conditioned behaviour. It aims to complement similar reviews that
have largely examined non-human animal experiments (Bouton, 2002; 2004; Bouton,
Westbrook et al., 2006) by focussing specifically on experiments that use human
participants. It also updates and complements prior reviews of human research
(Hermans, Craske, Mineka, & Lovibond, 2006; Vansteenwegen, Dirikx, Hermans,
Vervliet, & Eelen, 2006) by incorporating newly published research and by drawing
from the experimental literature that has employed a conditioned suppression and
causal learning task in addition to the fear conditioning procedure. The examination
of the return of extinguished conditioned behaviour in clinical studies is also
considered. Before examining this research it is first necessary to define the relevant
terms and methods of Pavlovian conditioning. There are various procedures by which
a return of extinguished conditioned behaviour can be produced. The investigation of
these in research with human participants will be addressed in turn by first
considering studies conducted in the laboratory. The return of extinguished
conditioned behaviour in the treatment of anxiety disorders and alcohol dependency
The Return of Extinguished Conditioned Behaviour
5
are finally considered.
PAVLOVIAN CONDITIONING
Pavlovian (or classical) conditioning is a form of associative learning in which
the relationship is learned between two or more previously unrelated stimuli. In his
seminal work with laboratory dogs, Ivan Pavlov (1849-1936) first observed that when
the animals were presented with a salient unconditional stimulus (US) (e.g., meat), an
unconditional response (UR) (e.g., salivation) was elicited. Moreover, he further
observed that if a neutral conditional stimulus (CS) (e.g., a tone) was paired with the
presentation of the meat US, the animals began to show a conditional response (CR)
of salivation to the tone CS. Thus, the tone CS initially induced no response, but when
an association between the CS and US was learnt after repeated pairings, the tone CS
on its own became capable of eliciting a CR. Since Pavlov’s influential work,
Pavlovian conditioning models have been used to explain a wide range of human
behavioural phenomena, including drug addiction (e.g., Drummond, Tiffany, Glautier,
& Remington, 1995), taste aversion (e.g., Rosas & Bouton, 1998), and fear learning
(e.g., Bouton, Mineka & Barlow, 2001). Indeed, the conditioning of emotional
responses such as fear is a central component of contemporary learning models of the
development of phobias and other anxiety disorders (e.g., Mineka & Zinbarg, 2006).
Conditioned responses can manifest in various ways including physiological
changes, such as those seen by Pavlov in the salivation volume of laboratory animals
or in the magnitude of skin conductance responses and changes in heart rate of
humans (e.g., Neumann & Waters, 2006). Emotional changes may also occur, such as
increased euphoria or increased fear levels. While the emotional changes can be
reflected in physiological responses, they may also be measured in human participants
The Return of Extinguished Conditioned Behaviour
6
by subjective ratings. Cognitive changes can occur in which there are increased
attentional demands and a higher expectation of the US during the CS presentation.
The cognitive changes can be measured through secondary task reaction time slowing
and ratings of the expectancy of the US, among others. Finally, behavioural changes
may also take place, such as avoidance behaviour in humans and other animals
(Davey, 1992; Dawson & Schell, 1985; Öhman, Hamm & Hugdahl, 2000).
Pavlovian conditioning protocols have typically been designed in one of two
ways. During simple or single cue conditioning, a neutral CS is paired repeatedly with
the salient US and within-subject conditioned responses are recorded over consecutive
trials (see Lissek et al., 2005 for review). The single cue conditioning procedure
requires the use of a control group that receives random pairings of the CS and US in
order to establish that the development of conditioned responses in the conditioning
group reflects associative processes. In discrimination or differential conditioning,
two CSs are presented. One CS is repeatedly paired with the salient US (i.e., CS+
trials) while the other CS is consistently presented alone (CS-). The development of
conditioned responses in the differential conditioning procedure can be indexed
through a within-subjects comparison of the difference in magnitude of responses to
the CS+ and to the CS-. The differential conditioning procedure can permit the
examination of both excitatory processes (i.e., conditioned responding on CS+ trials)
and inhibitory processes (i.e., capacity to inhibit conditioned responding to the safety
cue heralded by the CS- and during extinction) (see Lissek et al., 2005).
Pavlovian conditioning protocols involve two key components. The first
described above, in which a neutral CS is repeatedly paired with a salient US, is
referred to as acquisition. The CS acquires the ability to elicit a CR. The second
important component of Pavlovian conditioning is the demonstration that acquired
The Return of Extinguished Conditioned Behaviour
7
conditioned responses can be extinguished. Extinction of the CR occurs when the CS
is no longer paired with the salient US event, but is presented on its own. The
magnitude of CRs gradually diminishes over repeated presentations of the CS alone
until it is extinguished all together. Extinction is used as the cornerstone for
behavioural treatments of a range of psychological disorders. For instance, in
exposure therapy for simple phobia, the patient is repeatedly exposed to the feared
object until the fear response has diminished.
It is now widely accepted that the extinction of CRs does not result in a
“destruction” of the CS-US association formed during acquisition (see Bouton, 2004,
2004). Rather, extinction reflects new learning whereby the CS essentially has two
meanings – one that is associated with the US (i.e., a CS-US association) and one that
is not (i.e., a CS-noUS association). The fact that the CS-US association remains
intact means that there is always the potential that a return of conditioned behaviour
can occur following extinction. All that is required is that there is retrieval of the
original CS-US association (Bouton, 2002).
THE RETURN OF EXTINGUISHED CONDITIONED BEHAVIOUR
An extensive body of research on extinction has shown that there are four
mechanisms by which extinguished conditioned behaviour can return. All four
mechanisms are also potential explanations for why relapse can occur after successful
extinction in clinical treatments (i.e., exposure treatments). These mechanisms are (a)
renewal, (b) reinstatement, (c) spontaneous recovery, and (d) reacquisition. Each
highlights that extinction does not destroy the original learning about the CS-US
association (Bouton, 2002, 2004; Bouton et al., 2006). Moreover, they indicate that
the ambiguity that surrounds the CS after extinction is resolved by reference to other
The Return of Extinguished Conditioned Behaviour
8
cues that are present. For instance, if a concurrent cue promotes the retrieval of the
CS-US association learnt during acquisition, conditioned behaviour will result. On the
other hand, if the cue promotes retrieval of the CS-noUS association learnt during
extinction, the extinction of conditioned responses will persist.
Cues that are present in the context in which the CS is encountered may be
particularly important in whether conditioned behaviour is observed (Bouton, 2002,
2004; Bouton et al., 2006). Contextual stimuli can be wide and varied and may
include aspects of the physical environment in which conditioning and extinction
takes place, the passage of time following extinction, or factors related to the
organism itself during and after extinction. A useful distinction is between those
contexts that are exteroceptive and those that are interoceptive (Bouton, 2002).
Exteroceptive contexts are those that are external to the organism and may include
sights, sounds, smells, drug paraphernalia, and billboard advertisements, to name a
few. Interoceptive contexts are those that are internal to the organism and may include
drug states, emotions, physiological changes, cognitions, and the passage of time
(e.g., Bouton & Schwartzentruber, 1991; Bouton, Mineka, & Barlow, 2001; Bradizza,
Stasiewicz, & Maisto, 1994; Collins & Brandon, 2002).
The mechanism of renewal suggests that the reduction of conditioned
behaviour that occurs during extinction depends on the degree of learning that takes
place about the extinction context itself. In the typical renewal effect, conditioning
takes place in context A (e.g., laboratory chamber A), extinction training takes place
in context B (e.g., a different laboratory chamber B), and once the conditioned
behaviour has been extinguished, the CS is presented alone but this time in Context A.
The return to the original conditioning context (i.e., context A) typically ‘renews’
responding to the CS (e.g., Bouton & Bolles, 1979; Bouton & King, 1983; Bouton &
The Return of Extinguished Conditioned Behaviour
9
Peck, 1989; Harris, Jones, Bailey & Westbrook, 2000; Rauhut, Thomas & Ayres,
2001). Although ABA renewal (i.e., conditioning in Context A, extinction in Context
B, and retesting in Context A) is the most widely studied renewal procedure, renewal
can also occur when retesting is conducted in a third, different context (i.e., Context
C; ABC renewal) (e.g., Bouton & Bolles, 1979; Bouton & Brooks, 1993; Gunther,
Denniston & Miller, 1998; Harris et al., 2000). Although not as strong as ABA
renewal (Harris et al., 2000), ABC renewal highlights that the mere removal of the CS
from the extinction context can cause a return of the conditioned behaviour. Both
ABA and ABC renewal effects are stronger than those observed during an AAB
paradigm in which conditioning and extinction occur in context A and retesting
occurs in context B (see Bouton, 2002).
Overall, renewal effects are strong and robust, with the original learning that
takes place during conditioning impermeable to extensive extinction training (e.g.,
even after as many as 160 extinction trials) (Gunther et al., 1998; Rauhut et al., 2001).
Renewal has also been demonstrated in relation to a wide range of behavioural
phenomena, including fear conditioning (e.g., CS associated with a shock), appetitive
conditioning (e.g., CS associated with food) (e.g., Brooks & Bouton, 1994), and taste
aversion conditioning (e.g., food CS associated with illness) (e.g., Rosas & Bouton,
1998) and in a variety of animal species.
Reinstatement refers to the return of conditioned behaviour that occurs with
re-exposure to the US alone after extinction has taken place. The typical reinstatement
procedure involves a conditioning session in which the CS (e.g., a light) is repeatedly
paired with the US (e.g., a shock), and then extinction of the conditioned behaviour is
achieved by multiple exposures to the light CS alone. In another session, the shock
US is presented several times on its own, followed by a separate test session often 24
The Return of Extinguished Conditioned Behaviour
10
hours later or longer, in which the light CS is presented alone. During this final test
phase, the conditioned behaviour that was previously extinguished is observed to
recur to the light CS.
Bouton and others have shown repeatedly that reinstatement is strongest when
the test trials (i.e., when the CS is represented after the US alone presentations) are
given in the same context in which re-exposure to the US takes place (e.g., see
Bouton, 2002 for review). For example, in fear conditioning experiments with rats,
the context is typically the laboratory chamber in which re-exposure to the shock US
occurs. During re-exposure to the shock US, the rat associates the shock with the reexposure context (i.e., the laboratory chamber). This contextual conditioning or
formation of a new association is what triggers reinstatement of conditioned fear
responses when the light CS is subsequently presented again during the test trials.
This might occur if the context-US association promotes retrieval of a CS-US
association when the CS is encountered in that context.
Bouton and colleagues have also demonstrated that the extent of reinstatement
depends on the strength of the subjects “knowledge” about the context formed during
conditioning (e.g., Bouton, 1985; Bouton & King, 1983); the stronger the association,
the greater the likelihood that reinstatement will occur. He also points out that
conditioned fear associated with the original conditioning context is unlikely to
potentiate a fear response to a different CS that has not been extinguished (e.g.,
Bouton, 1984; Bouton & King, 1983). Thus, Bouton argues that extinguished CSs are
particularly vulnerable to reinstatement, possibly because their meaning has become
ambiguous.
More recent research (e.g., Westbrook, Iordana, McNalley, Richardson &
Harris, 2002) suggests that reinstatement can also occur due to another context-
The Return of Extinguished Conditioned Behaviour
11
learning effect, this time, between the CS and the context in which extinction took
place. When the shock US is presented in the same context in which extinction
occurred, competing associations of tone-context and shock-context are formed.
These findings suggest that if a particular context has become associated with an
aversive event for whatever reason, conditioned fear responses can be reinstated.
Thus, whereas Bouton’s earlier work suggested that the test trials (i.e., re-exposure to
the CS) must occur in the same context as where the shock US was presented for
reinstatement to occur, this more recent work suggests that reinstatement can occur in
any context providing that the context in which extinction took place is subsequently
associated with an aversive event.
Spontaneous Recovery is the most well-known process to occur after
extinction with observations of this behavioural phenomena dating back to the
seminal work of Pavlov with laboratory dogs (e.g., Pavlov, 1927). This effect reflects
that if time elapses after extinction training (e.g., the elimination of salivation by
laboratory dogs to a tone CS presented repeatedly without the meat US), the
extinguished salivation response can reoccur spontaneously when the tone CS is
presented again some time later. Moreover, initial responding to the CS during the test
trials can be as strong as that observed at the end of conditioning (e.g., Brooks &
Bouton, 1993).
Although there are numerous explanations of spontaneous recovery (e.g.,
Davenport, Hill, Wilson, & Ogden, 1997; Robbins, 1990), Bouton (2002, 2004)
proposes that as the passage of time represents a gradually changing context,
extinction may be specific to the physical context in which it occurs as well as to the
context of time. Thus, Bouton (2004) likened spontaneous recovery to the renewal
effect that occurs when the CS is tested in a new temporal context. Moreover, in both
The Return of Extinguished Conditioned Behaviour
12
spontaneous recovery and renewal paradigms, if a retrieval cue that reminds the
subject of extinction (through brief presentations of a retrieval cue during the
extinction session), is presented just before the test trials, return of the conditioned
behaviour is reduced (see Brooks, 2000). These results suggest that spontaneous
recovery and renewal represent a failure to retrieve extinction information in contexts
(whether physical or temporal) that are outside the original extinction context
(Bouton, 2002).
Reacquisition refers to the pairing of the CS and the US again after extinction
has taken place. Reacquisition after extinction may occur either rapidly, almost as if
extinction never occurred (Napier, Macrae & Kehoe, 1992) or slowly after numerous
re-pairings of the CS and US after extinction (Bouton and Schwartzentruber, 1989;
Calton, Mitchell, & Schachtman, 1996; Ricker & Bouton, 1996). Bouton (2002)
explains that variation in the rate of reacquisition depends on whether context cues
present during the test trials lead to the retrieval of conditioning or extinction
associations; the former resulting in rapid reacquisition, the latter resulting in slow
reacquisition. Thus, the rate and strength of reacquired conditioned responses depends
on the unique interaction of various types of contextual cues.
Our understanding of renewal, reinstatement, spontaneous recovery, and
reacquisition has been built up through extensive research with non-human animal
subjects. From this research, the notion of ambiguity and the important role of
exteroceptive, interoceptive, and temporal contexts on mediating the return of
extinguished conditioned behaviour has been established (Bouton, 2002, 2004). Given
the generality of Pavlovian conditioning processes across all organisms, including
humans, the investigation of renewal, reinstatement, and related phenomena in
humans has the potential to increase our understanding further. Moreover, the
The Return of Extinguished Conditioned Behaviour
13
relevance of the various phenomena as a potential explanation for relapse following
extinction-based behavioural treatments provides a practical justification for research
to be conducted in the human laboratory and in the clinical treatment context.
PROCEDURES USED TO STUDY RETURN OF EXTINGUISHED
CONDITIONED BEHAVIOUR IN THE HUMAN LABORATORY
Laboratory research has investigated renewal, reinstatement, and spontaneous
recovery in humans using three main experimental procedures: a fear conditioning
procedure, a conditioned suppression procedure, and a causal learning procedure. The
distinction between these different procedures is important because they may use
different types of stimuli as the CS and US, different modes of stimulus presentation,
and measure conditioned responses in different ways. The different procedures also
offer different levels of parallels to the methods by which conditioning is studied in
the laboratory with non-human animals or in the clinic to study fears and
dependencies in humans. It is essential that the various return of conditioned
behaviour phenomena be examined with more than one paradigm to ensure that the
results obtained are not overly specific to the particular methods in the learning
paradigm used.
The fear conditioning procedure (e.g., Alvarez, Ruben, Johnson & Grillon,
2007; Dirikx, Hermans, Vansteenwegen, Baeyens & Eelen, 2007; Neumann, Lipp &
Siddle, 1997; Neumann et al., 2007), sometimes also referred to as an aversive
conditioning procedure (e.g., Neumann & Waters, 2006), uses an aversive and
biologically salient stimulus as the US. The stimulus most commonly employed is a
mild electric shock presented to the participant’s arm or hand at an intensity that is
The Return of Extinguished Conditioned Behaviour
14
subjectively defined by the participant as “unpleasant, but not painful”. A loud tone
may also be used (LaBar & Phelps, 2005). It is common that fear conditioning
procedures employ a differential conditioning protocol (Öhman et al., 2000). The
differential conditioning procedure provides a within-subjects control to measure the
strength of conditioning. Only the CS+ should be expected to elicit conditioned
responses and a subsequent recovery of extinguished conditioned responses because
this stimulus and not the CS- was associated with the aversive US.
The fear conditioning procedure provides a strong procedural parallel to fear
conditioning procedures used in non-human animal experiments. This is particularly
the case with the use of an electric shock US in both applications. However, the
measurements of conditioned responses are different in the human studies. The skin
conductance response (e.g., Neumann, Lipp, & Siddle, 1997, 2002), which reflects the
activity of the eccrine sweat glands that are under the control of the sympathetic
nervous system, provides a key measure of the increases in arousal that are associated
with the conditioned response. In addition, potentiation of the startle blink reflex
during CSs associated with an aversive stimulus (e.g., Alvarez et al., 2007) provides a
second psychophysiological measure related to emotion (Lipp, Neumann, & Mason,
2001; Lipp, Neumann, Siddle, & Dall, 2001) that has been employed in research.
Although the startle reflex is sensitive to attentional processes (Lipp & Neumann,
2004; Lipp, Neumann, & McHugh, 2002; Lipp, Neumann, & Pretorius, 2003;
Neumann, 2002; Neumann, Lipp, & McHugh, 2004; Neumann & Lipp, 2003;
Neumann, Lipp, & Pretorius, 2004) it can provide a direct measure of fear because of
the involvement of the amygdala in the startle fear circuit (Angrilli et al., 1996;
Hitchcock & Davis, 1986). Startle potentiation is a commonly employed measure of
fear in non-human animal research and provides a promising means for cross-species
The Return of Extinguished Conditioned Behaviour
15
comparisons to be made. Self-reported expectancy of the US, either given on-line
(e.g., Neumann et al., 2007) or after a block of trials (e.g., Hermans et al., 2005),
ratings of fear (e.g., Dirikx et al., 2004), and performance on a secondary reaction
time task (e.g., Dirikx et al., 2004), provide additional measures to supplement the
physiological measures. While it is assumed that all these measures will show similar
effects in the return of conditioned fear, dissociations among them have also been
found (e.g., Hermans et al., 2005), suggesting that they may be differentially sensitive
to the various psychological processes that underlie conditioned fear.
The conditioned suppression task differs from the fear conditioning procedure
by measuring conditioned responses through a behavioural procedure. The task was
originally developed with the aim of providing a procedural parallel to the
measurement of conditioned suppression in non-human animal studies. In these
studies, animals are first trained through operant conditioning methods to depress a
lever to obtain a food or drink reward. Conditioning trials are next given in which a
CS is paired with an aversive US (e.g., shock). The aversive US presentations produce
the UR of suppressing the operant bar pressing. Following conditioning, presentations
of the CS on its own will elicit the suppression of the bar pressing and extinction of
the suppression can also be produced by presenting the CS on its own. A return of
extinguished conditioned suppression has been observed in animal subjects with this
procedure (Bouton, 1984; Bouton & Bolles, 1979; Johnson, Baker, & Azorlosa, 2000;
Wilson, Brooks, & Bouton, 1995).
To provide a human analogue to the measurement of conditioned suppression
in humans, Arcediano, Ortega, and Matute (1996) developed a task that used a game
format presented on a computer. The game involves the steady presentation of
“Martians” in rows across the computer screen. Participants are trained to press a
The Return of Extinguished Conditioned Behaviour
16
button, which in the context of the game fires a “laser gun”, at a steady rate to destroy
each Martian. However, the Martians are said to have a “laser shield”. If participants
fire the laser gun when the shield is activated, as indicated by the screen flashing on
and off intermittently, it has the consequence of allowing a large number of Martians
to appear on the screen. In the context of the game, the laser shield functions as the
US and participants can learn to predict when the shield is about to occur by CSs that
appear on the screen immediately before the shield. If participants withhold firing the
laser gun during the CS presentations, they will avoid firing when the shield is
activated and so prevent a flood of Martians appearing on the screen. The conditioned
suppression during the CS thus occurs due to the anticipated punishment within the
context of the task, rather than due to fear of an impending aversive US (Havermans,
Keuker, Lataster & Jansen, 2005). Nevertheless, the conditioned suppression task
provides a non-verbal behavioural measure of conditioning that has been applied to
study renewal and reinstatement in humans (Havermans et al., 2005; Neumann, 2006,
2007).
The final task that has been used in laboratory research is a causal learning
task (e.g., García-Gutiérrez & Rosas, 2003; Vila & Rosas, 2001). In this task,
participants are presented with a fictitious scenario in which events or stimuli are
followed by positive consequences, negative consequences, or no consequence.
Participants are asked to make judgments on the likelihood that certain consequences
will follow the stimuli. In one task used to investigate reinstatement, for example,
participants assumed the role of a healthcare inspector to investigate a problem in
which people developed a stomach ache after ingesting medicines bought at
importation pharmacies (Villa & Rosas, 2001). There are good reasons to assume that
the acquisition of causal judgments based on hypothetical situations and fictitious
The Return of Extinguished Conditioned Behaviour
17
stimuli reflects Pavlovian conditioning processes (see Dickson, 2001). The causal
learning task thus has the potential to contribute to our understanding of the return of
extinguished conditioned behaviour in humans.
LABORATORY RESEARCH FINDINGS ON THE RETURN OF EXTINGUISHED
CONDITIONED BEHAVIOUR IN HUMANS
Laboratory research on the return of extinguished conditioned behaviour has
largely focussed on renewal, reinstatement, or spontaneous recovery in humans. Few
studies in the human laboratory have investigated these phenomena in combination,
such as question of whether renewal and reinstatement have an additive effect
(Garcia-Gutierrez & Rosas, 2003). Such research would be enlightening given the
suggestion that the various phenomena have been suggested to reflect a similar
underlying mechanism of the highly context-dependent nature of extinction learning
(Bouton, 2002; 2004). Due to the fact that renewal, reinstatement, and spontaneous
recovery have largely been examined in isolation, the review below will address each
of these phenomena in turn.
Renewal
The renewal of extinguished conditioned behaviour in humans has been
reliably demonstrated with a variety of conditioning procedures. ABA renewal has
been observed in a causal learning task (Garcia-Gutierrez et al., 2005; Paredes-Olay &
Rosas, 1999; Rosas & Callejas, 2006). ABA renewal has also been observed with the
conditioned suppression task with two different context manipulations (Havermans et
al., 2005; Neumann, 2006, 2007). The fear-conditioning procedure has also yielded
reliable evidence of renewal in several measures of conditioned responding, including
skin conductance responses (e.g., Alvarez et al., 2007; Effting & Kindt, 2007;
The Return of Extinguished Conditioned Behaviour
18
Neumann & Longbottom, submitted; Vansteenwegen et al., 2005; Vervliet et al.,
2005), startle blink reflexes (Alvarez et al., 2007), ratings of the expectancy of the US
(e.g., Neumann et al., 2007; Neumann & Longbottom, submitted; Vansteenwegen et
al., 2005), and fear-ratings of the CS (e.g., Alvarez et al., 2007). The majority of
demonstrations of renewal have used within-session manipulations of context.
However, renewal may also be found when testing sessions are separated by a longer
period of time. Renewal of skin conductance responses has been found during a
renewal test when participants were tested 24 hours after the acquisition and
extinction phases (Milad, Orr, Pitman, & Rauch, 2005). The various demonstrations
across the different tasks and measures indicate that a context change after extinction
can result in the return of extinguished conditioned behaviour in humans.
Effects of Nature of CSs and Contexts on Renewal
In addition to the various conditioning procedures and measures that have
yielded renewal in humans are the various types of CSs and contexts. Most
demonstrations of renewal have used neutral CSs as stimuli, such as geometric shapes
(Neumann, 2006; Neumann et al., 2007), line drawings of faces (Vansteenwegen et
al., 2005), or a tone (Havermans et al., 2005). The context changes have also been
varied. Changing the perceptual features of the CS from a tall and thin parallelogram
to a short and thick parallelogram has produced a renewal type effect (Vervliet et al.,
2005). Renewal has also been found when the background colour and the direction at
which the stimuli appear on a computer screen are varied in the conditioned
suppression task (Havermans et al., 2005). However, contextual stimuli in the
laboratory environment is often conceptualised to be broader in scope to include the
background milieu of stimuli, such as the sights, sounds, and smells present in the
laboratory. Context changes that are consistent with this broader notion have also
The Return of Extinguished Conditioned Behaviour
19
produced renewal in humans. For instance, changing the illumination of the room
from dark to light (Vansteenwegen et al., 2005) and using different coloured lights
(Effting & Kindt, 2007) and combinations of colours lights and background sounds
(Neumann, 2006, 2007; Neumann et al., 2007) has resulted in renewal. A particularly
novel way to manipulate context is to use a virtual reality environment. Using this
technology, a renewal of extinguished conditioned responses has been observed
(Alvarez et al., 2007).
While research with humans has largely focussed on changes in the
exteroceptive context that may accompany acquisition and extinction, context may
also be conceived as broader still, by encompassing the states associated with the
organism itself. The return of extinguished conditioned behaviour has been
demonstrated in animal subjects by using interoceptive contexts (Bouton, 2002) such
as deprivation state (e.g., Davidson, 1993), hormonal state (e.g., Ahlers & Richardson,
1985), and drug state (e.g., Bouton, Kenney & Rosengard, 1990; Cunningham, 1979).
Drug state associated with caffeine ingestion has been reported to function as a
contextual cue that can produce the renewal of spider fear in a clinical fear-reduction
procedure (Mystkowski, Mineka, Vernon, & Zinbarg, 2003). However, the effects of
interoceptive contexts in producing renewal in the human laboratory remains to be
explored. Related research has shown that mood state can influence memory in
human participants (Eich, 1995). Taking the findings together, it would be expected
that changes in interoceptive contexts would produce renewal effects in human
laboratory studies of conditioning.
As noted earlier, research on renewal in humans has tended to use CSs and
contexts that are neutral in nature (e.g., geometric shapes and different coloured
lights, respectively). In a departure from this methodology, Neumann and
The Return of Extinguished Conditioned Behaviour
20
Longbottom (submitted) compared fear-relevant and fear-irrelevant CSs presented as
images upon natural or artificial contexts in a fear conditioning procedure with an
ABA renewal design. Fear-relevant stimuli are those stimuli that show a bias to be
associated with an aversive outcome and include predatory and poisonous animals
(Öhman & Mineka, 2001). Such stimuli may have been more likely to have
endangered our ancestors and may explain why phobias to threatening organisms,
such as spiders and snakes, are more common than are phobias to modern stimuli,
such as cars and electrical outlets (Hugdahl & Johnsen, 1989). In their first
experiment, a renewal of skin conductance responses and expectancy of the US was
found when images of spiders and snakes were used as the CSs. Renewal was also
found in a group that received flowers and mushrooms, which are examples of fearirrelevant stimuli, as the CSs. The results showed that a renewal effect can be found
for fear-relevant stimuli in an experimental procedure that also produces renewal with
neutral fear-irrelevant stimuli.
A second important empirical question is whether the magnitude of the
renewal effect differs between fear-relevant and fear-irrelevant CSs. Fear-relevant
stimuli have previously shown resistance to extinction, that is, a slower rate of
extinction of conditioned fear than fear-irrelevant stimuli (Fredrikson, Hugdahl, &
Öhman, 1976; Hugdahl, Fredrikson, & Öhman, 1977; Öhman, Fredrikson, Hugdahl,
& Rimmo, 1976). Although fear-relevant stimuli will extinguish provided that a
sufficient number of extinction trials are given, the different rates of extinction imply
that there may be different processes that underlie extinction in fear-relevant and fearirrelevant stimuli and that these may influence the amount of renewal observed. In
their second experiment, Neumann and Longbottom (submitted) did find a difference
in the size of renewal between fear-relevant and fear-irrelevant stimuli. Intriguingly,
The Return of Extinguished Conditioned Behaviour
21
this difference depended on the nature of the context that was used in the different
phases of the renewal procedure. Renewal was larger for fear-relevant stimuli when
acquisition used an indoor office context, extinction an outdoor bush context, and test
used an indoor office context. In contrast, renewal was larger for fear-irrelevant
stimuli when acquisition used an outdoor bush context, extinction an indoor office
context, and test used an outdoor bush context.
The results from Neumann and Longbottom’s (submitted) study do not appear
to support the idea that there is an overall effect of larger or smaller renewal with fearrelevant stimuli compared to fear-irrelevant stimuli. Instead, the authors suggested
that the results reflect the degree to which the participant’s expectancies were violated
during the different phases of the experiment. For instance, fear-relevant stimuli
presented in an outdoor bush context may represent a congruent context. An outdoor
bush context may be one in which people would be more likely to encounter fearrelevant stimuli and for such encounters to be associated with a negative outcome
(e.g., as in “snakes in the grass”). However, this expectation was violated in
participants that received extinction training with fear-relevant stimuli in the outdoor
bush context. This may have resulted in an ambiguity surrounding the fear-relevant
stimuli and increased attention to contextual cues that accompanied the CS
presentation. The increased salience of the contextual cues resulted in a larger renewal
effect during the test phase when the fear-relevant CS was presented in an indoor
office context. In contrast, acquisition trials of fear-relevant stimuli in an outdoor bush
context and extinction trials in an indoor office context may have made “sense” to
participants and produced less of a violation of expectancies and by consequence less
attention to contextual cues during extinction. This produced a relatively smaller
renewal effect in the test phase. While this explanation is speculative and requires
The Return of Extinguished Conditioned Behaviour
22
further investigation, their results do highlight that a complex interaction may occur
between the nature of the CS and context in producing the renewal effect. Moreover,
the renewal effect may also be influenced by the participants pre-existing biases or
expectations in relation to the stimuli that are used.
Effects of instructions on renewal
One way in which the participant’s expectations can be manipulated directly is
through explicit instructions regarding the contextual changes that are experienced
during the renewal procedure. Using a conditioned suppression task within an ABA
renewal design, Neumann (2007) gave participants instructions that aimed to devalue
the role of the context in the different phases of the experiment. Based on the notion
that the renewal effect reflects the context-specific nature of learning, particularly that
of extinction learning, it was hypothesised that using instructions that devalued the
role of contextual cues would attenuate renewal. However, instructing participants
prior to experiment that any changes in the meaning of the CS (i.e., whether it predicts
the US or not) are not related to changes in the context had no effect on renewal. In
addition, instructing participants in between the extinction and test phases that any
changes in the context they may have experienced are unrelated to whether the CS
predicts the US or not also did not attenuate renewal. The latter result also did not
appear to depend on whether a differential conditioning or a single cue conditioning
design was used. It could not also be attributed to the suggestion that participants did
not remember or believe in the instructions that they were given. The apparent
ineffectiveness of the instructions may be related to other factors yet to be determined.
Nevertheless, the results reported by Neumann (2007) suggest that contextual
cues are not easily ignored in a renewal procedure. This may be because after
extinction, the CS has become ambiguous and the only means by which to resolve the
The Return of Extinguished Conditioned Behaviour
23
ambiguity is by reference to contextual cues. If there are no other means by which to
resolve the ambiguity (e.g., alternative retrieval cues), renewal will result.
Alternatively, the results may suggest that non-cognitive processes may influence
renewal in humans. Such a non-cognitive explanation may be particularly relevant to
the conditioned suppression task given that the CS duration is short (1 – 3 s) and the
participants attention is partly distracted by the need to maintain a steady rate of
responding in order to destroy the Martians that appear at a rapid rate on the screen.
The instructions may be ineffective in such a situation, suggesting that replication of
this result to another conditioning procedure is required.
Comparisons among the various renewal designs
According to Bouton’s (Bouton, 1993, 2002, 2004) explanation of renewal, it
is the highly context specific nature of extinction learning that is the major factor in
producing renewal. Whenever the CS is encountered outside of the extinction context,
renewal can occur. This idea provides a parsimonious explanation for the observation
of renewal in the various ABA, ABC, and AAB procedures. All these procedures are
common in that test trials are conducted outside of the extinction context. Based on
these observations, it would be expected that given ABA renewal has been reliably
observed in human research, ABC and AAB renewal should also be found. However,
using a conditioned suppression task that reliably produced ABA renewal, no
evidence for ABC (Havermans et al., 2005; Neumann, 2006) or AAB renewal
(Neumann, 2004) has been found. In addition, no evidence for ABC renewal was
found in US expectancy ratings or skin conductance responses in a fear conditioning
procedure (Effting & Kindt, 2007). The finding of ABA renewal, but not ABC or
AAB renewal, suggests that that it is acquisition learning that is context specific such
that only a return to the original learning context will renew conditioned responding
The Return of Extinguished Conditioned Behaviour
24
(Havermans et al., 2005; Efftin & Kindt, 2007). Furthermore, a configural
CS+context stimulus may become associated with the US during acquisition and the
loss of responding observed during extinction reflects a generalisation decrement
(Havermans et al., 2005). The suggestion of the context specific nature of acquisition
may be seen as being at variance with the proposition that it is extinction learning that
is context specific.
The difficulty of finding evidence for ABC renewal to date may not be
surprising for two reasons. First, smaller ABC renewal than ABA renewal has been
reported in research with non-human animals (Harris et al., 2000). If renewal in an
ABC design is difficult to detect, stronger contextual manipulations or more sensitive
measures of conditioned behaviour may be required to observe renewal in humans.
Second, in the differential conditioning procedures that have been used to investigate
ABC renewal (Effting & Kindt, 2007; Neumann, 2006) a consistent finding has
emerged in that during the test phase an increase in conditioned responses during the
CS+ has been observed relative to the level of conditioned responding on the last
extinction trial. One might be tempted to take this finding as evidence of ABC
renewal. However, an increase in conditioned responses was also found for the CSon the first test trial relative to the last extinction trial. As a result, conditioned
responses to the CS+ has not been significantly higher than during the CS- during test,
although both have increased relative to that present at the end of extinction. The
ABC renewal design thus appears to produce a non-specific renewal of conditioned
responses to any CS that is presented during the test phase. Whether the increase can
also be found for a novel CS or if it is specific only to the CS+ and CS- for the test
phase will require further experimental research. Nevertheless, the ABC renewal
design may produce some non-specific renewal of conditioned responses in the test
The Return of Extinguished Conditioned Behaviour
25
phase.
The apparent renewal of conditioned responses to the CS- during the test
phase in an ABC design may be an example of a more general phenomenon when
context switches are made with a differential conditioning procedure. A similar,
though smaller, increase in responses to the CS- has also been found on the first
extinction trial after a change from the acquisition context (Effting & Kindt, 2007;
Neumann, 2006, 2007; Neumann & Longbottom, submitted) and on the first test trial
in an ABA renewal design (Effting & Kindt, 2007; Neumann, 2006; Neumann &
Longbottom, submitted). Basic associative learning models of conditioning would not
expect an increase in conditioned responding to the CS- to occur because this stimulus
had not been associated with the US during any phase of the experiment and as such
its associative strength should not change. One explanation could be that it reflects the
effects of US omission (Neumann, 2006). If the first trial of extinction or test is a CS+
trial, participants may expect that the US will follow. However, as no US is presented
during extinction or test the US omission may change the participant’s expectations
with regards to the CS-. For instance, if the participant has adopted a rule that “one
CS is followed by the US”, the participant may expect that the CS- will now be
followed by the US after the presentation of the CS+ alone. Consistent with this
interpretation, participants that receive the CS+ first in the test phase show a greater
increase in conditioned responding to the CS- when it is presented on the second trial
than participants that receive the CS- presentation on the first test trial (Neumann,
2006). An alternative explanation could be that it reflects a generalisation decrement
due to participants forming a configural CS-context stimulus during each phase.
Removal from the acquisition context results in a new CS-context combination that
produces an increase in responding to the CS- up to a level similar to that observed at
The Return of Extinguished Conditioned Behaviour
26
the start of acquisition. Likewise, removal from the acquisition context results in a
new CS-context combination in the ABC design to again increase responding to the
CS- up to a similar level as that observed at the start of the other phases of the
experiment.
Enhancing renewal
Due to the apparent difficulty in unequivocally demonstrating ABC renewal in
humans, it is worthwhile to consider what experimental manipulations might enhance
the renewal effect in either an ABA, ABC, or even an AAB design. Although there a
no published parametric studies in humans, it is likely that using contexts that have
sharp differences in the components of the context will produce stronger renewal than
using contexts that are more similar. In addition to the components of the context, the
overall number of shared or dissimilar contextual cues might also impact on renewal
(Thomas, Larsen, & Ayres, 2003). In a test of ABA renewal using a variation of the
conditioned suppression task, Havermans et al. (2005) found that using a change in
the background colour of the screen in which the stimuli were presented between blue
and red showed a modest, although non-significant renewal of conditioned
suppression. In a subsequent experiment, using a combination of changes in the
background colour of the screen and changes in the colour of the Martian stimuli
produced a stronger and statistically significant renewal of suppression. The results
are thus consistent with the notion that the size of renewal is dependent on the extent
to which the extinction and text context are perceptually different.
If renewal reflects the retrieval of the CS-US association, it might be expected
that experimental manipulations that encourage this retrieval will serve to enhance
renewal. Indeed, participants that are presented with a retrieval cue during the test
phase showed stronger renewal of skin conductance responses and expectancy ratings
The Return of Extinguished Conditioned Behaviour
27
if the cue was also presented during acquisition than if the cue was also presented
during extinction (Vansteenwegen, Vervliet, Hermans, Beckers, Baeyens, & Eelen,
2006). Although the design this study cannot determine whether it was necessarily the
presence of the cue during acquisition or extinction that was the major contributor to
the difference in the renewal effects, the results are consistent with the idea that
retrieval cues can modulate the renewal effect. Subsequent research might more
directly examine the presence or absence of retrieval cues during the acquisition and
test phases of a renewal procedure.
Attenuating renewal
While the majority of research with human participants has been concerned
with producing the renewal effect, the question of how to prevent renewal is an
important one for theoretical and practical reasons. Experimental procedures that
serve to attenuate renewal can be suggestive of the psychological processes that
underlie the effect. For instance, the relative ineffectiveness of instructions that
devalue the role of contextual cues to attenuate renewal during a conditioned
suppression task noted earlier (Neumann, 2007) suggests that non-cognitive processes
may play a role in renewal, at least in certain situations. Instructions might also be
employed in other ways in an attempt to reduce renewal. For example, instructions
might be used to draw attention away from the contextual cues that are present or to
increase the transfer of learning from extinction to test.
An alternative approach to reducing renewal is to increase the generalisation
of extinction to contexts outside of that experienced during extinction training. One
way in which this might be done is to present extinction trials across a number of
different contexts. This might increase the chance that similar contextual cues are
shared among the test and extinction contexts. Findings from non-human animal
The Return of Extinguished Conditioned Behaviour
28
research have shown that presenting extinction across multiple contexts can attenuate
renewal in an ABA design (Chelonis, Calton, Hart & Schactman, 1999) and an ABC
design (Gunther et al., 1998). Consistent with these findings, presenting extinction
trials across three different contexts abolished the renewal of conditioned suppression
in an ABA design (Neumann, 2006). The use of three extinction contexts also
attenuated the increase in conditioned suppression to the CS+ and CS- during test in
an ABC design (Neumann, 2006). Taken together, the results are consistent with the
animal studies of Chelonis et al. (1999) and Gunther et al. (1998) in suggesting that
the use of multiple extinction contexts will abolish the renewal effect.
In contrast to the above studies, two recent reports suggest that the use of
multiple extinction contexts does not necessarily attenuate renewal. Bouton, GarcíaGutiérreza, Zilskia, and Moody (2006) was unable to replicate the attenuation of
renewal in a fear conditioning procedure with rats. In line with these findings,
Neumann et al. (2007) also did not find strong evidence for an attenuation of ABA
renewal when extinction trials were given across three or five contexts in a fear
conditioning procedure with humans. The different results among the studies may
reflect that one or more variables will mediate whether or not multiple extinction
contexts attenuates renewal. The exact nature of the contextual cues that are present
may be one important factor. For instance, renewal is larger when extinction and test
differ on a larger number of distinct contextual cues (Thomas et al., 2003).
Conversely, the greater the similarity in the cues between the extinction contexts and
a subsequent test phase, the greater will be the attenuation of renewal. Although both
the studies by Neumann (2006) and Neumann et al. (2007) used a combination of a
coloured light and sound as the context, the two studies differed in exactly what
combinations were used. A future parametric study may be required that
The Return of Extinguished Conditioned Behaviour
29
systematically manipulates the number and/or type of contexts used in the different
phases of the experiment. For instance, using multiple extinction contexts of a blue
light plus and bell sound and a red light plus a drum sound would produce a smaller
renewal effect if test is conducted in a context that used a combination of these
features, such as a blue light plus drum sound, than if test was conducted in a
completely novel context, such as a yellow light plus cymbal sound (Neumann et al.,
2007).
Reinstatement
Reinstatement in humans has been demonstrated with a causal learning task
(García-Gutiérrez & Rosas, 2003; Vila & Rosas, 2001), a fear conditioning task
(Dirikx et al., 2004; Dirikx et al., 2007; Hermans et al., 2005; La Bar & Phelps, 2005;
Van Damme, Crombez, Hermans, Koster, & Eccleston, 2006), and a conditioned
suppression task (Neumann, in press). In the conditioned suppression task, six
presentations of the laser shield US on its own were made after extinction training.
The unwarned US presentations had the effect of increasing conditioned suppression
to the CS+ and no effect on the CS-. A control group that did not receive the US
presentations after extinction, but received a similar time delay prior to the test trials,
did not show any change in responding during the CS+ and CS- (Neumann, in press).
Research conducted by Hermans, Dirikx and colleagues (Dirikx, Hermans,
Vansteenwegen, Baeyens, & Eelen, 2004; Dirikx, Hermans, Vansteenwegen,
Baeyens, & Eelen, 2007; Hermans, Dirikx, Vansteenwegenin, Baeyens, Van den
Bergh, & Eelen, 2005; Van Damme, Crombez, Hermans, Koster, & Eccleston, 2006)
has investigated reinstatement in a fear conditioning procedure. Across the series of
the experiments, the presence of a reinstatement effect has been tested with a variety
of measures of conditioned behaviour. For example, one experiment employed a
The Return of Extinguished Conditioned Behaviour
30
spatial cueing paradigm (Van Damme et al., 2006). The reaction times during the
paradigm were suggested to reflect attentional biases that can accompany conditioned
fear. Consistent with a reinstatement effect, attentional biases were greater when the
cueing task involved CS+ presentations than when it involved CS- presentations
following a reinstatement procedure. The two earlier experiments, reported by Dirikx
et al. (2004) and Hermans et al. (2005), measured conditioned responses with US
expectancy ratings, subjective fear ratings, and secondary task reaction time to
auditory probes presented during the visual CSs. The most consistent evidence for
reinstatement was observed for fear ratings. Fear ratings of the CS+ increased from
extinction to the reinstatement test trial when unwarned presentations of the US were
given after extinction. In addition, rated fear during test was higher for the CS+ than
for the CS-. Ratings of US expectancy showed a similar pattern as the fear ratings
during test trials (i.e., higher expectancy of US for CS+ than CS-) in one experiment
(Hermans et al., 2005), but not in the other experiment (Dirikx et al., 2004). Likewise,
evidence of reinstatement in secondary task reaction time (i.e., slower reaction time
during CS+ than during CS- during test trials) was found in one experiment (Dirikx et
al., 2004), but not in the other experiment (Hermans et al., 2005).
The experiments reported by Dirikx and colleagues (Dirikx et al., 2004, 2007;
Hermans et al., 2005) also examined the relationship between the measures of
conditioned responding and subjective ratings of the affective meaning of the CS+
taken immediately after extinction. Valence was measured on a rating scale with the
anchors of very unpleasant and very pleasant. Results showed that more negative
valence ratings of the CS+ was associated with higher reinstatement in fear ratings
(Hermans et al., 2005), and secondary reaction time slowing (Dirikx et al., 2004,
2007) during test. No association was found between valence ratings and ratings of
The Return of Extinguished Conditioned Behaviour
31
the expectancy of the US in two studies (Dirikx et al., 2007; Hermans et al., 2005).
The associations between the measures indicate that the amount of reinstatement
found in some measures of conditioned responding is related to the evaluated valence
of the CSs immediately after extinction (Dirikx et al., 2004).
In one of the first demonstrations of reinstatement in humans, a causal
learning task was used that required participants to assume the role of a healthcare
inspector that was investigating stomach aches in people who ingested medicines
bought at importation pharmacies (Villa & Rosas, 2001). Ingestion of one medicine
brand (CS+) was followed by a stomach ache (US) and ingestion of another medicine
brand (CS-) had no consequence. In extinction, ingestion of both medicines were
presented without any consequence. At the end of extinction, participants rated the
probability that the illness followed either the CS+ or CS- as low. However, after
extinction some participants were presented with trials in which the illness occurred
when people merely visited a pharmacy. This phase thus represented a reinstatement
procedure as the US (stomach ache) was presented on its own. After this phase,
participants in both groups judged the probability that the stomach ache would follow
ingestion of the CS+ medicine as higher than participants who did not receive a
reinstatement phase of US only presentations, consistent with a reinstatement effect.
A reinstatement effect has also been found in a causal learning task that used a
different scenario in which eating different foods were followed by illness (GarcíaGutiérrez and Rosas, 2003)
Context changes and reinstatement
Animal research has suggested that reinstatement is dependent on the context
in which the unwarned US presentations are made. For example, reinstatement has
been found when exposure to the US alone is given in the same context as a
The Return of Extinguished Conditioned Behaviour
32
subsequent test phase, but not when exposure is given outside of the test context or
when the test context only is presented before test (e.g., Bouton & King, 1986).
Reinstatement also occurs when exposure to the US and the subsequent test phase is
in a different context to that used during acquisition and extinction (Westbrook et al.,
2002). These findings are consistent with the notion that reinstatement represents
another instance of context dependent learning (Bouton, 1993; 2002; 2004).
Presentations of the US after extinction will result in the organism associating it with
the context and this promotes subsequent retrieval of the US when presentations of
the CS are given in the same context. Extinction may result in the CS being under a
contextually modulated form of inhibition (Bouton, 1993) such that the presence of
the extinction context will promote the retrieval of a CS-noUS association. As
research on renewal has suggested that ABC renewal has been difficult to demonstrate
in humans, and by implication questioning the notion that it is merely the context
specific nature of extinction learning that is of importance, the question of whether
reinstatement shows context specificity in humans is of theoretical importance.
The results from a series of experiments employing a fear conditioning
procedure appear to be consistent with context specific nature of reinstatement (LaBar
& Phelps, 2005). In the first experiment, a single cue conditioning procedure was used
in which a CS was paired with a loud noise US. Participants received four reinstating
US presentations in either the same or a different experimental room to that in which
the preceding acquisition and extinction phases were given. Test was always
conducted in the same context as acquisition and extinction. Participants that received
the reinstating US presentations in the same context as the subsequent test phase
showed larger skin conductance responses to the CS during test relative to the last
extinction trial. In contrast, participants that received the reinstating US presentations
The Return of Extinguished Conditioned Behaviour
33
in a different context did not show a return of conditioned responses. These results
were replicated in a subsequent study that used a differential conditioning procedure
and an electric shock as the US. Moreover, a final experiment failed to find any
reinstatement in two amnesic patients despite these patients showing a reliable
acquisition of fear. Taken together, these results support the notion that reinstatement
is context dependent and may reflect context conditioning during the US exposure
phases.
A similar conclusion was reached in earlier studies that used a causal learning
task to investigate reinstatement (García-Gutiérrez & Rosas, 2003). In these studies, a
causal learning task that was based on the scenario that people received illnesses after
eating certain foods at a particular location. Thus, the CSs were ingestion of foods
(e.g., garlic), the USs were gastric illnesses (e.g., diarrhea, constipation), and the
contexts were names of restaurants (e.g., “The Swiss Cow”) or eating locations
(“going on a picnic”). After an acquisition phase, a retroactive interference phase was
introduced in which one food that was followed by one outcome (e.g., diarrhea) in
acquisition, was followed by a different outcome in the retroactive interference phase.
In the reinstatement phase, the contexts (eating locations) were presented with the
outcomes. Using these methods, reinstatement was also observed and it was shown to
be influenced by contextual changes. For instance, no reinstatement was observed
when presentations of the outcome only were made in a different context to that in
which the test trials were presented in.
However, not all results have been consistent with the view that reinstatement
is specific to the context in which US exposure takes place. A casual learning task in
which participants were required to rate the probability that illnesses followed the
ingestion of certain medicines showed that reinstatement was larger when the US
The Return of Extinguished Conditioned Behaviour
34
outcome (illness) was presented in either the same context (the name of the pharmacy
at which the medications were purchased) as the subsequent test phase than when the
outcome was presented in a different context (Vila & Rosas, 2001). However, a
significant reinstatement effect was still present in those participants that received
different contexts for the US outcome and test phases. In the only study to investigate
reinstatement with the conditioned suppression task, a reliable reinstatement effect
was found when the US outcome (presentation of the laser shield) was given after
extinction (Neumann, in press). Moreover, the reinstatement of conditioned
suppression persisted even when the US presentations were made in a different
context to the subsequent test phase. An additional experiment indicated that this
persistence of a reinstatement effect did not depend on the differential exposure to the
test context across the different groups.
The contradictory findings that have emerged in some studies on the context
dependency of reinstatement places doubt on the notion that extinction learning is
context dependent in humans. One possible explanation for the discrepancies may be
that the contextual changes that were used in some studies were not salient or distinct
enough to produce a strong context dependency effect. Vila and Rosas (2001) raised
this possibility in their causal learning experiment by suggesting that the contexts they
used may have been considered to be similar by the participants and that this
promoted generalization of judgments between contexts. The designation of the
pharmacy names as either “Yellow Pharmacy” or “Red Pharmacy” appears to be
consistent with this explanation. Distinctive names were employed in the studies by
García-Gutiérrez and Rosas (2003) that did find context dependent reinstatement
effects. A similar explanation, however, does not seem to apply to the results of the
conditioned suppression task by Neumann (in press). The context manipulations used
The Return of Extinguished Conditioned Behaviour
35
in this study were illuminating the experimental room with different coloured lights
and playing different background sounds. These context manipulations have been
shown to produce reliable renewal effects in prior research (Neumann, 2006;
Neumann et al., 2007). Instead, the conditioned suppression task may contain unique
features that tend to promote the transfer of learning across different contexts. For
instance, the procession of experimental phases without any interruption from the
experimenter, the short presentations of the CS, and the continuous nature of the task
in which the stimuli appear at a steady rate across the entire experimental session, are
all present in the conditioned suppression task and may make the contextual
presentations during the US exposure and test phases less salient.
An alternative explanation for the discrepant findings could be that there are
additional processes that mediate reinstatement in humans. The different processes
may either complement each other or may be either present or absent in a given
situation. Garcia-Gutierrez and Rosas (2003) tested the parsimonious explanation that
reinstatement results from confusion on the part of the participants that is caused by
the presentation of the US after extinction. However, the investigators ruled out this
possibility by showing that reinstatement and renewal had an additive effect after
extinction. Such an additive effect would not be expected if either or both the
reinstatement and renewal procedures produced confusion in the participants.
Other associative learning explanations for reinstatement have been suggested.
For instance, Rescorla and Heth (1975) initially proposed that reinstatement reflected
the US representation weakens during extinction and that this weakening is
counteracted by the presentation of the US before test. Such a process does not
depend on the context in which the US is presented and may promote reinstatement
across contexts and account for the results of Vila and Rosas (2001) and Neumann (in
The Return of Extinguished Conditioned Behaviour
36
press). This explanation may be particularly applicable to the conditioned suppression
task used by Neumann (in press). Research on the renewal effect with this task has
yielded results suggesting that participants may develop a configural context-CS
stimulus and that this is associated with the US during acquisition (Havermans et al.,
2005). The reinstating presentations of the US may have had the effect of promoting
retrieval of the CS-US association during the test phase, particularly because the test
phase was conducted in the same context as that used during acquisition (Neumann, in
press).
Spontaneous Recovery
Spontaneous recovery has long been known as a mechanism for the return of
extinguished conditioned responses (e.g., Pavlov, 1927) and has been observed in a
wide variety of animal conditioning studies (see Rescorla, 2004 for a review).
However, its examination in laboratory-based research using human participants has
been surprisingly limited. This may reflect that there was one very early and
apparently clear demonstration of spontaneous recovery of the galvanic skin response
in a human fear conditioning procedure (Ellson, 1939; see also Hovland, 1937). In
this study, spontaneous recovery was tested after intervals of 5 min, 20 min, 60 min,
and 180 min. A trend emerged across time with greater spontaneous recovery of the
galvanic skin response with longer delay intervals. The trend was curvilinear,
reflecting that the increase in spontaneous recovery from one time interval to the next
became progressively smaller as the time interval was increased. The curvilinear
pattern replicated that found in comparable non-human animal research (e.g., Ellson,
1938) to suggest similar interval effects across species. Although there has been little
further research on spontaneous recovery in a human fear conditioning procedure
since this initial study (but see Beeman & Grant, 1961; and Franks, 1963 for studies
The Return of Extinguished Conditioned Behaviour
37
that used human eyelid conditioning), there is at least one report showing that
spontaneous recovery of extinguished fear can be observed using modern laboratory
materials and procedures (Guastella, Lovibond, Dadds, Mitchell & Richardson, 2007).
Spontaneous recovery has also been observed in research that has used the causal
learning task (Vila & Rosas, 2001; Vila, Romero, & Rosas, 2002). The research
which has demonstrated spontaneous recovery suggests that this phenomenon is a
reliable effect in human participants. Further research should be encouraged in order
to better understand the mechanisms that underlie it and those variables that influence
its magnitude in humans.
Summary and conclusion of human laboratory studies
It has been evident from the explosion of research on renewal and
reinstatement in recent times that considerable progress is being made in
understanding these phenomena in humans. Additional research efforts to examine
spontaneous recovery and even reacquisition will help to maintain some degree of
balance between the four phenomena that can produce a return of conditioned
behaviour in the laboratory. The several demonstrations of renewal and reinstatement
that have been reported show that they are reliable effects and can be observed with a
variety of CSs, contexts, and learning paradigms. Now that the basic methodologies in
producing the effects have been established, the time appears right to further our
knowledge in a systematic manner. Some fundamental parametric studies appear to be
needed in order to understand what exteroceptive and interoceptive contextual cues
can produce powerful renewal effects. The extent to which many prior findings from
non-human animal research apply to humans remains to be determined. There is also
a need to elaborate on the theoretical basis of the return of extinguished conditioned
behaviour in humans. The well developed theoretical models that have been based on
The Return of Extinguished Conditioned Behaviour
38
non-human animal research can be applied and tested in human studies. Moreover,
research can investigate the role of those “human” aspects of learning, such as
cognitive processes in the recovery from extinction. Finally, the means by which
renewal, reinstatement, and spontaneous recovery can be prevented needs further
investigation. While it may be unreasonable to expect that a total abolishment of these
effects can be achieved, their attenuation would provide significant practical
applications to the return of extinguished conditioned behaviour in clinical
psychology.
APPLICATIONS OF THE RETURN OF EXTINGUISHED CONDITIONED
BEHAVIOUR IN CLINICAL PSYCHOLOGY
One key reason for ongoing interest in the return of extinguished conditioned
behaviour is its implications within clinical psychology. Behavioural models of
psychopathology have previously used conditioning research to help explain the
etiology and maintenance of symptoms in conditions such as specific phobia (Davey,
2002; Rachman, 1991), post-traumatic stress disorder (Pitman, Shalev & Orr, 2000),
and depression (Lewinsohn, 1974), among others. Behavioural and cognitivebehavioural treatments of many clinical conditions involve exposure tasks, which
have been proposed to exert their clinical effect (at least in part) through extinction
processes (e.g., Tryon, 2005; Waters, McDonald, & Koresco, 1972; Emmelkamp,
1994). Despite successful treatment, relapse is a frequent observation in clinical
practice (e.g., Yonkers, Bruce, Dyck, & Keller, 2003). One potential explanation that
has been offered for such relapse is the return of extinguished conditioned responses
through mechanisms such as renewal, reinstatement, and spontaneous recovery.
Research conducted on anxiety disorders has tended to support this interpretation.
The Return of Extinguished Conditioned Behaviour
39
Moreover, other research that has examined substance dependence highlights the
generality of the return of conditioned responses in the clinic.
Anxiety Disorders
Anxiety disorders are prevalent psychological conditions which can result in
significant impairment of functioning (e.g., Kroenke, Spitzer, Williams, Monahan &
Rowe, 2007) and quality of life (Lochner, Mogotski, du Toit, Kaminer, Niehaus &
Stein, 2003; Olatunji, Cisler & Tolin, 2007; Rapaport, Clary, Fayyad, & Endicott,
2005). Previous research has supported behavioural and cognitive behavioural
therapies as the treatments of choice (Barlow, Raffa & Cohen, 2002; Franklin & Foa,
2002) and as the most cost-effective interventions (e.g., RANZCP Clinical Practice
Guidelines Team for Panic Disorder and Agoraphobia, 2003) for these conditions.
Exposure treatments have been conceptualised as the repeated presentations of a CS
in the absence of the US and underlies the incorporation of behavioural concepts into
the understanding of these interventions as important.
Despite effective treatments, evidence has consistently emerged since the late
1960s that there are a proportion of individuals who experience a recurrence in
anxiety symptoms following treatment (e.g., Rachman, 1966). Such recurrence in fear
responses after successful treatment is a phenomenon often referred to as the return of
fear (ROF; Rachman, 1979; 1989). The ROF is reported in as many as 33-50% of
successfully treated individuals (Craske & Rachman 1987; Rachman, 1966; Rose &
McGlynn, 1997). The typical clinical observation of ROF is the successful reduction
in fear through exposure-based treatment, followed by a period in which the
individual does not come into contact with their formerly feared object or situation.
After such a hiatus, re-exposure to the feared stimulus results in the individual
showing subjective experience and objective measures that indicate that the fear has
The Return of Extinguished Conditioned Behaviour
40
grown from its immediate post-treatment levels. Such ROF does not usually lead to a
fear response at the same strength as pre-treatment, but nevertheless can present a
significant clinical problem for patient and therapist (Rachman, 1989). It is also
possible that small lapses may recur with increasing strength to result in a full-blown
relapse. The phenomena of renewal, reinstatement, and spontaneous recovery provide
a organisational framework with which to understand the ROF and in turn, may
suggest means by which to attenuate the ROF following treatment.
Renewal as Return of Fear
In renewal of fear responses, differences in the context for which the original
acquisition, extinction, and follow-up testing occur are thought to influence the degree
of ROF observed. Support for this notion has been obtained in research that used
spider-fearful individuals. Mineka, Mystkowski, Hladek, and Rodriguez (1999)
required spider-fearful participant to undergo a two-hour exposure/modelling session
in which their fear was reduced. Treatment-responders were followed up after one
week, with a reassessment that included a self-report questionnaire of spider phobia
symptoms and subjective fear ratings during a behavioural approach test. Half the
participants conducted their reassessment in the same location as their treatment
procedure, while the other half was placed in a novel location. For the group retested
in a different context, the authors reported a moderate renewal of fear relative to that
observed in the control group. Similar results were reported by Rodriguez, Craske,
Mineka, & Hladek (1999) also using spider-fearful individuals retested after a twoweek period. In this study, the presence/absence of a particular therapist and salient
visual cues within the test rooms were manipulated in addition to the setting itself.
Although self-reported fear did not show renewal in a different context, other
measures such as heart-rate and behavioural avoidance provided support for the
The Return of Extinguished Conditioned Behaviour
41
concept of ROF through renewal.
Contextual variables which influence ROF via renewal may also be occur
through manipulations of the interoceptive contexts. In a counterbalanced design,
Mystkowski et al. (2003) administered either caffeine or a placebo solution to
individuals undergoing an extinction process for spider fear responses. At follow-up,
half the participants received the same solution, while the other half received the
placebo. For those participants who conducted their reassessment in a different state
as the extinction procedure, there was significant renewal of fear at the closest
approach to the spider stimulus. The implications of these results are relevant for
therapeutic approaches that combine medications with exposure treatment. The ROF
via renewal may remain as a potential danger if the individual discontinues their
medications after exposure treatment has concluded. At the very least, the exposure
treatment should be continued well beyond the cessation of all medications.
It is noteworthy that one recent study has failed to find the renewal effect after
a three month period in participants whose spider phobia had been extinguished
(Vansteenwegen, Vervliet, Hermans, Thewissen, and Eelen, 2007). At the three
month follow-up, those tested in a different room and building to the one in which
their exposure treatment was conducted showed no greater return of fear than those
assessed in the same location, despite assessment including self-report, behavioural
and physiological measures. Interestingly, at one-year follow-up, those tested in a
different location showed significantly less ROF on their self-report measure of spider
anxiety. The authors suggested that this reduction in the ROF as reflecting that the
participants were exposed to multiple contexts prior to the one-year follow-up testing
session. This exposure may have increased the generalisation of extinction learning to
the follow-up testing session. Although requiring further direct experimental support,
The Return of Extinguished Conditioned Behaviour
42
this interpretation suggests that there are means by which the ROF via a renewal
effect may be attenuated.
A direct attempt to attenuate the renewal of fear was reported by Mystkowski,
Craske, Echiverri, and Labus (2006). Spider-fearful participants underwent exposure
treatment to extinguish their fear responses. The treatment session was given in a
distinctive room. During a subsequent renewal test phase, half of those re-tested were
asked to mentally reinstate the conditions of the treatment room, while the other half
were asked to think of events from an unrelated time. Those participants who used the
mental reinstatement of the treatment context showed significantly less renewal of
fear than those participants who did not. The results are encouraging in suggesting
that there may be cognitive strategies that could be used by individuals post-treatment
in order to reduce the ROF through a renewal effect.
Reinstatement as Return of Fear
There has been comparatively little research on the reinstatement of anxiety
and fear in a clinical context. Perhaps one reason for this is that it is difficult to test
for reinstatement effects in an ethical and experimentally controlled manner. By
definition, reinstatement results from the re-experiencing of the UR of fear following
successful exposure treatment. As such, it can be difficult to experimentally induce
such a fear reaction in patients. An early study using snake and spider phobic
individuals explored one means by which a fear response may be induced (Rachman
& Whittal, 1989a). Fear responses were assessed using heart rate and subjective report
of fear. After successful extinction of their fear response, participants were asked to
return two weeks later for a reassessment. When participants returned for their retest
session, half were presented with an electric shock to their forearm during their
behavioural approach test, while the other half did not receive such a shock, acting as
The Return of Extinguished Conditioned Behaviour
43
a control group. In this study, despite the increase in anxiety and nervousness reported
by the participants in the shock group, there was no significant difference in
subjective fear rating or heart rate between the experimental and control conditions.
The authors attributed the absence of a significant reinstatement of fear to the
weakness of their aversive shock event. Evidence supporting this conclusion was the
fact that the shock did not significantly elevate heart rate in the experimental group.
As such, the shock may have been insufficiently aversive to elicit a reinstatement
effect. Notwithstanding these methodological concerns, results from human
laboratory investigations (e.g., Dirikx et al., 2004, 2007; Hermans et al., 2005;
Neumann, in press) suggest that reinstatement in humans can be observed. Further
tests for reinstatement in a clinical context might use more intense or alternative
means by which to induce fear, such as a higher intensity shock stimulus or a threat of
shock condition. Alternatively, reinstatement of fear might be tested in a naturalistic
design that correlates the experience of fear or major periods of illness or anxiety in
patients following exposure therapy.
Spontaneous Recovery as Return of Fear
ROF can occur in successfully treated individuals, despite no clear evidence
that they have been re-exposed to pairings of the feared stimulus and an aversive
event. In such cases, the spontaneous recovery may provide a viable explanation for
the return of fear. Spontaneous recovery of fear was documented by Rachman in a
seminal paper in 1979 and it has been observed in clinical and research settings in
numerous studies since. Spontaneous recovery of fear responses has been documented
to occur after both short-term and long-term time delays. Philips (1985) treated a
small group of patients with emetophobia (fear of vomiting) and found that just under
half of patients showed significant spontaneous recovery of their anxiety responses,
The Return of Extinguished Conditioned Behaviour
44
necessitating an extended number of exposure sessions for therapy to be successful.
Comparable findings have been reported in claustrophobia (Wood & McGlynn,
2000), and phobias of spiders (e.g., de Jong, van den Hout, & Merckelbach, 1995) and
snakes (e.g., Rose & McGlynn, 1997).
Factors Influencing Return of Fear
Factors that influence the development of ROF have been divided into (a)
training factors and variables during the exposure process, (b) post-training factors
that occur after the successful extinguishing of the fear response, and (c) state-related
factors of the individual (Rachman, 1989). In terms of training factors, variables such
as the level of difficulty (“demand”; Grey, Sartory, & Rachman, 1979), number of
exposures (Craske & Rachman, 1987), use of distraction (Rose & McGlynn, 1997),
and speed of fear reduction (Rachman & Whittal, 1989a; 1989b) have all been
assessed for their relationship to ROF, often with inconsistent results across studies.
The post-training factors that may influence return of fear can include reinstatement
and related phenomena. As noted earlier, research into reinstatement of fear in
humans has been scarce. Finally, numerous state-related factors have been
investigated in studies examining ROF. Several of these factors have been
demonstrated to influence ROF, although the most consistent finding is arguably the
lack of consistency across different research studies. Factors such as initial fear levels,
cognitive content and process, and mood state during exposure have all being
investigated.
One example of inconsistent findings regarding state-related factors in
predicting ROF is that of original levels of fear when exposed to the feared stimulus.
Using clinical patients, several studies have demonstrated that ROF is correlated with
initial fear levels in individuals with panic disorder (Rachman & Levitt, 1985), and
The Return of Extinguished Conditioned Behaviour
45
performance anxiety (Craske & Rachman, 1987). In a sample of patients with
claustrophobia, subjective fear ratings did not predict ROF, while heart rate during
initial exposure did (Wood & McGlynn, 2000). In contrast, Rose and McGlynn
(1997) reported that initial fear level was not predictive of ROF in a small sample of
snake-phobic patients.
One finding which has emerged with some consistency is the ability of
cognitive variables to predict ROF. There is some support from a small number of
studies that both cognitive content and cognitive processes are associated with ROF.
High levels of anxiety-related cognitions have been associated with ROF in anxious
musical performers (Craske & Rachman, 1987). Covariation biases, the tendency to
associate aversive outcomes with phobic stimuli, have also been associated with ROF
in spider phobics (de Jong, van den Hout, & Merckelbach, 1995). Individuals who
experience a sudden and subjectively important reduction in fear responses have also
demonstrated reduced levels of ROF (Rachman & Whittal, 1989b).
The mood state of individuals during exposure tasks may have important
effects on ROF. At least three studies have demonstrated that ROF is greater in
subjects who undergo exposure treatment in a dysphoric mood state, than for those
subjects in a positive mood state. This increased ROF has been observed when
participants are tested 30 minutes (Salkovskis & Mills, 1994), 1 week (Philips, 1985),
or 1 month (Samsom & Rachman, 1989) after exposure. This difference is observed
even when all participants are retested when in a neutral mood state at the follow-up
(Salkovskis & Mills, 1994). It has been suggested that this effect may result from both
a more elaborate encoding of negative material and a less elaborate encoding of
positive material when the participant undergoes exposure in a dysphoric state.
Treatment Approaches Aimed at Reducing Return of Fear
The Return of Extinguished Conditioned Behaviour
46
Research has aimed to elucidate the treatment approaches which may assist in
reducing the possibility of relapse from ROF. Clinicians conducting behavioural or
cognitive behavioural interventions for the anxiety disorders should be mindful of this
literature when planning their treatment approach, and informing their patients of this
relapse risk. Factors which have been shown to reduce the probability of ROF after
successful extinguishing of fear responses include extended duration exposure
sessions, increased numbers of exposure sessions, increased hiatus between exposure
sessions, reducing use of distraction, use of multiple exposure stimuli, use of diverse
contexts, and rehearsal out-of-session.
Exposure treatments for anxiety typically last until such a time as habituation
has occurred (i.e., that anxiety has reduced despite continued exposure to the feared
stimulus). Although evidence in clinical studies is scarce, Craske, Lopatka &
Rachman (as cited in Rachman, 1989) reported that extending the duration of
exposure sessions may assist in reducing ROF. In this study, individuals were exposed
to their feared stimulus for a further ten minutes beyond the point at which anxiety
had abated. Although detailed results are not available, Rachman (1989) reported that
such a procedure produced some suppression of ROF.
In addition to extending the duration of exposure sessions, some authors have
suggested that increasing the overall number of exposure sessions may assist in
preventing ROF. As early as 1965, Agras reported that repeated exposure was
effective in reducing spontaneous recovery of fear in a group of six individuals with
specific phobias. In a similarly small group of individuals with emetophobia, Philips
(1985) used an extended number of sessions to treat participants who showed
significant between-session ROF. In this study, a larger number (13 compared to 8) of
exposure sessions resulted in the elimination of ROF in the short-term, as well as at
The Return of Extinguished Conditioned Behaviour
47
six-month follow-up. Although human clinical studies are few in number, there is also
evidence from animal fear studies that repeated ‘massive’ extinction procedures can
reduce the renewal of extinguished fear responses that are otherwise difficult to
reduce by ‘standard’ extended extinction treatments (Dennitson, Chang & Miller,
2003).
Procedures for exposure therapy have varied the period between successive
exposures. Although there is some indication that massed or even single session
exposure can be effective (e.g., Ost, 1989), there is also evidence that increasing
durations between successful exposure may attenuate ROF. Rowe and Craske (1998a)
compared massed exposure procedures to an exposure schedule with increasing
durations between exposure sessions in a sample of spider phobic individuals. A
group receiving massed exposure sessions showed more complete habituation during
treatment than the expanding-spaced exposure groups. Despite this, those participants
on the expanding-spaced exposure schedule showed significantly less ROF when
presented with either the same spider used for exposure treatment, or a different,
novel spider. Interestingly, these results were not replicated when Lang and Craske
(2000) used expanding-spaced exposure sessions in treatment of height phobia. In this
study, there were no significant differences in ROF, although the authors questioned
whether their one-month follow-up period was a sufficiently long enough time for
differences in ROF to be observed.
Behavioural theory on which some explanations of exposure therapy are based
suggests that the use of distraction during the exposure process may serve to prevent
full engagement with, and habituation to, the feared stimuli. Few studies have
examined the impact of distraction during exposure on ROF. Rose and McGlynn
(1997) reported on an experimental study in which snake-fearful participants were
The Return of Extinguished Conditioned Behaviour
48
asked to either focus on the snake-stimuli, or monitor an irrelevant audiotape for
certain key phrases. Although both experiments in this paper showed that ROF was
observed more frequently in the group who utilised distraction, these results did not
reach statistical significance. Although the authors interpreted their findings as being
suggestive that distraction may increase the likelihood of ROF being observed,
replication with a larger sample is required to more fully answer questions around the
role of distraction in ROF.
Renewal effects following successfully extinguished fear responses may be
reduced through conducting exposure therapy with multiple different stimuli and in
multiple different contexts. Two studies examining the use of varied stimuli have
returned different findings. Using 28 spider-phobic undergraduates Rowe and Craske
(1998b) investigated the impact of using varied stimuli on ROF. Half of their
participants were exposed to a single tarantula over four exposure trials, while the
other half was exposed to a different tarantula in each of the four trials. When the
groups were reassessed after a three-week period, the group which had only seen the
single spider showed greater ROF than those who had undergone exposure to a series
of different spiders. Lang and Craske (2000) attempted to replicate the earlier work of
Rowe and Craske (1998a) using participants who had a fear of heights. Similarly to
the earlier study, half of the participants were exposed to the same situation across
exposure trials, while the other half was exposed to a series of different situations.
Unlike Rowe and Craske (1998a), however, there was no significant difference in
ROF between the two groups as measured by subjective, behavioural or physiological
measures. The effect of varied exposure stimuli on eventual ROF remains unclear,
and further work using longer-term follow-up is also needed.
The early findings that ROF is observed more often when exposure tasks are
The Return of Extinguished Conditioned Behaviour
49
demanding suggests an avenue to reduce the likelihood of ROF. As discussed earlier,
exposure therapy sessions which result in dramatic increases in subjective anxiety
have been associated with increased likelihood of ROF. This suggests that the level of
difficulty for exposure treatment sessions needs to be carefully planned. It would
appear that a balance needs to be struck between exposure to significant stimuli to
allow meaningful extinguishing of fear responses, and not placing unnecessarily high
demand on the individual and increasing the probability of significant ROF.
Individuals who engage in behavioural or cognitive-behavioural treatment for anxiety
disorders are usually requested to undertake between-session ‘homework’ tasks to
assist in therapy. One such task, imaginal exposure, may assist in reducing ROF.
Sartory, Rachman and Grey (1982) assessed the impact of a brief 30 minute imaginal
exposure session immediately following a successful in-vivo exposure session in a
group of 28 individuals with animal phobias. Half of the participants spent 30 minutes
after exposure conducting imaginal exposure, while the other half were asked to
distract themselves by reading unrelated magazine articles. Contrary to the authors’
expectations, when participants were reassessed one week later, the group who used
distraction immediately following exposure showed increased ROF as measured by
subjective fear ratings. These findings give tentative support to the importance of
rehearsal and imaginal exposure after successful treatment to reduce ROF.
Recent research has investigated the ability of the NMDA agonist, dcycloserine (DCS) as an adjunct to the treatment of phobic anxiety. While DCS has
been demonstrated to be effective in enhancing exposure therapy in a virtual-reality
environment and social anxiety (Hofmann et al., 2006; Ressler et al., 2004), there is
less evidence of its ability to prevent ROF. In a large group of undergraduates, DCS
did not, however, lead to significant differences in ROF when participants were tested
The Return of Extinguished Conditioned Behaviour
50
with a more methodologically sophisticated differential conditioning paradigm
(Guastella, Lovibond, Dadds, Mitchell & Richardson, 2007). The role of DCS in
exposure and ROF attenuation remains unclear, and requires further research to
replicate the recent findings of Guastella et al. (2007) using clinical participants.
Substance Use Disorders
Despite that the majority of clinical research into the return of extinguished
conditioned responses in humans has been conducted in relation to anxiety disorders,
there exists a smaller body of research into other conditions such as substance use
disorders. One such example is the renewal of craving responses in alcohol use
following successful extinguishing of craving. Drawing on the Pavlovian conditioning
literature and the success of exposure treatments for anxiety, behavioural treatments
for substance use problems have incorporated cue exposure components in which the
individual is gradually exposed to increasingly more salient cues previously
associated with their substance use. Similar to the phenomenon of ROF, however,
such treatments may often be associated with a renewal effect, in which the same cues
in a different context produce the same craving response, and hence, relapse occurs.
Pavlovian conditioning models of substance use suggest that exteroceptive and
interoceptive cues (i.e., CSs) of drug use (e.g., drug paraphernalia, negative affect)
become paired or associated with the unconditioned, pharmacological effects of the
drug (e.g., tachycardia, euphoria). Over time, the previously neutral CSs develop the
capacity to elicit physiological conditioned responses (CRs) in the absence of drug
ingestion. A number of studies have shown these conditioning effects in alcoholics,
opiate addicts, and smokers (e.g., Brandon, Piasecki, Quinn, & Baker, 1995;
Childress, McLellan, Natale, & O’Brien, 1987). Consequently, extinction-based
treatment studies of substance use that have been based on Pavlovian conditioning
The Return of Extinguished Conditioned Behaviour
51
models have shown post-treatment decreases in substance cravings and consumption
(e.g., Drummond & Glautier, 1994; Stasiewicz et al., 1997). However, long-term
outcomes have been relatively poor and the effectiveness of cue exposure
interventions that are based on Pavlovian conditioning models relative to cognitivebehavioural relapse prevention has been questioned (e.g., Niaura et al., 1999). Some
have argued that this may be due to a lack of attention paid to context effects in cue
exposure treatments (e.g., Brandon et al., 1995; Childress et al., 1986; Rodriguez,
Craske, Mineka, & Hladek, 1999).
Collins and Brandon (2002) recently addressed this problem experimentally in
a sample of 78 nonalcoholic social drinkers. Because extinction effects (upon which
cue exposure treatments are based) are unstable and do not generalise well to other
contexts (Bouton, 2002), extinguished conditioned behaviour (i.e., the urge to drink)
may “renew” with a change of context (i.e., a renewal effect). Moreover, based on
animal research evidence that the renewal effect can be attenuated if a memory
retrieval cue that was present during extinction is also presented during the renewal
test trials (e.g., Brooks & Bouton, 1994), Collins and Brandon conducted a treatmentanalogue study to test the role of context in renewal and the effects of a potential
strategy to attenuate renewal.
After completing a cue exposure phase in an experimental room in which all
participants were exposed repeatedly to alcohol (i.e., a beer can and a beer-filled cup)
(context A), an extinction phase was completed in another room (context B) in which
participants were repeatedly exposed to the same alcohol cues until their self-reported
urge to drink returned to baseline levels. An extinction retrieval cue was present
throughout the extinction phase (i.e., a novel coloured pencil participants used to
record their urge ratings). This phase was followed some 25 min later by a renewal
The Return of Extinguished Conditioned Behaviour
52
test phase in which participants were randomly assigned to either the same context as
extinction (i.e., the same room the extinction phase was completed in), a different
context to extinction (i.e., a different experimental room), or to a different context as
extinction but with the memory retrieval cue present. Self-reported urge to drink on
visual analogue scales and saliva volume via the insertion of dental rolls into the
mouth during each trial were sampled throughout each phase. As expected, the
different context to extinction produced greater renewal effects, as indexed by both
self-reported urge to drink and saliva volume than the same context as extinction.
Moreover, renewal was attenuated when the memory retrieval cue was present. These
findings were interpreted as highlighting the important role of context effects that may
contribute to relapse following alcohol-cue exposure therapy, and the importance of
strategies such as extinction context memory retrieval cues for attenuating renewal. In
clinical terms, these findings translate to the likelihood that individuals with alcohol
use problems will relapse following successful cue exposure therapy when they are
subsequently exposed to drinking cues (whether internal or external) in situations
other than those included during treatment. These findings also suggest that if these
individuals can be instructed in the use of strategies (whether behavioural or
cognitive) that remind them of their extinguished behaviour during treatment, the
chance that they will relapse may be reduced.
However, a subsequent study by Stasiewicz, Brandon and Bradizza (2007) did
not replicate these findings in a large sample of 143 alcohol-dependent outpatients.
These authors used a similar procedure as Collins and Brandon (2002) in which
participants completed extinction trials to reduce the craving and salivation responses
to alcohol cues after repeated exposure to their preferred alcoholic beverage during
the cue exposure phase. Each phase was completed in a different experimental room
The Return of Extinguished Conditioned Behaviour
53
within the same building. Moreover, there was an extinction context memory retrieval
cue present throughout extinction for all participants (i.e., a novel coloured pencil).
Participants were then randomised to renewal tests in either (a) the same context as
extinction (i.e., the same experimental room), (b) a different context to extinction (i.e.,
a different experimental room), (c) a different context to extinction plus the extinction
retrieval cue (i.e., a different context plus the novel coloured pencil), or (d) a different
context to extinction plus a manipulation to increase the salience of the retrieval cue
(i.e., a different experimental room plus specific instruction to associate the novel
coloured pencil with the context). Contrary to expectations and the previous results,
the different context did not produce the expected renewal effect. Instead, selfreported craving continued to decrease between extinction and renewal retest,
regardless of the renewal test condition.
The authors offered numerous explanations for the results that highlight both
the subtleties of potential contextual cues that may operate during extinction and
renewal retest as well as the participant characteristics. They suggested that even
though cue exposure and extinction took place in different experimental rooms, these
rooms may not have been sufficiently discriminable because both were located in the
same building. Thus, the building itself may have represented the context of
extinction for all participants (Bouton, 2002). Similarly, the presence of the
experimenter in the room during extinction and the renewal test may have
inadvertently served as a salient extinction context cue that attenuated renewal. The
mean of 1.1 days elapsed time between extinction and the renewal test also was
suggested to be too short in this alcohol dependent population and/or demand effects
and social desirability may have influenced reporting of low craving in this group.
Another suggestion was that because the extinction criteria was reached by only 69%
The Return of Extinguished Conditioned Behaviour
54
of the sample, there may not have been sufficient extinction achieved prior to the
renewal test. The authors also suggested that the utilisation of an ABC design may
have prevented renewal effects from being observed based research which indicates
that ABA renewal tends to be stronger than ABC renewal (Bouton, 2002). Finally,
since the major difference between Stasiewicz et al.’s (2007) study and that of Collins
and Brandon (2002) was the use of a clinical versus non-selected sample, the authors
concluded that sample differences may be the most likely explanation for the different
renewal effects between studies.
A recent study on the renewal of cue-elicited urge to smoke cigarettes has also
been investigated using Pavlovian conditioning models. Thewissen, Snijders,
Havermans, van den Hout, & Jansen (2007) exposed 37 participants who smoked five
or more cigarettes per day for at least 2 years to a cue predicting smoking availability
(CS+; either a blue or yellow ashtray) and a cue predicting smoking unavailability
(CS-; the other coloured ashtray) in the acquisition context (context A; either an office
or a therapy room located in different buildings). Following extinction in the other of
these two rooms (context B) in which participants were not allowed to smoke, a
renewal test took place in the original acquisition context A (i.e., ABA renewal). The
dependent variable was urges to smoke as measured using a visual analogue scale.
Results indicated that renewal of differentially conditioned urge responding occurred
when participants were tested in the acquisition context, whereas differential urge
responding remained extinguished when tested in the extinction context. The authors
concluded that the extinguished cue-elicited urge to smoke was context-dependent.
Moreover, that the cue-elicited urge to smoke was renewed when individuals find
themselves outside the context where extinction treatment took place.
A strength of Thewissen et al.’s (2007) study compared with the renewal
The Return of Extinguished Conditioned Behaviour
55
studies involving alcohol dependence (e.g., Brandon & Collins, 2002; Stasiewicz et
al., 2007) is the experimental control that was established over the acquisition of cue
reactivity by the use of a differential conditioning paradigm involving both CS+ and
CS- trials. Renewal might also have been more reliably demonstrated in Thewissen et
al.’s study than in Stasiewicz et al.’s study by use of an ABA design, because the
experimental contexts may have been more clearly discriminable due to the
experimental rooms being located in different buildings, and because the
experimenter was absent from all experimental contexts, hence avoiding a potential
extinction retrieval cue confound. On the other hand, the acquisition and extinction
conditions in Thewissen et al.’s study were highly discriminable because participants
engaged in the smoking behaviour in the CS+ condition during acquisition and did not
engage in this behaviour during extinction. This contrasts with Stasiewicz et al’s
study in which participants were instructed only to look at and smell the alcoholic
beverage during both cue-exposure and extinction. The sharper distinction between
explicit conditioned responding during acquisition (i.e., smoking) and complete
abstinence from the behaviour during extinction may have contributed to the stronger
rates of extinction that were reported in Thewissen et al.’s study compared Stasiewicz
et al.’s study. This in turn, may have allowed for the emergence of stronger renewal
effects. Nevertheless, as participants in Thewissen et al’s study were mainly smokers
with a low level of smoking dependence and who had no intention of quitting, similar
to the unselected social drinkers studied in Collins and Brandon’s (2002) study, the
difference in renewal results between these two studies and Stasiewicz et al.’s study
may reflect on the severity of alcohol dependence in their outpatient sample.
Summary and conclusion on clinical research
The return of extinguished conditioned behaviour has been most extensively
The Return of Extinguished Conditioned Behaviour
56
investigated in the context of anxiety disorders and substance dependence disorders.
This is not surprising given that exposure therapy has had wide application in the
treatment of these conditions. The return of extinguished conditioned behaviour in
clinical investigations has been found for the renewal of fear responses, urge to drink,
and urge to smoke, and for the spontaneous recovery of fear responses. Although
there are discrepancies among the results reported so far, these may reflect the
influence of a range of variables that remain to be specified. Such variables can be
particularly difficult to control in treatment-based clinical studies. Nevertheless, the
demonstration that fears or dependencies can return following apparently successful
exposure therapy underpins the need for therapists to consider relapse via renewal,
spontaneous recovery, or related effects as a significant challenge. Future research
that aims to investigate the means by which relapse can be attenuated will have
significant benefits for the long-term treatment of individuals who engage in exposure
therapy.
CONCLUSION
The increasing number of researchers that are investigating the return of
extinguished conditioned behaviour in humans bodes well for our future
understanding of the theoretical basis and practical applications of this phenomenon.
The current research questions are now moving beyond asking whether renewal,
reinstatement, and spontaneous recovery can occur in human conditioning procedures
to more pertinent issues in relation to the psychological basis of the phenomena. A
more detailed understanding will enable researchers to explain the apparent
discrepancies that exist in the current literature, such as by specifying the conditions
under which exposure to multiple extinction contexts does and does not attenuate
The Return of Extinguished Conditioned Behaviour
57
renewal in laboratory-based studies. Moreover, closer links between the laboratorybased research and clinical-based studies will be forged. It is known that there are
differences between these two methodologies in fear acquisition with some cognitive
phenomena such as implicit associations being observed in naturally occurring
phobias, but not in newly conditioned fear responses (Boschen, Parker & Neumann,
2007). Likewise, there may be differences in the return of extinguished conditioned
behaviour that may suggest limits on the generalisability of laboratory-created anxiety
responses to a clinical context. As an example, Hermans et al. (2005) reported the
reinstatement of an artificially-induced fear reaction to a relatively fear-irrelevant
stimulus, but similar reinstatement effects have not yet been reliably found in
clinically-based studies (Rachman & Whittal, 1989a). Progressive research that
bridges the gap between the laboratory and the clinic will be needed. For instance, the
testing of reinstatement in the laboratory with fear-relevant stimuli (cf. Neumann &
Longbottom, submitted, who used a renewal procedure) may represent one step in this
process.
Due to the particular relevance that the return of extinguished conditioned
behaviour has for relapse in a clinical context, a particular exciting avenue for future
research is in delineating the conditions under which renewal, reinstatement, and
spontaneous recovery can be attenuated. However, there also remains an important
need for basic parametric studies to determine what fundamental variables influence
these phenomena in both increasing and decreasing the magnitude of their effects.
Likewise, theoretical explanations for the return of extinguished conditioned
behaviour in humans remain to be elaborated upon by using human studies. The
explanations regarding the importance of ambiguity following extinction and the use
of contextual cues to resolve this ambiguity as proposed by Bouton (2002, 2004;
The Return of Extinguished Conditioned Behaviour
58
Bouton et al., 2006) will provide the starting point for such research. The relationship
that such concepts have to existing theoretical approaches to conditioning and
extinction in humans, and in particular the role of cognitive processes in learning
(e.g., Davey 1987; Lovibond, 2004), promises to be an exciting future area of
theoretical development.
Finally, the return of extinguished conditioned behaviour remains to be
explored in children in either the laboratory or clinic. Such research has the potential
to increase the generality of phenomena such as renewal and reinstatement across the
lifespan. Moreover, further information on how return of extinguished behaviour
phenomena are implicated in relapse following exposure therapy also has relevance
for the treatment of children with anxiety disorders. Further research is warranted
given that childhood-onset anxiety affects up to 20% of children and is linked as a
risk factor for adult anxiety (McGee et al., 1992), depression (Pine et al., 1998), and
substance use disorders (Merikangas et al., 1999). Childhood anxiety disorders are
also associated with debilitating academic and vocational functioning (Kessler et al.,
1995) and impaired social competence (Spence, Donovan, & Brechmann-Touissant,
1999). The ethical difficulties in using noxious stimuli like electric shock and loud
tones as USs in fear conditioning procedures does limit further research. The adoption
of other unpleasant, but not painful or intense, stimuli as USs (Neumann & Waters,
2006; Neumann, Waters, & Westbury, in press) or the use of other associative
learning tasks (e.g., conditioned suppression task; Arcediano et al., 1996), may
provide a solution to this problem.
The Return of Extinguished Conditioned Behaviour
59
REFERENCES
Agras, S. (1965). An investigation of decrements of anxiety responses during
systematic desensitization. Behaviour Research and Therapy, 2, 267-270.
Ahlers, S. T. & Richardson, R. (1985). Administration of dexamethasone prior to
training blocks ACTH-induced recovery of an extinguished avoidance
response. Behavioral Neuroscience, 99, 760-764.
Angrilli, A., Mauri, .A, Palomba, D., Flor, H., Birbaumer, N., Sartori, G., et al.
(1996). Startle reflex and emotion modulation impairment after a right
amygdala lesion. Brain, 119, 1991-2000.
Alvarez, R. P., Ruben, P., Johnson, L., & Grillon, C. (2007). Contextual-specificity of
short-delay extinction in humans: Renewal of fear-potentiated startle in a
virtual environment. Learning and Memory, 14, 247-253.
Arcediano, F., Ortega, N., & Matute, H. (1996). A behavioural preparation for the
study of human Pavlovian conditioning. Quarterly Journal of Experimental
Psychology: Comparative & Physiological Psychology, 49B, 270-283.
Barlow, D.H., Raffa, S.D., & Cohen, E.M. (2002). Psychosocial treatments for panic
disorders, phobias and generalized anxiety disorder. In P.E. Nathan and J.M.
Gorman (Eds.), A guide to treatments that work (2nd ed., pp. 301-335). New
York: Oxford University Press.
Beeman, E. Y. & Grant, D. A. (1961). Delayed extinction and spontaneous recovery
following spaced and massed acquisition of the eyelid CR. The Journal of
General Psychology, 65, 293-300.
Boschen, M.J., Parker, I., & Neumann, D.L. (2007). Changes in implicit associations
do not occur simultaneously to Pavlovian conditioning of physiological
anxiety responses. Journal of Anxiety Disorders, 21, 788-803.
The Return of Extinguished Conditioned Behaviour
60
Bouton, M. E. (1984). Differential control by context in the inflation and
reinstatement paradigms. Journal of Experimental Psychology: Animal
Behavior Processes, 10, 56-74.
Bouton, M.E. (1993). Context, time, and memory retrieval in the interference
paradigms of Pavlovian learning. Psychological Bulletin, 114, 80- 99
Bouton, M. E. (2000). A learning theory perspective on lapse, relapse, and the
maintenance of behavior change. Health Psychology, 19, 57-63.
Bouton, M. E. (2002). Context, ambiguity, and unlearning: Sources of relapse after
behavioral extinction. Biological Psychiatry, 52, 976-986.
Bouton, M. E. (2004). Context and behavioral processes in extinction. Learning &
Memory, 11, 485-494.
Bouton, M. E., & Bolles, R. C. (1979). Role of conditioned contextual stimuli in
reinstatement of extinguished fear. Journal of Experimental Psychology:
Animal Behavior Processes, 5, 368-378.
Bouton, M. E., & Brooks, D. C. (1993). Time and context effects on performance in a
Pavlovian discrimination reversal. Journal of Experimental Psychology:
Animal Behavior Processes, 19, 165-179.
Bouton, M. E., & King, D. A. (1983). Contextual control of the extinction of
conditioned fear: Tests for the associative value of the context. Journal of
Experimental Psychology: Animal Behavior Processes, 9, 248-265.
Bouton, M. E., & King, D. A. (1986). Effect of context on performance to conditioned
stimuli with mixed histories of reinstatement and nonreinforcement. Journal of
Experimental Psychology: Animal Behavior Processes, 9, 248-265.
Bouton, M. E., Mineka, S., & Barlow, D. H. (2001). A modern learning theory on the
etiology of panic disorder. Psychological Review, 108, 4-32.
The Return of Extinguished Conditioned Behaviour
61
Bouton, M. E., & Peck, C. A. (1989). Context effects on conditioning, extinction, and
reinstatement in an appetitive conditioning preparation. Animal Learning and
Behavior, 17, 188-198.
Bouton, M. E., & Swartzentruber, D. (1989). Slow reacquisition following extinction:
Context encoding and retrieval mechanisms. Journal of Experimental
Psychology: Animal Behavior Processes, 15, 43-53.
Bouton, M. E., & Swartzentruber, D. (1991). Sources of relapse after extinction in
Pavlovian and instrumental learning. Clinical Psychology Review, 11, 123140.
Bouton, M. E., García-Gutiérreza, A., Zilskia, J., & Moody, E. W. (2006). Extinction
in multiple contexts does not necessarily make extinction less vulnerable to
relapse. Behaviour Research and Therapy, 44, 983-994.
Bouton, M. E., Kenney, F. A., & Rosengard, C. (1990). State-dependent fear
extinction with two benzodiazepine tranquilizers. Behavioural Neuroscience,
104, 44-55.
Bouton, M. E., Westbrook, K. A., Corcoran, K. A., & Maren, S. (2006). Contextual
and temporal modulation of extinction: Behavioral and biological
mechanisms. Biological Psychiatry, 60, 352-360.
Bradizza, C. M., Stasiewicz, P. R., & Maisto, S. A. (1994). A conditioning
reinterpretation of cognitive events in alcohol and drug cue exposure. Journal
of Behavior Therapy and Experimental Psychiatry, 25, 15-22.
Brandon, T. H., Piasecki, T. M., Quinn, E. P., & Baker, T. B. (1995) Cue exposure
treatment in Nicotine dependence, In D. C. Drummond, S. T. Tiffany, S
Glautier, & B. Remington (Eds) Addictive behavior: Cue exposure theory and
practice (pp. 211- 227). New York: Wiley.
The Return of Extinguished Conditioned Behaviour
62
Brooks, D. C. (2000). Recent and remote extinction cues reduce spontaneous
recovery. Quarterly Journal of Experimental Psychology, 153B, 25-58.
Brooks, D. C., & Bouton, M. E. (1993). A retrieval cue for extinction attenuates
spontaneous recovery. Journal of Experimental Psychology: Animal Behavior
Processes, 20, 366-379.
Brooks, D. C., & Bouton, M. E. (1994). A retrieval cue for extinction attenuates
response recovery (renewal) caused by a return to the conditioning context.
Journal of Experimental Psychology: Animal Behavior Processes, 20, 366379.
Calton, J. L., Mitchell, K. G., & Schachtman, T. R. (1996). Conditioned inhibition
produced by extinction of a conditioned stimulus. Learning and Motivation,
27, 335-361.
Chelonis, J. J., Calton, J. L., Hart, J. A., & Schachtman, T. R. (1999). Attenuation of
the renewal effect by extinction in multiple contexts. Learning and
Motivation, 30, 1-14.
Childress, A. R., McLellan, A.T., Natale, M., & O'Brien, C.P. (1987). Mood states
can elicit conditioned withdrawal and craving in opiate abuse patients NIDA
Res Monogr.;76:137-44.Links
Collins, B.N., & Brandon, T.H. (2002). Effects of extinction context and retrieval
cues on alcohol cue reactivity among nonalcoholic drinkers. Journal of
Consulting and Clinical Psychology, 70, 390-397.
Craske, M.G. & Rachman, S.J. (1987). Return of fear: Perceived skill and heart rate
responsivity. British Journal of Clinical Psychology, 26, 187-200.
Cunningham, C. L. (1979). Alcohol and a cue for extinction: State dependency
produced by conditioned inhibition. Animal Learning & Behavior, 7, 45-52.
The Return of Extinguished Conditioned Behaviour
63
Davey, G. C. (1992). Classical conditioning and the acquisition of human fears and
phobias: A review and synthesis of the literature. Advances in Behaviour
Research & Therapy 14, 29-66.
Davey, G.C.L. (2002). ‘Non-specific’ rather than ‘non-associative’ pathways to
phobias: A commentary on Poulton & Menzies. Behaviour Research and
Therapy, 40, 151-158.
Davenport, L., Hill, T., Wilson, M., & Ogden, E. (1997). Tracking and averaging in
variable environments: A transition rule. Journal of Experimental Psychology:
Animal Behavior Processes, 23, 450-460.
Davidson, T. L. (1993). The nature and function of interoceptive signals to feed:
Toward integration of physiological and learning perspectives. Psychological
Review, 100, 640-657.
Dawson, M. E., & Schell, A. M. (1985). Information processing and human autonomic
classical conditioning. Advances in Psychophysiology,1, 89-165.
Denniston, J.C., Chang, R.C., & Miller, R.R. (2003). Massive extinction treatment
attenuates the renewal effect. Learning and Motivation, 34, 68-86.
de Jong, P.J., van den Hout, M.A., & Merckelbach, H. (1995). Covariation bias and
return of fear. Behaviour Research and Therapy, 33, 211-213.
Dickson, A. (2001). Causal learning: An associative analysis. Quarterly Journal of
Experimental Psychology: Comparative and Physiological Psychology, 54B,
3-25.
Dirikx, T., Hermans, D., Vansteenwegen, D., Baeyens, F., & Eelen, P. (2004).
Reinstatement of extinguished conditioned responses and negative stimulus
valence as a pathway to return of fear in humans. Learning and Memory, 11,
549-554.
The Return of Extinguished Conditioned Behaviour
64
Dirikx, T., Hermans, D., Vansteenwegen, D., Baeyens, F., & Eelen, P. (2007).
Reinstatement of conditioned responses in human differential fear
conditioning. Journal of Behavior Therapy and Experimental Psychiatry, 38,
237-251.
Drummond, D. C., & Glautier, S. (1994). A controlled trial of cue exposure treatment
in alcohol dependence. Journal of Consulting and Clinical Psychology, 62,
809-817.
Drummond, D. C., Tiffany, S., Glautier, S., & Remington, B. (Eds.). (1995).
Addictive behaviour: Cue exposure theory and practice. New York: Wiley.
Effting, M. & Kindt, M. (2007). Contextual control of human fear associations in a
renewal paradigm. Behaviour Research and Therapy, 45, 2002-2018.
Ellson, D. G. (1939). Spontaneous recovery of the galvanic skin response as a
function of the recovery interval. Journal of Experimental Psychology, 25,
586-600.
Eich, J. E. (1995). Mood as a mediator of place dependent memory. Journal of
Experimental Psychology, 124, 293-308.
Emmelkamp, P.M.G. (1994). Behaviour therapy with adults. In A.E. Bergin & S.L.
Garfield (Eds.), Handbook of psychotherapy and behaviour change. New
York: Wiley.
Franklin, M.E., & Foa, E.B. (2002). Cognitive behavioural treatments for obsessive
compulsive disorder. In P.E. Nathan and J.M. Gorman (Eds.), A guide to
treatments that work (2nd ed., pp. 367-386). New York: Oxford University
Press.
Franks, C. M. (1963). Ease of conditioning and spontaneous recovery from
experimental extinction. British Journal of Psychology, 54, 351-357.
The Return of Extinguished Conditioned Behaviour
65
Fredrikson, M., Hugdahl, K., & Öhman, A. (1976). Electrodermal conditioning to
potentially phobic stimuli in male and female subjects. Biological Psychology,
4, 305-314.
García-Gutiérrez, A., & Rosas, J. M. (2003). Context change as the mechanism of
reinstatement in causal learning. Journal of Experimental Psychology: Animal
Behavior Processes, 29, 292-310.
Garcia-Gutierrez, A., Rosas, J. M., & Nelson, J. M. (2005). Extensive interference
attenuates reinstatement in human predictive judgments. International Journal
of Comparative Psychology, 18, 240-248.
Grey, S., Sartory, G., & Rachman, S. (1979). Synchronous and desyncrhronous
changes during fear reduction. Behaviour Research and Therapy, 17, 137-147.
Guastella, A.J., Lovibond, P.F., Dadds, M.R., Mitchell, P., & Richardson, R. (2007).
A randomized controlled trial of the effect of d-cycloserine on extinction and
fear conditioning in humans. Behaviour Research and Therapy, 45, 663-672.
Gunther, L. M., Denniston, J. C., & Miller, R. R. (1998). Conducting exposure
techniques in multiple settings can prevent relapse. Behaviour Research
Therapy, 36, 75-91.
Harris, J. A., Jones, M. L., Bailey, G. K., & Westbrook, R. F. (2000). Contextual
control over conditioned responding in an extinction paradigm. Journal of
Experimental Psychology: Animal Behavior Processes, 26, 174–185.
Havermans, R. C., Keuker, J., Lataster, T., & Jansen, A. (2005). Contextual control of
extinguished conditioned performance in humans. Learning and Motivation,
36, 1-19.
Hermans, D., Craske, M., Mineka, S., & Lovibond, P. F. (2006). Extinction in human
fear conditioning. Biological Psychiatry, 60, 361-368.
The Return of Extinguished Conditioned Behaviour
66
Hermans, D., Dirikx, T., Vansteenweginin, D., Baeyens, F., Van den Bergh, O.,
Eelen, P. (2005). Reinstatement of fear responses in human aversive
conditioning. Behaviour Research and Therapy, 43, 533-551.
Hitchcock, J. & Davis, M. (1986). Lesions of the amygdala, but not of the cerebellum
or red nucleus, block conditioned fear as measured with the potentiated startle
paradigm. Behavioral Neuroscience, 100, 11-22.
Hofmann, S.G., Meuret, A.E., Smits, J.A.J., Simon, N.M., Pollack, M.H.,
Eisenmenger, K., et al. (2006). Augmentation of exposure therapy with dcycloserine for social anxiety disorder. Archives of General Psychiatry, 63,
298-304.
Hovland, C. I. (1937). The generalization of conditioned responses: III. Extinction,
spontaneous recovery, and disinhibition of conditioned and generalized
responses. Journal of Experimental Psychology, 21, 47-62.
Hugdahl, K., Fredrikson, M., & Öhman, A. (1977). "Preparedness" and "arousability"
as determinants of electrodermal conditioning. Behavior Research and
Therapy, 15, 345-353.
Hugdahl, K., & Johnsen, B. H. (1989). Preparedness and electrodermal fearconditioning: Ontogenetic vs phylogenetic explanations. Behavior Research
and Therapy, 27, 269-278.
Johnson, D. M., Baker, J. D., & Azorlosa, J. L. (2000). Acquisition, extinction, and
reinstatement of Pavlovian fear conditioning: the roles of the NMDA receptor
and nitric oxide. Brain Research, 28, 66-70.
Kessler, R. C., Foster, C. L., Saunders, W. B., & Stang, P. E. (1995). Social
consequences of psychiatric disorders I: Educational attainment. American
Journal of Psychiatry, 46, 1567-1578.
The Return of Extinguished Conditioned Behaviour
67
Kroenke, K., Spitzer, R.L., Williams, J.B., Monahan, P.O., & Lowe, B. (2007).
Anxiety disorders in primary care: Prevalence, impairment, comorbidity, and
detection. Annals of Internal Medicine, 146, 317-325.
LaBar, K. S., & Phelps, E. A. (2005). Reinstatement of conditioned fear in humans is
context dependent and impaired in amnesia. Behavioral Neuroscience, 119,
677-686.
Lang, A.J., & Craske, M.G. (2000). Manipulations of exposure-based therapy to
reduce return of fear: A replication. Behaviour Research and Therapy, 38, 112.
Lewinsohn, P.M. (1974). A behavioural approach to depression. In R.M. Friedman, &
M.M. Katz (eds.), The Psychology of depression: Contemporary theory and
research. New York: Wiley.
Lipp, O. V., & Neumann, D. L. (2004). Attentional blink reflex modulation in a
continuous performance task is modality specific. Psychophysiology, 41(3),
417-425.
Lipp, O.V., Neumann, D.L., & Mason, V. (2001). Stimulus competition in affective
and relational learning. Learning and Motivation, 32(3), 306-331.
Lipp, O. V., Neumann, D. L., McHugh, M. R. (2002). Lead stimulus modality change
and the attentional modulation of the acoustic and electrical blink reflex.
Biological Psychology, 62, 27-48.
Lipp, O. V., Neumann, D. L., & Pretorius, N. (2003). Attentional blink modulation
during sustained and after discrete lead stimuli presented in three sensory
modalities. Psychophysiology, 40, 285-290.
Lipp, O. V., Neumann, D. L., Siddle, D. A. T., & Dall, P. J. (2001). Assessing the
effects of attention and emotion on blink startle modulation. Journal of
The Return of Extinguished Conditioned Behaviour
68
Psychophysiology, 15, 173-182.
Lissek, S., Powers, A. S., McClure, E. B., Phelps, E. A., Woldehawariat, G., Grillon,
C., & Pine, D. S. (2005). Classical fear conditioning in the anxiety disorders:
A meta-analysis. Behaviour Research and Therapy 43, 1391-1424.
Lochner, C., Mogotski, M., du Toit, P.L., Kaminer, D., Niehaus, D.J., & Stein, D.J.
(2003). Quality of life in anxiety disorders: A comparison of obsessivecompulsive disorder, social anxiety disorder, and panic disorder.
Psychopathology, 36, 255-262.
McGee, R., Feehan, M., Williams, S. & Anderson, J. (1992). DSM-III disorders from
age 11 to age 15 years. Journal of the American Academy of Child &
Adolescent Psychiatry, 31, 50-59.
Merikangas, K. R., Avenevoli, S., Dierker, L. & Grillon, C. (1999). Vulnerability
factors among children at risk for anxiety disorders. Society of Biological
Psychiatry, 99, 172-179.
Milad, M. R., Orr, S. P., Pitman, R. K., & Rauch, S. L. (2005). Context modulation of
memory for fear extinction in humans. Psychophysiology, 42, 456- ???
Mineka, S., Mystkowski, J.L., Hladek, D., & Rodriguez, B.I. (1999). The effects of
changing contexts on return of fear following exposure therapy for spider fear.
Journal of Consulting and Clinical Psychology, 67, 599-604.
Mineka, S., & Zinbarg, R. (2006). A contemporary learning theory perspective on the
etiology of anxiety disorders: It’s not what you thought it was. American
Psychologist, 61, 10-26.
Mystkowski, J.L., Mineka, S., Vernon, L.L., & Zinbarg, R.E. (2003). Changes in
caffeine states enhance return of fear in spider phobia. Journal of Consulting
and Clinical Psychology, 71, 243-250.
The Return of Extinguished Conditioned Behaviour
69
Mystkowski, J.L., Craske, M.G., Echiverri, A.M., & Labus, J.S. (2006). Mental
reinstatement of context and return of fear in spider-fearful participants.
Behavior Therapy, 37, 49-60.
Napier, R. M., Macrae, M., & Kehoe, E. J. (1992). Rapid reacquisition in conditioning
of the rabbit’s nicitating membrane response. Journal of Experimental
Psychology: Animal Behavior Processes, 18, 182-192.
Neumann, D. L. (2002). Effects of mental workload on the startle eyeblink reflex.
Ergonomics, 45, 583-602.
Neumann, D. L. (2006). The effects of physical context changes and multiple
extinction contexts on two forms of renewal in a conditioned suppression task
with humans. Learning and Motivation, 37, 149-175.
Neumann, D. L. (2007). The resistance of renewal to instructions that devalue the role
of contextual cues in a conditioned suppression task with humans. Learning
and Motivation, 38, 105-127.
Neumann, D. L. (in press). The effects of context changes on the reinstatement of
extinguished conditioned behavior in a conditioned suppression task. Learning
and Motivation.
Neumann, D. L., & Lipp, O. V. (2003). The independent effects of attention and lead
stimulus properties on the acoustic blink reflex. Journal of Psychophysiology,
17, 124-134.
Neumann, D. L., Lipp, O. V., & Cory, S. E. (2007). Conducting extinction in multiple
contexts does not necessarily attenuate the renewal of shock expectancy in a
fear conditioning procedure with humans. Behaviour Research and Therapy,
45, 385-394.
The Return of Extinguished Conditioned Behaviour
70
Neumann, D. L., Lipp, O. V., & McHugh M. R. (2004). The effect of stimulus
modality and task difficulty on attentional modulation of blink startle.
Psychophysiology,41, 407-416.
Neumann, D. L., Lipp, O. V., & Pretorius, N. (2004). The effects of lead stimulus and
reflex stimulus modality on modulation of the eyeblink reflex at very short,
short, and long lead intervals. Perception and Psychophysics, 66, 141-151.
Neumann, D. L., Lipp, O. V., & Siddle, D. A. T. (2002). Discriminating between
task-relevant and task-irrelevant stimuli: The effects on autonomic orienting
and secondary task reaction time. Journal of Psychophysiology, 16, 191-200.
Neumann, D. L., Lipp, O. V., & Siddle, D. A. T. (1997). Conditioned inhibition of
autonomic Pavlovian conditioning in humans. Biological Psychology, 46, 223233.
Neumann, D. L., & Longbottom, P. L. (submitted). The renewal of extinguished
conditioned fear with fear-relevant and fear-irrelevant stimuli by a context
change after extinction.
Neumann, D. L., & Waters, A. M. (2006). The use of an unpleasant sound as a
unconditional stimulus in a human aversive Pavlovian conditioning procedure.
Biological Psychology, 73, 175-185.
Neumann, D. L., Waters, A. M., & Westbury, H. R. (in press). The use of an
unpleasant sound as the unconditional stimulus in aversive Pavlovian
conditioning experiments that involve children and adolescent participants.
Behavior Research Methods.
Niaura, R., Britt, D. M., Borrelli, B., Shadel, W. G., Abrams, D. B., & Goldstein, M.
G. (1999). History and symptoms of depression among smokers during a selfinitiated quit attempt. Nicotine & Tobacco Research, 1, 251–257.
The Return of Extinguished Conditioned Behaviour
71
Öhman, A., Fredrikson, M., Hugdahl, K., & Rimmö, P. A. (1976). The premise of
equipotentiality in human classical conditioning: Conditioned electrodermal responses
to potentially phobic stimuli. Journal of Experimental Psychology: General,
105, 313-337.
Öhman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: toward an
evolved module of fear and fear learning. Psychological Review, 108, 483522.
Öhman, A., Hamm, A., & Hugdahl, K. (2000). Cognition and the autonomic nervous
system: Orienting, anticipation, and conditioning. In J. T. Cacioppo, L. G.
Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology (2nd ed.)
(pp. 533-575). New York, NY: Cambridge University Press.
Olatunji, B.O., Cisler, J.M., & Tolin, D.F. (2007). Quality of life in the anxiety
disorders: A meta-analytic review. Clinical Psychology Review, 27, 572-581.
Öst, L.-G. (1989). One-session group treatment of spider phobia. Behaviour Research
and Therapy, 34, 707-715.
Paredes-Olay, C., & Rosas, J. M. (1999). Within-subjects extinction and renewal in
predictive judgments. Psychologica, 20, 195-210.
Pine, D., Cohen, P., Gurley, D., Brook, J., & Ma, Y. (1998). The risk for earlyadulthood anxiety and depressive disorders in adolescents with anxiety and
depressive disorders. Archives of General Psychiatry, 55, 56-64.
Pavlov, I. (1927). Conditioned Reflexes. New York: Oxford University Press.
Philips, H.C. (1985). Return of fear in the treatment of a fear of vomiting. Behaviour
Research and Therapy, 23, 45-52.
Pitman, R.L., Shalev, A.Y., & Orr, S.P. (2000). Posttraumatic stress disorder:
emotion, conditioning, and memory. In M.S. Gazzaniga (Ed.), The new
The Return of Extinguished Conditioned Behaviour
72
cognitive neurosciences (2nd ed.) (pp. 1133–1147). Cambridge, MA: MIT
Press.
Rachman, S. (1966). Studies in desenstization-III. Speed of generalization. Behaviour
Research and Therapy, 4, 7-16.
Rachman, S. (1979). The return of fear. Behaviour Research and Therapy, 17, 164165.
Rachman, S. (1989). The return of fear: Review and prospect. Clinical Psychology
Review, 9, 147-168.
Rachman, S. (1991). Neo-conditioning and the classical theory of fear acquisition.
Clinical Psychology Review, 11, 155-173.
Rachman, S.J., & Levitt, K. (1985). Panics and their consequences. Behaviour
Research and Therapy, 23, 585-600.
Rachman, S., & Whittal, M. (1989a). The effect of an aversive event on the return of
fear. Behaviour Research and Therapy, 27, 513-520.
Rachman, S., & Whittal, M. (1989b). Fast, slow and sudden reductions in fear.
Behaviour Research and Therapy, 27, 613-620.
RANZCP Clinical Practice Guidelines Team for Panic Disorder and Agoraphobia
(2003). Australian and New Zealand clinical practice guidelines for the
treatment of panic disorder and agoraphobia. Australian and New Zealand
Journal of Psychiatry, 37, 641-656.
Rapaport, M.J., Clary, C., Fayyad, R., & Endicott, J. (2005). Quality-of-life
impairment in depressive and anxiety disorders. American Journal of
Psychiatry, 162, 1171-1178.
Rauhut, A. S., Thomas, B. L., & Ayres, J. J. B. (2001). Treatments that weaken
Pavlovian conditioned fear and thwart its renewal in rats: Implications for
The Return of Extinguished Conditioned Behaviour
73
treating human phobias. Journal of Experimental Psychology: Animal
Behavior Processes, 27, 99-114.
Rescorla, R. A. (2004). Spontaneous Recovery. Learning and Memory, 11, 501-509.
Rescorla, R.A., & Heth, C.D. (1975). Reinstatement of fear to an extinguished
conditioned stimulus. Journal of Experimental Psychology: Animal Behavior
Processes, 1, 88-96.
Ressler, K.J., Rothbaum, B.O., Tannenbaum, L., Anderson, P., Graap, K., Zimand, E.,
et al. (2004). Cognitive enhancers as adjuncts to psychotherapy: Use of dcycloserine in phobic individuals to facilitate extinction of fear. Archives of
General Psychiatry, 61, 1136-1144.
Ricker, S. T., & Bouton, M. E. (1996). Reacquisition following extinction in
appetitive conditioning. Animal Learning and Behavior, 24, 423-436.
Robbins, S. J. (1990). Mechanisms underlying spontaneous recovery in autoshaping.
Journal of Experimental Psychology: Animal Behavior Processes, 16, 235249.
Rodriguez, B. I. I., Craske, M. G., Mineka, S., & Hladek, D. (1999). Contextspecificity of relapse: Effects of therapist and environmental context on return
of fear. Behaviour Research and Therapy, 37, 845-862.
Rosas, J. M., & Bouton, M. E. (1997). Context change and retention interval can have
additive, rather than interactive effects after taste aversion extinction.
Psychonomic Bulletin Review, 5, 79-83
Rosas, J. M. & Callejas-Aguilera, J. M. (2006). Context Switch Effects on
Acquisition and Extinction in Human Predictive Learning. Journal of
Experimental Psychology: Learning, Memory, and Cognition, 32, 461-474.
Rose, M.P., & McGlynn, F.D. (1997). Toward a standard experiment for studying
The Return of Extinguished Conditioned Behaviour
74
post-treatment return of fear. Journal of Anxiety Disorders, 11, 263-277.
Rowe, M.K., & Craske, M.G. (1998a). Effects of an expanding-spaced vs massed
exposure schedule on fear reduction and return of fear. Behaviour Research
and Therapy, 36, 701-717.
Rowe, M.K., & Craske, M.G. (1998b). Effects of varied-stimulus exposure training
on fear reduction and return of fear. Behaviour Research and Therapy, 36,
719-734.
Salkovskis, P., & Mills, I. (1994). Induced mood, phobic responding and the return of
fear. Behaviour Research and Therapy, 32, 439-445.
Samsom, D., & Rachman, S. (1989). The effect of induced mood on fear reduction.
British Journal of Clinical Psychology, 28, 227-238.
Sartory, G., Rachman. S., & Grey, S. (1982). Return of fear: The role of rehearsal.
Behaviour Research and Therapy, 20, 123-133.
Spence, S. H., Donovan, C., & Brechman-Toussaint, M. (1999). Social skills, social
outcomes, and cognitive features of childhood social phobia. Journal of
Abnormal Psychology, 108, 211-221.
Stasiewicz, P. R., Brandon, T. H., Bradizza, C. M. (2007). Effects of extinction
context and retrieval cues on renewal of alcohol-cue reactivity among alcoholdependent outpatients. Psychology of Addictive Behaviors, 21(2), 244-248.
Stasiewicz, P. R., Gulliver, S. B., Bradizza, C. M., Torrisi, R., Rohsenow, D. J., &
Monti, P. M. (1997). Exposure to negative affect and reactivity to alcohol cues
during alcohol cue exposure. Behaviour Research and Therapy, 35, 1143–
1149.
The Return of Extinguished Conditioned Behaviour
75
Thewissen, R., Snijders, S. J. B. D., Havermans, R. C., van den Hout, M., & Jansen,
A. (2006). Renewal of cue-elicited urge to smoke: Implications for cue
exposure treatment. Behaviour Research and Therapy, 44, 1441-1449
Thomas, B. L., Larsen, N. & Ayres, J. J. B. (2003). Role of context similarity in ABA,
ABC, and AAB renewal paradigms: Implications for theories of renewal and
for treating human phobias. Learning and Motivation, 34, 410-436.
Tryon, W.W. (2005). Possible mechanisms for why desensitization and exposure
therapy work. Clinical Psychology Review, 25, 67-95.
Van Damme, S., Crombez, G., Hermans, D., Koster, E. H. W., & Eccleston, C.
(2006). The role of extinction and reinstatement in attentional bias to threat: A
conditioning approach. Behaviour Research and Therapy, 44, 1555-1563.
Vansteenwegen, D., Dirikx, T,, Hermans, D., Vervliet, B., & Eelen, P. (2006).
Renewal and reinstatement of fear: Evidence from human conditioning
research. In M. G. Craske, D. Hermans, & D. Vansteenwegen (Eds.), Fear and
learning: From basic processes to clinical implications (pp. 197-215).
Washington, DC: American Psychological Association.
Vansteenwegen, D., Hermans, D., Vervliet, B., Francken, G., Beckers, T., Baeyens,
F., et al. (2005). Return of fear in a human differential conditioning paradigm
caused by a return to the original acquisition context. Behaviour Research and
Therapy, 43, 323-336.
Vansteenwegen, D., Vervliet, B., Hermans, D., Beckers, T., Baeyens, F., & Eelen, P.
(2006). Stronger renewal in human fear conditioning when tested with an
acquisition retrieval cue than with an extinction retrieval cue. Behaviour
Research and Therapy, 44, 1717-1725.
Vansteenwegen, D., Vervliet, B., Hermans, D., Thewissen, R., Eelen, P. (2007).
The Return of Extinguished Conditioned Behaviour
76
Verbal, behavioural and physiological assessment of the generalization of
exposure-based fear reduction in a spider-anxious population. Behaviour
Research and Therapy, 45, 291-300.
Vervliet, B., Vansteenwegen, D., Baeyens, F., Hermans, D., & Eelen, P. (2005).
Return of fear in a human differential conditioning paradigm caused by a
stimulus change after extinction. Behaviour Research and Therapy, 43, 357371.
Vila, N. J., Romero, M. A., & Rosas, J. M. (2002). Retroactive interference after
discrimination reversal decreases following temporal and physical context
changes in human subjects. Behavioural Processes, 59, 47-54.
Vila, N. J., & Rosas, J. M. (2001). Reinstatement of acquisition performance by
presentation of the outcome after extinction in causality judgments.
Behavioural Processes, 56, 147-154.
Waters, W.F., McDonald, D.G., & Koresko, R.L. (1972). Psychophysiological
responses during analogue systematic desensitization and non-relaxation
control procedures. Behaviour Research and Therapy, 10, 381-393.
Westbrook, R.F., Iordanova, M., McNally, G., Richardson, R., & Harris, J.A. (2002).
Reinstatement of fear to an extinguished conditioned stimulus: Two roles for
context. Journal of Experimental Psychology: Animal Behavior Processes, 28,
97-110.
Wilson, A., Brooks, D. C., & Bouton, M. E. (1995). The role of the rat hippocampal
system in several effects of context in extinction. Behavioral Neuroscience,
109, 828-836.
Wood, B.S., & McGlynn, F.D. (2000). Research on posttraumatic return of
claustrophobic fear, arousal and avoidance using mock diagnostic imaging.
The Return of Extinguished Conditioned Behaviour
77
Behaviour Modification, 24, 379-394.
Yonkers, K.A., Bruce, S.E., Dyck, I.R., & Keller, M.B. (2003). Chronicity, relapse,
and illness-course of panic disorder, social phobia, and generalized anxiety
disorder: Findings in men and women from 8 years of follow-up. Depression
and Anxiety, 17, 173-179.