Neurophysiologie clinique 34 (2004) 33–39

www.elsevier.com/locate/neucli

ORIGINAL ARTICLE

Fear-conditioned cues of impending pain facilitate

attentional engagement
Stefaan Van Damme a,b,*, Jürgen Lorenz c, Christopher Eccleston d,
Ernst H.W. Koster a, Armand De Clercq e, Geert Crombez a,b
a
Department of Psychology, Ghent University, Henri Dunantlaan 2, B-9000 Ghent, Belgium
b
Research Institute for Psychology and Health, P.O. Box 80.140, 3508 TC Utrecht, The Netherlands
c
University of Hamburg, Institute of Neurophysiology and Pathophysiology, Martinistrabe 52,
20246 Germany
d
Department of Psychology, University of Bath, Claverton Down, Bath BA2 7AY, UK
e
Department of Applied Mathematics and Computer Science, Ghent University, Krijgslaan 281 (S9),
B-9000 Ghent, Belgium
Received 7 August 2003; revised and accepted 17 November 2003

KEYWORDS Abstract
Selective attention; Aims of study. – Selective attention to signals of impending pain allows the avoidance of
Experimental pain; bodily harm. In order to identify the attentional components involved in the selection of
Classical conditioning pain signals over competing demands, we used an emotional modification of an exogenous
cueing task.
Methods. – Fifty-two pain-free volunteers detected visual targets of which the location
was correctly or incorrectly predicted by a spatial cue. Cues were emotionally modulated
using differential classical conditioning. The conditioned cue (CS+) was sometimes
followed by an electrocutaneous stimulus (UCS), thus becoming a pain signal, whereas the
UCS never followed the other cue (CS–), referred to as safety signal.
Results. – Analyses of response times showed that pain signals facilitated the directing of
attention to their location in comparison to safety signals. In contrast, pain signals did not
impair disengagement of attention from their location in comparison to safety signals.
Conclusion. – It is concluded that attention is more strongly engaged to a signal of
impending pain compared with a cue signalling its absence. We explore why disengage-
ment from the pain signal is not impaired compared to the safety signal. The findings are
discussed in terms of the defensive importance of pain anticipation.
© 2003 Elsevier SAS. All rights reserved.

Résumé
MOTS CLÉS
Attention sélective ; Objectifs. – L’attention sélective dirigée vers un signal de la douleur imminente permet
Douleur d’éviter les dommages physiques. Afin d’identifier les composantes attentionnelles
expérimental ; impliquées dans la sélection des signaux de la douleur, nous avons utilisé une version
Conditionnement émotionnelle de la tâche d’indiçage.
classique Méthodes. – Cinquante-deux sujets volontaires sains avaient pour tâche de détecter des
cibles visuelles, dont la localisation spatiale était annoncée — de façon correcte ou
incorrecte — par un indice spatial. La valence émotionnelle de l’indice était induite à

* Corresponding author. Faculty of Psychology and Educational Sciences, Ghent University, Henri Dunantlaan 2, 9000 Ghent,
Belgium. Tel.: +32-9-2649105; fax: +32-9-2649149.
E-mail address: Stefaan.VanDamme@UGent.be (S. Van Damme).

© 2003 Elsevier SAS. All rights reserved.

doi: 10.1016/S0987-7053(03)00102-3
34 S. Van Damme et al.

l’aide d’une procédure de conditionnement classique. Lors de certains essais, l’indice

conditionné (CS+) était suivi d’un stimulus électrique nociceptif (UCS), devenant alors un
signal de douleur. En revanche, aucun UCS ne suivait l’indice non conditionné (CS–), qui
devenait alors un signal de sécurité.
Résultats. – L’analyse des temps de réaction a montré que le signal de douleur facilitait
la direction de l’attention vers sa localisation spatiale, en comparaison au signal de
sécurité. En revanche, le signal de douleur ne détériorait pas le désengagement de sa
localisation spatiale, par rapport au signal de sécurité.
Conclusion. – Nous concluons que l’attention est attirée plus fortement par un signal de
douleur imminente en comparaison à un signal annonçant l’absence de douleur. Nous
explorons pourquoi le désengagement du signal de douleur n’est pas détérioré en
comparaison au signal de sécurité. Les résultats sont discutés en termes de caractère
défensif de l’anticipation de la douleur.
© 2003 Elsevier SAS. All rights reserved.

Introduction the mechanisms by which pain signals capture at-

The question of how pain attracts attention over
competing demands has become a substantial re-
search topic over the last decade. There is already
a significant amount of research documenting the
effects of pain on attention. The idea that pain
demands attention, interrupts ongoing activities,
and interferes with present demands has been sup-
ported by numerous studies in both clinical and
non-clinical populations. These studies feature a
variety of research methods, such as behavioural
tasks [2,5,12,29,33], psychophysiological measures
[9,10,19,20], and functional brain imaging [1,8,24].
Eccleston and Crombez [13] developed a
cognitive-affective model in which they argued
that the interruption of attention by pain is a
normal and evolutionary adaptive process. Accord-
ing to these authors, pain has a processing priority
by activating a primitive defensive system that
urges escape from somatic threat. Although pain
can occur without warning, the learning of signals
of impending pain significantly contributes to this
protective function. For example, when we hear
the humming of a wasp while eating a fruit, our
attention will be immediately drawn to the threat
of a painful sting, and we will attempt to escape
from this situation. The idea that pain anticipation
subserves an important protective function has
been supported by neurophysiological research in
both clinical and non-clinical populations. For in-
stance, in a number of functional brain imaging
studies, changes in activity of cortical nociceptive
networks were measured during anticipation of
pain and during actual painful stimulation. It was
found that cortical networks involved in the pro-
cessing of pain itself were already activated during
anticipation of pain, suggesting that these locations
are directly affected by cognitive factors such as
attention [25,26]. However, little is known about
tention, facilitating the detection of pain itself.
Dawson et al. [6] investigated the allocation of
attention to signals of impending pain. They asked
participants to concentrate on the differential con-
ditioning of visual stimuli. The conditioned stimulus
(CS+) was frequently followed by an electrical
shock, thus becoming a pain signal. The other
stimulus (CS–) was never followed by an electrical
shock. Furthermore, participants were asked to
perform an auditory reaction time task as a second-
ary task. The authors found that reaction times to
auditory stimuli were significantly slower during
CS+ presentation than during CS– presentation, sug-
gesting an increased allocation of cognitive re-
sources to pain signals [6]. Because this study mea-
sured general attentional deployment through the
interference of task performance by pain signals, a
more detailed understanding of the attentional
sub-components involved was not possible.
In general, three components of attention to all
forms of threat can be distinguished [14,15,23,33]:
(1) an initial transient shift of attention to a threat-
ening stimulus, (2) a sustained engagement with
the threatening stimulus, and (3) disengagement
from the threatening stimulus. In order to differen-
tiate these attentional components during the pro-
cessing of pain signals, we used an emotional modi-
fication of an exogenous cueing paradigm,
originally developed by Posner et al. [27]. In an
exogenous cueing paradigm, participants are asked
to detect a visual target presented at the left or
right side of a fixation cross. Targets are preceded
by a visual cue at the same spatial location (validly
cued trials) or at the opposite location (invalidly
cued trials). Presenting a spatial cue facilitates or
inhibits target detection in comparison with a con-
dition in which no spatial cues are presented: the
presentation of a valid cue typically leads to re-
sponse time benefits (due to attentional engage-
Fear-conditioned cues of impending pain facilitate attentional engagement
ment at the correctly cued location), whereas the
presentation of an invalid cue leads to response
time costs (due to attentional disengagement from
the incorrectly cued location), described as the cue
validity effect [27]. In the present study, spatial
cues are emotionally modulated by a differential
classical conditioning procedure. A nociceptive
stimulus (UCS) sometimes follows the conditioned
cue (CS+), rendering it a pain signal. In contrast,
the UCS never follows the other cue (CS–), which we
refer to as the “safety signal” according to Selig-
man’s hypothesis [28]. Using this paradigm we hy-
pothesize that two components of attention to
signals of impending pain will be differentiated:
First, we expect facilitated attentional engage-
ment to pain signals, indicated by stronger re-
sponse time benefits when the CS+ in comparison
with the CS– is used as a valid spatial cue. Second,
difficulty disengaging from pain signals should be
indicated by stronger response time costs when the
CS+ in comparison with the CS– is used as an invalid
spatial cue.
Until now, most studies investigated the effect
of pain on attention. The present study is one of the
first to investigate the effect of pain anticipation
on spatial attention. Furthermore, the present
study differs from previous work in providing a
detailed examination of the underlying attentional
components.
Method
Participants
Fifty-two undergraduate psychology students (eight
males and 44 females; mean age = 19.04 years)
participated to fulfil course requirements. All par-
ticipants gave their informed consent and were free
to terminate the experiment at any time. Each
person had normal or corrected-to-normal eye-
sight. Experimental duration was approximately
30 min.
Apparatus and test material
The exogenous cueing task was programmed and
presented by the INQUISIT Millisecond software
package (Inquisit 1.32, 2001) on a S710 Compaq
Deskpro computer with a 72 Hz, 17-inch color moni-
tor. INQUISIT measures response times with a milli-
second accuracy [7].
Target stimuli consisted of black squares (1.1 by
1.1 cm), presented on a white background. Two
colour slides (green and pink; 4.8 cm high × 6.5 cm
wide) were used as spatial cues for the location of
35
the targets. Each trial began with a fixation cross in
the middle of the screen (duration of 1000 ms).
Cues were presented 9.2° from the fixation cross
for a duration of 200 ms. Target onset followed
immediately after cue offset. On half of the test
trials, cue location correctly predicted target loca-
tion (validly cued trials). On the other half of the
test trials, cue location incorrectly predicted target
location (invalidly cued trials). Participants were
seated 60 cm from the computer screen. They were
instructed to respond to the left targets by pressing
the ‘q’ key with the left index finger and to the
right targets by pressing the ‘5’ key with the right
index finger on a standard AZERTY computer key-
board. A trial ended when a participant responded
or 2000 ms had elapsed. In order to control for
responses to cues instead of targets, a number of
trials were presented, in which the cue was not
followed by a target (catch trials). Furthermore, in
order to ensure that participants maintained gaze
at the middle of the screen, a number of control
trials were presented. In these trials, the fixation
cross was followed only by a randomly selected
digit between 1 and 9 for a duration of 50 ms (digit
trials). Participants were instructed to report the
digit aloud. If participants were not able to report
the digits (correctly), this indicated that they did
not maintain gaze at the fixation cross.
Cues were emotionally modulated by a differen-
tial classical conditioning procedure. The condi-
tioned cue (CS+) was on one third of the presenta-
tions followed by a nociceptive stimulus (UCS). The
other cue (CS–) was never followed by an UCS. The
UCS was a transcutaneous electrocutaneous stimu-
lus, delivered by a Digitimer constant current
stimulator (Digitimer DS7A, 1998). Intensity of the
electrocutaneous stimulus was selected individu-
ally by each participant (see below). Electrocuta-
neous stimuli had an instantaneous rise and fall
time, and a duration of 750 ms. The stimuli were
delivered by two lubrificated Fukuda standard
Ag/AgCl electrodes (1 cm diameter) attached to
the external side of the right ankle. The skin at the
electrode sites was first abraded with a peeling
cream (Nihon Kohden) to reduce skin resistance.
Which colour was CS+ or CS– was counterbalanced
across participants. The CS+ and CS– were pre-
sented equally often, in a fixed random order with
no more than three consecutive presentations of
one cue.
Procedure
Participants were tested individually in a sound-
attenuated room designed for psychophysiological
experiments.
36
Figure 1 Schematic illustration of the four trial types. On each trial, a fixation cross was presented for 1000 ms. This was immediately
followed by the presentation of a cue (200 ms duration). Immediately after cue offset the target was introduced. Targets were
presented at the same location of cues (validly cued trials), or at the opposite location of cues (invalidly cued trials). The CS+ was
followed by the UCS in one third of the trials.
Preparation phase
Participants were informed that an electrocutane-
ous stimulus would be used during the experiment.
They were further informed that this stimulus
“stimulates the pain fibres and that most people
find this kind of stimulation unpleasant”. After this,
participants gave informed consent. To familiarise
the participants with the electrocutaneous stimuli,
they were given a series of stimuli with increasing
intensity. They were asked to select a stimulus
which they found aversive but tolerable, and which
required a certain effort to deal with. The electro-
cutaneous stimulus chosen by the participant was
set as the intensity used during the experiment.
Practice phase
Participants were seated in front of a computer to
perform the exogenous cueing task. All instructions
were presented on the computer screen. Partici-
pants were instructed to respond to the targets as
quickly as possible, without sacrificing accuracy.
Participants were informed about cues and targets,
and they were asked to respond only to the location
of the targets by pressing on the corresponding key.
Participants were told that cues would predict tar-
get location on some of the trials. Furthermore,
they were informed that there would be trials on
which only a cue but no target would appear and
they were asked not to respond on these trials. They
were told that there would also be trials in which
S. Van Damme et al.
only a digit would appear which they had to report
aloud. The practice phase consisted of 10 trials:
four validly cued trials, four invalidly cued trials,
one catch trial, and one digit trial. Participants
were made aware of the fact that no electrocutane-
ous stimuli would be presented during this phase.
Experiment phase
Participants were informed that one type (colour)
of cue would sometimes be followed by an electro-
cutaneous stimulus, and that the other type of cue
would never be followed by an electrocutaneous
stimulus. Participants did not know in advance
which cue would be followed by the electrocutane-
ous stimulus. The experiment phase consisted of
165 trials: 72 validly cued trials, 72 invalidly cued
trials, 12 catch trials, and nine digit trials. One
third of the CS+ presentations was followed by an
electrocutaneous stimulus (UCS). These trials were
not analysed in order to make sure that the effect
of the CS+ was not confounded by the effect of the
UCS. The experiment phase started with two buffer
trials in which the CS+ was followed by an UCS in
order to facilitate the differential conditioning.
Fig. 1 shows a schematic illustration of the four trial
types used in the study.
Post-experiment phase
As a method check, participants rated to what
extent they expected an electrocutaneous stimulus
following the CS+ and the CS– on an 11-point nu-
Fear-conditioned cues of impending pain facilitate attentional engagement
merical graphic rating scale (anchored zero = not at
all to 10 = very strongly). On a similar scale, partici-
pants also rated how aversive they found the elec-
trocutaneous stimulus.
Statistical analyses
A 2 (cue validity: valid, invalid) × 2 (signal: CS+,
CS–) ANOVA with repeated measures was performed
upon the mean response times (RT). Responses
faster than 150 ms were considered as responses to
cues instead of targets, and were removed from the
RT analyses. Greenhouse-Geisser corrections (with
corrected degrees of freedom) are presented
where the sphericity assumption is violated
(Mauchly’s test of sphericity; P < 0.05).
Results
Participants rated the electrocutaneous stimulus as
aversive (M = 6.38, S.D. = 1.51). The differential
conditioning procedure was successful. Partici-
pants expected the electrocutaneous stimulus sig-
nificantly more after the presentation of a CS+
(M = 6.94, S.D. = 2.22) than after the presentation
of a CS– (M = 0.71, S.D. = 1.64), t(51) = 14.72,
P < 0.001.
The mean percentage of error rates was rather
small for responses to validly cued CS+ trials
(0.62%), validly cued CS– trials (0.44%), invalidly
cued CS+ trials (2.96%), and invalidly cued CS– trials
(1.18%). Participants responded (erroneously) to
3.37% of the catch trials. They complied with gaze
fixation, consistently reporting the digits. All error
trials (1.31%) and outliers (RTs less than 150 ms or
greater than 750 ms; 1.03%) were removed from the
RT analyses. Also the trials in which the CS+ was
followed by an electrocutaneous stimulus (UCS)
were removed from the analyses, in order to pre-
vent that the effect of the UCS would confound the
effect of the CS+. The mean RT was then calculated
for each participant as a function of each factor in
the design.
A 2 (cue validity: valid, invalid) × 2 (signal: CS+,
CS–) ANOVA with repeated measures showed a sig-
nificant main effect of cue validity, F(1.51) = 30.59,
MSE = 548.24, P < 0.001, indicating that responses
to validly cued targets were faster than responses
to invalidly cued trials (331 vs. 349 ms). The main
effect of signal was not significant, F(1.51) = 2.34,
MSE = 238.13 ns. Of particular importance for this
study was the significant interaction effect of cue
validity × signal, F(1.51) = 5.93, MSE = 214.93,
P < 0.05. This interaction was further analysed in
terms of engagement and disengagement effects.
37
The engagement component relates to response
times on validly cued trials. In particular, we tested
whether the presentation of the CS+ as valid cue
facilitated target detection compared to the pre-
sentation of the CS– as a valid cue. The disengage-
ment component covers response times on invalidly
cued trials. We tested whether the presentation of
the CS+ as an invalid cue inhibited target detection
compared to the presentation of the CS– as an
invalid cue. All tests were done using t-tests for
dependent samples.
We found that the presentation of pain signals as
spatial cues affected the engagement component
but not the disengagement component. Responses
were significantly faster on trials with the CS+ as a
valid cue (M = 327 ms, S.D. = 41 ms) compared to
trials with the CS– as a valid cue (M = 336 ms,
SD = 46 ms), t(51) = 2.52, P < 0.05. However,
response times did not differ on trials with the CS+
as an invalid cue (M = 350 ms, S.D. = 47 ms)
compared to trials with the CS– as an invalid cue
(M = 349 ms, S.D. = 49 ms), t(51) = 0.65 ns.
Discussion
The main objective of this study was to investigate
the mechanisms by which pain signals capture at-
tention. We characterized pain signals as stimuli
that signal the occurrence of pain, whereas we
considered stimuli signalling the absence of pain as
safety signals. We used both of these stimuli in an
emotional modification of the exogenous cueing
paradigm and hypothesized that two attentional
components could be identified: (1) Pain signals
may facilitate attentional engagement by acceler-
ating covert orienting to the target location when
compared with safety signals (engagement compo-
nent). (2) Pain signals may inhibit attentional dis-
engagement by slowing covert orienting to targets
in the opposite location when compared with safety
signals (disengagement component).
First, we replicated the cue validity effect: Pre-
senting a valid spatial cue produced covert orient-
ing of attention to the cue location and accelerated
target detection [27]. Notably, we obtained a ro-
bust cue validity effect although we used an equal
number of correctly and incorrectly cued trials. In
original experiments, valid and invalid cues had
occurrence probabilities of 80% and 20% of the
trials, respectively [27]. Second, and of most im-
portance to this study, we observed a differential
modulation of attentional engagement and disen-
gagement by the signal value of the cues: the pain
signal induced stronger attentional engagement
relative to the safety signal, whereas both pain and
38
safety signals were equally difficult to disengage
from.
The differential effect of pain signals on engage-
ment and disengagement is intriguing and needs
further consideration. First, it appears reasonable
that the attentional engagement component in the
exogenous cueing task benefits from threatening
cues due to their greater perceptual salience and
induction of more arousal than neutral cues. How-
ever, a limitation of the present study was that no
physiological measures were included, which could
have clarified the role of arousal. Second, strong
engagement might generally be facilitated by
simple warning signals that allow rapid processing.
Consistent with this view, LeDoux [18] argued that
the simplicity of conditioned stimuli contributes to
the efficiency of recruitment of the brain network
underlying fear-conditioning. Thus, it appears that
the phasic engagement process benefits from the
simple and alerting character of the pain signal.
The biological value of this function may be seen in
the heightened spatial awareness of a potential
threat that needs to be rapidly defended. In con-
trast, disengagement involves a release from an
ongoing tonic process. The pain signal, due to its
short-lived duration and due to the brevity and low
cognitive demand of the electrocutaneous stimulus
that it signals, may have failed to sufficiently inten-
sify this tonic process to render disengagement
impaired. This would explain why attentional dis-
engagement is affected by more complex cognitive
cues such as pictures or words, as has been demon-
strated in a number of recent studies using a cross-
modal cueing paradigm [33,34].
Further support for a dissociation of attentional
engagement and disengagement is provided by neu-
roimaging studies. A cortical network consisting of
frontal, parietal, and cingulate regions has been
described to play a key role in identifying and
shifting attention to salient features of the sensory
environment [11]. By rendering the cue a pain
signal, this network might have been more strongly
recruited, facilitating target detection within the
cued location. In contrast, holding of attention over
prolonged periods of time has been suggested to
rely on sustained activity in the basal ganglia and
prefrontal cortex [3,4]. These regions have been
described to be active during sustained painful
stimulation in humans [21]. More particularly, the
left dorsolateral prefrontal cortex has been sug-
gested to be specifically involved in the disengage-
ment from affective pain processing [22].
Our findings are partly in contrast with previous
studies using an emotional modification of the ex-
ogenous cueing paradigm. One reason for discrep-
ancy may be that most studies used threatening
S. Van Damme et al.
words [15,32] or pictures [15,16,35] as cues, which
involve more complex cognitive and emotional pro-
cessing, influencing disengagement (see above).
Another reason may be that none of these studies
used paradigms with pain stimuli or conditioning.
More similar to our study are exogenous cueing
paradigms that have used a fear-conditioning pro-
cedure with aversive noise [30,31]. However, in
these studies, the exogenous cueing task was not
performed during acquisition as in our study, but
only during extinction. The apparent discontinuity
between acquisition and extinction might have ac-
counted for the contrasting results in these studies
[17].
It can be concluded that attention is more
strongly engaged to a signal of impending than to a
cue signalling the absence of pain. From an evolu-
tionary perspective, one can argue that this process
may subserve the function of locating the potential
risk and adopting protective behaviours before an
injury occurs. However, it may become maladap-
tive in situations of chronic pain where there is no
behavioural escape from pain. In the general con-
text of attention to the threat of pain and the
initiation of avoidance behaviour, it is therefore
necessary to disentangle the diverse components of
attentional shift, engagement and disengagement
[14,15,23,33]. Our study is one of the first that
allows such detailed investigation of the underlying
processes involved in spatial attention to pain sig-
nals. One limitation of the present study is that we
did not use control trials with non-nociceptive
stimuli. Further studies may use a non-painful so-
matosensory stimulus of similar salience [34] in
order to investigate whether our effects are unique
to pain. In future research, it may also be useful to
create experimental paradigms that allow a direct
investigation of the link between spatial attention
to pain signals and avoidance behaviour. Finally,
our modulation of an attentional cueing task by a
fear-conditioning procedure may be combined in
future experiments with neurophysiological mea-
sures (EEG or fMRI) to foster our understanding of
the differential anatomical representation of at-
tentional engagement to and disengagement from
pain.
Acknowledgements
This study was supported by a research grant
(G.0107.00) of the Fund for Scientific Research,
Flanders (Belgium) to Geert Crombez. The authors
wish to thank Jan De Houwer and Bruno Verschuere
for their helpful comments on earlier drafts of the
manuscript, and Valéry Legrain for helping with the
French summary.
Fear-conditioned cues of impending pain facilitate attentional engagement
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