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Attentional disruption is enhanced by the threat of pain
BEHAVIOUR RESEARCH AND THERAPY PERGAMON
Behaviour Research and Therapy 36 (1998) 195-204
Attentional disruption is enhanced by the threat of pain Geert Crombez a'*, Chris Eccleston b, Frank Baeyens a, Paul Eelen a ~Department of Psychology, Katholieke Universiteit te Leuven, Tiensestraat 102, B-3000 Leuven, Belgium bSchool of Social Sciences, University of Bath, Bath, U.K.
Received 28 August 1997
Abstract
Using a primary task paradigm this study investigated whether attentional disruption to a lowintensity electrocutaneous pain stimulus is enhanced by the threat of intense pain. Healthy volunteers (n = 38) performed a tone discrimination task in the presence of two types of distractors (a lowintensity electrocutaneous stimulus and a control stimulus) which they were instructed to ignore. In some trials, tone probes were presented immediately (250 ms) after distractor onset, further on (750 ms) during the distractor, and immediately (250 ms) after distractor offset. In a threat condition half of the participants were informed that a high-intensity painful stimulus would occur. As predicted, those participants who received the threat instructions, displayed a specific larger disruption of task performance immediately after the onset of the low-intensity pain stimulus in comparison with the control group. The results are discussed in terms of hypervigilance to pain. ~) 1998 Elsevier Science Ltd. All rights reserved.
I. Introduction
Evidence is accumulating for the role of attention in controlling and managing pain (Eccleston, 1995b). Attention has also been theorized as the primary mechanism by which nociception accesses awareness and disrupts current activity (Crombez et al., 1996a; Jerome, 1993; Price, 1988; Wall, 1994). The access of nociception into awareness and its fate as pain once it has captured attention is a complex phenomenon requiring an understanding of the perceptual characteristics of the invading stimulus, as well as of the current engagement of the attentional system. In order to study both of these facets we have introduced a primary task paradigm
* Author for correspondence. 0005-7967/98/$19.00 © 1998 Elsevier Science Ltd. All rights reserved.
PII: S0005-7967(97) 10008-0
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that focuses upon the disruption of attentional performance due to pain (Crombez et al., 1994; Eccleston, 1994). In this paradigm, participants are instructed to ignore pain in order to effectively perform an attentionally demanding task. The degradation in task performance, in terms of speed and accuracy, is then taken as a measure of pain interference. Using this paradigm with a chronic pain population, Eccleston (1994) has demonstrated that pain intensity is a principal variable: High intensity chronic pain seems to afford direct access to awareness. Crombez et al. (1997) have found that in healthy volunteers the novelty of an experimental pain stimulus is also a key factor in forcing access and disrupting current attentional engagement. Further, it has been reliably demonstrated that the temporal unpredictability of a nociceptive event produces greater task disruption (Crombez et al., 1994; Dawson et al., 1982). Recently Eccleston et al. (1997) reported that the awareness of bodily information is also an important factor in explaining attentional disruption. In this study only those chronic pain patients who report both high somatic awareness and high-intensity pain show disruption of attention. This effect was discussed in terms of a hypervigilance to somatic sensations (Barsky and Klerman, 1983; Rollman and Lautenbacher, 1993). It was argued that for those who are hypervigilant for bodily information, intense pain quickly and repeatedly accesses awareness. Clinical (Eysenck, 1992) and experimental (Dawson et al., 1982) evidence from the fear literature converge on the view that hypervigilance is a form of attentional bias which normally develops in the presence of threat. It is therefore hypothesized that the attentional interference by pain is, at least in part, a function of its threat value. The following study is designed to investigate whether attentional disruption to a low-intensity electrocutaneous pain stimulus is enhanced by the threat of intense pain. In a mixed design, participants performed an auditory discrimination task in which they report whether tones are high or low in pitch. During this task participants were repeatedly exposed to distractors, i.e. a low-intensity electrocutaneous pain stimulus and a control stimulus. In some trials, a tone was presented at one of three temporal positions: immediately (250 ms) after distractor onset, further on (750 ms) during the distractor and immediately (250 ms) after distractor offset. In a threat manipulation half of the participants were informed that the electrocutaneous stimulus would be occasionally increased in intensity to a high level of pain. The data will be discussed in terms of effects specific to the threat manipulation. It is likely that if the disruption is differential over time, the largest disruption due to threat should occur immediately after onset. First, previous results have indicated that this disruption is most pronounced immediately at the onset of the invading stimulus with this paradigm (Crombez et al., 1996a). Second, Dawson et al. (1982) have found that task interference during a signal for threat is most pronounced immediately after the onset of that signal.
2. Method
2.1. Participants Thirty-eight undergraduate students (22 men and 16 females between the ages of 18 and 20 yr; mean age 18.5 yr) participated in the experiment. The data from one S were excluded from
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statistical analyses because he made more than 20% errors on the discrimination task. All participants gave informed consent and were instructed that they were free to terminate the experiment at anytime.
2.2. Apparatus and material For procedural reasons a level of stimulation was required that was aversive, but tolerable for all participants. A pilot study revealed that an electrocutaneous stimulus of 0.63 mA was judged as tolerable but mildly aversive. Using the Dutch McGill Pain Questionnaire (Vanderiet et al., 1987) the 0.63 mA stimulus was described as pricking, boring, flickering, electric and cutting. The electrocutaneous stimuli were delivered by an A.C. stimulator with an internal frequency of 50 Hz. They had an instantaneous rise and fall time, and a duration of 1500 ms. The stimuli were delivered through two Fukuda standard Ag/AgCI electrodes attached to the left forearm and filled with KY Jelly. The inter-electrode distance was 1 cm. The skin at this site was first abraded with a peeling cream (Brasivol) to reduce the skin resistance. The control stimulus consisted of a picture of a female face (22.5 cm × 18.5 cm; neutral facial expression) which was digitized and presented on a computer screen (1500 ms duration) at a distance of 1 meter. High (1000 Hz) and low (250 Hz) pitch tones (200 ms duration) were emitted by the computer. Participants responded with the right hand by pressing a two-buttoned console.
2.3. Procedure 2.3.1. Preparation phase In order to control for demand characteristics participants were unaware of the true nature of the experiment. They were led to believe that the main interest of the experiment was the putative influence of various distractors on psychophysiological measures. In order to add credence to this cover story, they were led to believe that electrodes would measure the electrodermal activity. To familiarize the participants to the electrocutaneous stimuli, they were given a series of stimuli with increasing intensity. The computer screen displayed an intensity range between 1 and 255 (arbitrary units). On each trial the participants saw that the experimentor typed one of the following arbitrary units: l, 5, 10 and 20, which corresponded to respectively 0.032 mA, 0.16 mA, 0.32 mA and 0.63 mA. These electrocutaneous stimuli were delivered through the same electrodes. Participants were asked to verbally rate the (un)pleasantness of the 0.63 mA stimulus on a bipolar numerical scale with three anchor points (-100: most unpleasant imaginable, 0: neutral and 100: most pleasant imaginable). Thereafter, participants from the Control Group were assured that during the experimental phase the intensity of the electrocutaneous stimulus would always be 20. Participants from the Threat Group received further instructions. They were informed that most of the electrocutaneous stimuli would be of an intensity of 20, but that some highly intense paififul stimuli would also be applied. The timing of these intense painful stimuli would be randomly generated by the computer. Participants of the Threat Group were also led to believe that the computer was responsible for generating individually tailored near tolerance intense pain. In the Threat Group it was further explained that we were interested in the impact of unfamiliar, very intense painful stimuli on the electrodermal activity.
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Next, in order to equate for the acquired familiarity with the electrocutaneous stimulus, the control picture was presented twice. Finally, participants were introduced to the discrimination task and were instructed to respond to the tones as quickly as possible without sacrificing accuracy. Participants practised the task (15 low and 15 high pitch tones) without any distractors (control picture or electrocutaneous stimulus).
2.3.2. Experimental phase For both the Control and the Threat Group the intensity of the electrocutaneous stimulus was always 20 (0.63 mA). The Electrocutaneous Stimulus and the picture of a human face (Control Stimulus) were each presented 16 times for 1.5 sec duration. The Electrocutaneous Stimulus and the Control trials were never presented together. Participants were not informed when distractors would be applied. During some of the Electrocutaneous Stimulus and Control trials, a tone probe was presented at one of three temporal positions, resulting in 6 different types of experimental events. Time 1: During four of the electrocutaneous/control stimulus trials a tone was presented 250 ms after electrocutaneous/control onset. Time 2: During four other electrocutaneous/control trials a tone was presented at 750 ms after electrocutaneous/ control onset. Time 3: During a further four electrocutaneous/control trials a tone was presented 250 ms after the electrocutaneous/control offset. Baseline: 160 tones were presented in the absence of distractors. The reaction time to the tone presented immediately prior to each electrocutaneous/control stimulus was used as baseline. Finally, in order to avoid the electrocutaneous/control stimuli becoming perfect predictors of tones, four electrocutaneous/ control stimuli without tone probes were presented. The distractors were presented in an individually determined random sequence with the restriction that in the first block of the experiment each type of experimental event was presented twice. Of the total of 184 tones presented, half were high in pitch. The inter-stimulus interval for the tones varied between 1200 and 1800 ms. Before the presentation of each distractor, the number of tone alone trials varied between 4 and 6. No more than three consecutive trials consisted of a tone with the same pitch. Reaction times and discrimination errors were recorded by the computer.
2.3.3. Postexperimen tal phase Following the experimental phase participants were required to complete a number of selfreport instruments. Graphic Rating Scales (GRSs) of 10 cm in length were used (Jensen and Karoly, 1992). Participants reported 4 aspects of their experience of the experiment. (1) The intensity of the electrocutaneous stimulus was reported using a verbal GRS [using the adjectives "weak" ( = 0 cm), "moderate", "intense", "enormous" and "unbearable" (--10 cm)]. (2) Whether the intensity of the electrocutaneous stimulus was higher or lower than expected, was reported using a numerical GRS (anchored by + 5 = higher than expected and - 5 = lower than expected). (3) Each participant rated how distracted he/she was by the electrocutaneous stimulus using a numerical GRS (anchored by 0 = not at all distracted and 10 = very strongly distracted). (4) Each subject also rated how distracted he/she was by the control stimulus using the same scale. After completion of the self-report measures participants were informed about the aim of the experiment. In order to control for the possibility of other participants learning about our
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primary interest in task interference, the aim of the experiment was explained without reference to the reaction time measures. Instead the purpose of the experiment was explained while viewing a computer stored profile of electrodermal activity from a previous similar threat experiment (Crombez, 1994). Participants were led to believe that they were viewing their profile of electrodermal activity.
3. Results 3.1. Verbal reports
Before the experiment, participants evaluated the electrocutaneous stimulus as mildly aversive. There was no significant difference between the Threat Group (mean = - 9 . 3 7 ) and the Control Group (mean = - 9 . 1 7 ) (t(35) = - 0 . 8 , NS). Also, after the experimental phase participants from the Threat Group (mean = 1.6) and from the Control Group (mean = 1.56) rated the electrocutaneous stimulus as equally intense (t(35)= 0.08, NS). As expected, the participants of the Threat Group rated the electrocutaneous intensity as lower than expected (mean = - 2.7) than participants of the Control Group (mean = - 1.5) (t(35) = 1.8, P < .05). In comparison with the participants in the Control Group, participants from the Threat Group did not report having been more distracted by the control stimulus (mean of Control Group = 2.64, of Threat Group = 3.04; t(35) = - 0 . 9 7 ) or by the Electrocutaneous Stimulus (mean of Control Group = 3.35, of Threat Group = 3.36; t(35) = - 0.16). 3.2. Behavioural Measures
The overall percentage of errors in the discrimination task was 3.4%. The total number of errors during the Electrocutaneous Stimulus (N = 18) almost equalled the number of errors during the Control Stimulus (N = 19). No difference between the Threat and the Control Group was found (Mann-Whitney test). For the analysis of the reaction times (RTs), the RTs to the tones during the experimental trials (Distractor Tones) and to the tones immediately prior to these events (Baseline Tones) were taken into account. Only 0.5% of the RTs were missing or invalid (RT less than 150 ms or greater than 2000 ms). Valid RTs for each type of experimental event were averaged over the four trials. A 2 × (Group: Control Group and Threat Group) ×2 (Tone Type: Baseline Tone and Distractor Tones) x2 (Distractor Type: Electrocutaneous and Control Stimulus) ×3 (Time of Tone Presentation: Time 1, Time 2, Time 3) analysis of variance was performed on the RT data. The first variable was between-subject. All other variables were within-subject. 3.2.1. General interference effects A significant main effect of Tone Type appeared (F(1,35)= 79.67, M S E = 13691, P < 0.001) which was due to the fact that, averaged over Electrocutaneous and Control Stimuli, the presentation of a Distractor interfered with the discrimination task (Baseline Tone: mean = 430 ms; Distractor Tone: mean = 530 ms). Both the RTs to the tones during the Control Stimulus (t(35)= 6.66 P < 0.001) (mean = 508 ms) and the Electrocutaneous
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Stimulus (t(35) = 6.56 P < 0.001) (mean -- 550 ms) were significantly slower in comparison with the baseline measures (respectively, mean = 431 ms and mean = 429 ms). There was also a significant interaction between Tone Type and Distractor Type (F(1,35) = 4.35, M S E = 12720, P < 0.05). Furthermore, a significant interaction between Distractor Type and Time of Tone presentation (F(2,70)= 6.05, M S E = 6214, P < 0.005) emerged. Despite the fact that the interaction between Tone Type, Distractor Type and Time of Tone presentation was not significant (F(2,70) = 1.96, M S E = 5418, P = < 0.15), analysis of the latter interaction was necessary to interpret the interaction between Distractor Type and Time of Presentation (Bobko, 1986). In order to further interpret this effect, RTs were expressed as change scores from baseline measures. This way interference scores were obtained. Figure 1 displays these interference scores. Pairwise comparisons revealed that the interference during the Electrocutaneous Stimulus was significantly larger than during the Control Stimulus at Time 1 (t(36) = 3.24 P < 0.01) and at Time 2 (t(36) = 1.86 P < 0.05), but not at Time 3 (t(36) = 0.44, NS).
3.3. Threat manipulation effects Of particular interest to our hypothesis was the significant G r o u p × Tone Type × Distractor Type x Time of Tone Presentation interaction (F(2,70) = 3.42, MSE = 5419, P < 0.04). No other effects of the threat manipulation reached statistical significance. In order to further interpret the significant four-way interaction, interference scores were calculated. These interference scores are displayed in Fig. 2. This figure illustrates that the corruption of the primary task was especially large during the onset of the Electrocutaneous Stimulus in the Threat Group. This observation was confirmed by pairwise comparisons using the least
Interference (ms) 150
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Time 3
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Electrical Stimulus
Fig. 1. The interference scores for tone probes that are presented at 250 ms after the electrocutaneous/control stimulus onset (Time 1), at 750 ms after the electrocutaneous/control stimulus onset (Time 2) and at 250 ms after the electrocutaneous/control stimulus offset (Time 3).
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250
-
Interference
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(ms)
]
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15o
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50 2®
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Fig. 2. The interference scores for tone probes that are presented at Time 1, Time 2 and Time 3 as a function of the threat manipulation.
significant difference test (Fisher, 1935). In the Threat Group, the deterioration was significantly larger for the Electrocutaneous Stimulus than for the Control Stimulus at Time 1 (P < 0.001), but not at Time 2 (P = 0.36) or Time 3 (P = 0.30). In the Control Group the deterioration in the RT was not different between the Control Stimulus and the Electrocutaneous Stimulus at Time 1 (P = 0.82), Time 2 (P = 0.23) nor Time 3 (P = 0.47). Comparing the interference scores between the Threat and the Control Group only one pairwise comparison was significant: at Time 1 the deterioration during the Electrocutaneous Stimulus was significantly larger in the Threat Group than in the Control Group (P < 0.01). This was not the case at Time 2 (P = 0.15) and at Time 3 (P = 0.36). During the Control Stimulus there were no significant differences between the Control and Threat Group at Time 1 (P = 0.11), at Time 2 (P = 0.23) nor at Time 3 (P = 0.92).
4. Discussion
The primary focus of this investigation was the putative influence of the threat of intense pain on attention. As predicted, those participants who were threatened, showed pronounced task disruption during the electrocutaneous stimulus. As predicted, the differential disruptive effects of threat could be wholly accounted for by the strong disruption at the beginning of the electrocutaneous stimulus. In other words, disruption was highly pronounced at the onset of the electrocutaneous stimulus, but dissipated quickly afterwards. In the context of threat of imminent pain one might expect a global attentional redeployment. Eysenck (1992) has argued that fear and anxiety are characterized by a general distractibility. In discussing the relationship between affective distress and health complaints, Watson and Pennebaker (1989) have suggested that a nonspecific hypervigilance develops in
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which individuals scan their body for possible threat. In the present study, however, no general effects of threat were found. The threat manipulation did not result in an overall detriment of task performance, or in an enhanced general distractibility. Threat resulted in a specific attentional bias to the electrocutaneous stimulus, only disrupting task performance at Time 1. It seems that in normals attentional disruption in response to the threat of intense pain is specific rather than global. In this study, it is clear that this cannot be due to the stimulus characteristics of the electrocutaneous stimulus alone as those in the control group did not show differential task disruption. One possible explanation for the attentional interference due to threat is via the amplification of the perceptual characteristics of the electrocutaneous stimulus (see Arntz, 1996; Barsky and Klerman 1983; but see Crombez et al., 1996b). However, self-report data show that the threatened group and the control group judged the electrocutaneous stimulus to be of a similar intensity. A more plausible explanations for these effects stresses not the perceptual components of the invading stimulus but the appraisal, or the meaning of electrocutaneous stimulus. A number of authors have argued for the importance of such appraisal processes. Ohman (1979; Ohman, 1988; Hermans et al., 1994) stemming from a conditioning background of psychology, argues that all incoming stimuli are automatically appraised for their possible threat value. Cognitive psychologists interested in motivation for action have stressed the importance of attentional priorities and the appraisal of novel information in line with these priorities (Norman and Shallice, 1986). We propose that the threat of intense pain primes the attentional system for the interruption of the primary task. When an electrocutaneous stimulus is delivered, a new priority is imposed and attention is switched to the object of threat for further investigation. When the electrocutaneous stimulus is appraised as non-threatening, attention returns to the primary task and further disruption is avoided. If the object of threat is not selected via somatic amplification, why then is it selected? We suggest that the object of threat is selected because it urges to (re)act/escape. This view implies a close link between attentional interference and the disposition to (re)act. Although evidence is lacking in the pain literature, this view is congruent with Lang's affective-motivational theory of emotions (Lang, 1995; Lang et al., 1992). In this theory threatening stimuli prime a primitive behavioral repertoire of avoidance and escape. Of importance for our argument are the recent findings (1) that also non-painful affective stimuli interfere with task performance, (2) that the task interference is most marked early after stimulus onset and (3) that variations in the task interference are wholly accounted for by variations in arousal (Bradley et al., 1996a; Bradley et al., 1996b). According to Lang's theory, attentional interference is then owing to a strong and primitive disposition to act. In the context of pain, it may be hypothesized that attentional interference is strongly related to the urge to escape from pain (see Crombez et al., 1997). In line with this reasoning, is the clinical finding that chronic low back pain patients who try to avoid back straining activities do not only report high fear of pain and of (re)injury, but also being very alert for back sensations (Crombez et al., in press). An unexpected finding in our study was the divergence between the behavioral and the selfreport measure of attentional interference. Indeed, although the task interference during the electrocutaneous stimulus was larger in the threat group than in the control group, the threat group did not report being more distracted by the electrocutaneous stimulus. As yet we do not have a full explanation for this divergence. One reason, we suspect, is that the self-report
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measure is less sensitive than the behavioral measure. Error variance in the self-reports may have been high because participants had to report their experience only after an extended series of electrocutaneous stimuli, and because it was left unclear which out of the 16 electrocutaneous stimuli had to be evaluated. Also, the self-report measure was a global measure and did not allow to assess the differential pattern of attentional interference during the electrocutaneous stimuli. Despite this remark, it is noteworthy that in this study a significant correlation between the reported distractibility and the task interference during the electrocutaneous stimulus (r(37)= 0.41, P < 0.01) was obtained. This finding supports the construct validity of our behavioral measure of attentional interference. Adopting a functional view of attention focuses research interest upon the meaning of pain and the context in which it occurs. In future studies, the primary task paradigm will need to be adapted in order to study the malleability of attentional switching as a function of task priority (Eccleston, 1995b). Second, individual differences in attentional priorities will need to be accounted for. For example, the attentional bias due to threat may be a function of catastrophic thinking about pain (e.g. Heyneman et al., 1990) or negative affectivity (e.g. Eysenck 1992). Using an experimental model of pain with painfree humans allows for more accurate manipulation of pain, threat and attention. However, although there are similarities between experimental pain and clinical pain such as their limited escape potential, future research will need to address the complex interplay between attention and the range of cognitive functions inevitably triggered by the threat of pain. Rollman and Lautenbacher (1993), for example, have suggested that attentional biasing in the form of chronic hypervigilance may help us understand disability associated with chronic musculoskeletal pain disorders such as fibromyalgia (see also Crombez et al., in press). Primary task paradigms may offer one method to experimentally investigate the attentional nature of hypervigilance.
Acknowledgements This study was supported by the Academic Research Collaboration Programme between the Fund for Scientific Research (Flanders), Belgium, and the British Council. Geert Crombez and Frank Baeyens are postdoctoral researchers for the Fund for Scientific Research (Flanders) Belgium.
References Allport, D. A. (1989). Visual attention. In M. I. Posner (Eds.), Foundations of cognitive science (pp. 631-682). Bradford Press, London. Arntz, A. (1996). Why do people tend to overpredict pain?On the asymmetries between underpredictions and overpredictions of pain. Bchaviour Research and Therapy, 34, 545-554. Barsky, A. J., & Klerman, G. L. (1983). Hypochrondriasis, bodily complaints, and somatic styles. American Journal q['P.~vchiatry, 140, 273-283. Bradley, M. M., Cuthbert, B. N., & Lang, P. J. (1996a). Picture media and emotion: Effects of a sustained affective context. Psychophysiology. 33, 662-770. Bradley, M., Drobes, D., & Lang, P. J. (1996b). A probe for all reasons: Reflex and RT measures in perception. Psychophysiology, 33, $25. Bobko, P. (1986). A solution to some dilemmas when testing hypotheses about ordinal interactions. Journal c~]'Applied Psychology. 71, 323 326.
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Crombez, G. (1994). Pijnmodulatie door anticipatie [pain modulation through anticipation]? Unpublished Ph.D. thesis, Leuven, Belgium. Crombez, G., Baeyens, F., & Eelen, P. (1994). Sensory and temporal information about impending pain: The influence of predictability on pain. Behaviour Research and Therapy, 32, 611-622. Crombez, G., Baeyens, F., Vansteenwegen, D. & Eelen, P. (1997). Startle intensification during painful heat. European Journal of Pain, 1, 87-94. Crombez, G., Eccleston, C., Baeyens, F., & Eelen, P. (1996a). The disruptive nature of pain: an experimental investigation. Behaviour Research and Therapy, 34, 911-918. Crombez, G., Eccleston, C., Baeyens, F., & Eelen, P. (1997). Habituation and the interference of pain with task performance. Pain, 70, 149-154. Crombez, G., Vervaet, L., Lysens, R., Eelen, P., & Baeyens, F. (1996b). Do pain expectancies cause pain in chronic low back patients?A clinical investigation. Behaviour Research and Therapy, 34, 919-925. Crombez, G., Vervaet, L., Lysens, R., Baeyens, F. & Eelen, P. (in press). Avoidance and confrontation of painful, back straining movements in chronic back pain patients. Behavior ModO%ation. Dawson, M. E., Schell, A. M., Beers, J. R., & Kelly, A. (1982). Allocation of cognitive processing capacity during human autonomic classical conditioning. Journal of Experimental Psychology, 111. 273 294. Eccleston, C. (1994). Chronic pain and attention: A cognitive approach. British Journal Of Clinical Psychology, 33, 535-547. Eccleston, C. (1995a). Chronic pain and distraction: An experimental investigation into the role of sustained and shifting attention in the processing of chronic persistent pain. Behaviour Research and Therapy. 33, 391-405. Eccleston, C. (1995b). The attentional control of pain: methodological and theoretical concerns. Pain, 63, 3-10. Eccleston, C., Crombez, G., Aldrich, S. & Stannard, C. (1997). The role of somatic awareness in the attentional interference caused by chronic pain. Pain, 72, 209-215. Eysenck, M. W. (1992). Anxiety." the cognitive perspective. Lawrence Erlabum Associates, Hillsdale. pp. 195. Fisher, R. A. (1935). The design of experiments. Oliver & Boyd, Edinburgh, Scotland. Hermans, D., De Houwer, J., & Eelen, P. (1994). The affective priming effect: automatic activation of evaluative information in memory. Cognition and Emotion, 8, 515-533. Heyneman, N., Fremouw, W. J., Gano, D., Kirkland, F., & Heiden, L. (1990). Individual differences and the effectiveness of different coping strategies for pain. Cognitive Therapy and Research, 14, 63-77. Jensen, M. P. & Karoly, P. (1992). Self-report scales and procedures for assessing pain in adults. In Turk DC & Melzack R (Eds.), Handbook of pain assessment (pp. 135-151). The Guildford Press, New York. Jerome, J. (1993). Transmission or transformation?Information processing theory of chronic human pain. American Pain Society, 2, 160-171. Lang, P. J. (1995). The emotion probe: Studies of motivation and attention. American Psychologist, 50, 372-385. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1992). A motivational.analysis of emotion: Reflex-cortex connections. Psychological Science, 3, 44-49. Norman, D. A. & Shallice, T. (1986). Attention to action: Willed and automatic control of behaviour. In Davidson R. J., Schwartz G. E. & Shapiro D. (Eds.), Consciousness and self regulation. Vol. 4. Plenum Press, New York. pp. 1-18. Ohman, A. (1979). The orienting response, attention and learning: an information-processing perspective. In Kimmel HD, Van Olst EH & Orlebeke JF (Eds.), The orienting reflex in humans (pp. 443-471). Lawrence Erlbaum Associates, Hillsdale. Ohman, A. (1988). Preattentive processes in the generation of emotions. In Hamilton V, Bower GH & Frijda N (Eds.), Cognitive perspectives on emotion and motivation (pp. 127 143). Kluwer Academic Publishers, Dordrecht. Price, D. D. 1988. Psychological and neural mechanisms of pain. Raven press, New York. pp. 241.. Rollman, G. B. & Lautenbacher, S. (1993). Hypervigilance effects in fibromyalgia: pain experience and pain perception. In Voeroy H & Merskey H (Eds.), Progress in Fibromyalgia and Myofascial Pain. Eslevier. Wall, P. D. (1994). Introduction to the edition after this one. tn Wall P. D. & Melzack R. (Eds.), The textbook of pain. 3rd edn. Churchill Livingstone, Edinburgh. pp. I 7. Watson, D., & Pennebaker, J. W. (1989). Health complaints, stress, and distress: exploring the central role of negative affectivity. Psychological Review, 96, 234-254.
Behaviour Research and Therapy 36 (1998) 195-204
Attentional disruption is enhanced by the threat of pain Geert Crombez a'*, Chris Eccleston b, Frank Baeyens a, Paul Eelen a ~Department of Psychology, Katholieke Universiteit te Leuven, Tiensestraat 102, B-3000 Leuven, Belgium bSchool of Social Sciences, University of Bath, Bath, U.K.
Received 28 August 1997
Abstract
Using a primary task paradigm this study investigated whether attentional disruption to a lowintensity electrocutaneous pain stimulus is enhanced by the threat of intense pain. Healthy volunteers (n = 38) performed a tone discrimination task in the presence of two types of distractors (a lowintensity electrocutaneous stimulus and a control stimulus) which they were instructed to ignore. In some trials, tone probes were presented immediately (250 ms) after distractor onset, further on (750 ms) during the distractor, and immediately (250 ms) after distractor offset. In a threat condition half of the participants were informed that a high-intensity painful stimulus would occur. As predicted, those participants who received the threat instructions, displayed a specific larger disruption of task performance immediately after the onset of the low-intensity pain stimulus in comparison with the control group. The results are discussed in terms of hypervigilance to pain. ~) 1998 Elsevier Science Ltd. All rights reserved.
I. Introduction
Evidence is accumulating for the role of attention in controlling and managing pain (Eccleston, 1995b). Attention has also been theorized as the primary mechanism by which nociception accesses awareness and disrupts current activity (Crombez et al., 1996a; Jerome, 1993; Price, 1988; Wall, 1994). The access of nociception into awareness and its fate as pain once it has captured attention is a complex phenomenon requiring an understanding of the perceptual characteristics of the invading stimulus, as well as of the current engagement of the attentional system. In order to study both of these facets we have introduced a primary task paradigm
* Author for correspondence. 0005-7967/98/$19.00 © 1998 Elsevier Science Ltd. All rights reserved.
PII: S0005-7967(97) 10008-0
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that focuses upon the disruption of attentional performance due to pain (Crombez et al., 1994; Eccleston, 1994). In this paradigm, participants are instructed to ignore pain in order to effectively perform an attentionally demanding task. The degradation in task performance, in terms of speed and accuracy, is then taken as a measure of pain interference. Using this paradigm with a chronic pain population, Eccleston (1994) has demonstrated that pain intensity is a principal variable: High intensity chronic pain seems to afford direct access to awareness. Crombez et al. (1997) have found that in healthy volunteers the novelty of an experimental pain stimulus is also a key factor in forcing access and disrupting current attentional engagement. Further, it has been reliably demonstrated that the temporal unpredictability of a nociceptive event produces greater task disruption (Crombez et al., 1994; Dawson et al., 1982). Recently Eccleston et al. (1997) reported that the awareness of bodily information is also an important factor in explaining attentional disruption. In this study only those chronic pain patients who report both high somatic awareness and high-intensity pain show disruption of attention. This effect was discussed in terms of a hypervigilance to somatic sensations (Barsky and Klerman, 1983; Rollman and Lautenbacher, 1993). It was argued that for those who are hypervigilant for bodily information, intense pain quickly and repeatedly accesses awareness. Clinical (Eysenck, 1992) and experimental (Dawson et al., 1982) evidence from the fear literature converge on the view that hypervigilance is a form of attentional bias which normally develops in the presence of threat. It is therefore hypothesized that the attentional interference by pain is, at least in part, a function of its threat value. The following study is designed to investigate whether attentional disruption to a low-intensity electrocutaneous pain stimulus is enhanced by the threat of intense pain. In a mixed design, participants performed an auditory discrimination task in which they report whether tones are high or low in pitch. During this task participants were repeatedly exposed to distractors, i.e. a low-intensity electrocutaneous pain stimulus and a control stimulus. In some trials, a tone was presented at one of three temporal positions: immediately (250 ms) after distractor onset, further on (750 ms) during the distractor and immediately (250 ms) after distractor offset. In a threat manipulation half of the participants were informed that the electrocutaneous stimulus would be occasionally increased in intensity to a high level of pain. The data will be discussed in terms of effects specific to the threat manipulation. It is likely that if the disruption is differential over time, the largest disruption due to threat should occur immediately after onset. First, previous results have indicated that this disruption is most pronounced immediately at the onset of the invading stimulus with this paradigm (Crombez et al., 1996a). Second, Dawson et al. (1982) have found that task interference during a signal for threat is most pronounced immediately after the onset of that signal.
2. Method
2.1. Participants Thirty-eight undergraduate students (22 men and 16 females between the ages of 18 and 20 yr; mean age 18.5 yr) participated in the experiment. The data from one S were excluded from
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statistical analyses because he made more than 20% errors on the discrimination task. All participants gave informed consent and were instructed that they were free to terminate the experiment at anytime.
2.2. Apparatus and material For procedural reasons a level of stimulation was required that was aversive, but tolerable for all participants. A pilot study revealed that an electrocutaneous stimulus of 0.63 mA was judged as tolerable but mildly aversive. Using the Dutch McGill Pain Questionnaire (Vanderiet et al., 1987) the 0.63 mA stimulus was described as pricking, boring, flickering, electric and cutting. The electrocutaneous stimuli were delivered by an A.C. stimulator with an internal frequency of 50 Hz. They had an instantaneous rise and fall time, and a duration of 1500 ms. The stimuli were delivered through two Fukuda standard Ag/AgCI electrodes attached to the left forearm and filled with KY Jelly. The inter-electrode distance was 1 cm. The skin at this site was first abraded with a peeling cream (Brasivol) to reduce the skin resistance. The control stimulus consisted of a picture of a female face (22.5 cm × 18.5 cm; neutral facial expression) which was digitized and presented on a computer screen (1500 ms duration) at a distance of 1 meter. High (1000 Hz) and low (250 Hz) pitch tones (200 ms duration) were emitted by the computer. Participants responded with the right hand by pressing a two-buttoned console.
2.3. Procedure 2.3.1. Preparation phase In order to control for demand characteristics participants were unaware of the true nature of the experiment. They were led to believe that the main interest of the experiment was the putative influence of various distractors on psychophysiological measures. In order to add credence to this cover story, they were led to believe that electrodes would measure the electrodermal activity. To familiarize the participants to the electrocutaneous stimuli, they were given a series of stimuli with increasing intensity. The computer screen displayed an intensity range between 1 and 255 (arbitrary units). On each trial the participants saw that the experimentor typed one of the following arbitrary units: l, 5, 10 and 20, which corresponded to respectively 0.032 mA, 0.16 mA, 0.32 mA and 0.63 mA. These electrocutaneous stimuli were delivered through the same electrodes. Participants were asked to verbally rate the (un)pleasantness of the 0.63 mA stimulus on a bipolar numerical scale with three anchor points (-100: most unpleasant imaginable, 0: neutral and 100: most pleasant imaginable). Thereafter, participants from the Control Group were assured that during the experimental phase the intensity of the electrocutaneous stimulus would always be 20. Participants from the Threat Group received further instructions. They were informed that most of the electrocutaneous stimuli would be of an intensity of 20, but that some highly intense paififul stimuli would also be applied. The timing of these intense painful stimuli would be randomly generated by the computer. Participants of the Threat Group were also led to believe that the computer was responsible for generating individually tailored near tolerance intense pain. In the Threat Group it was further explained that we were interested in the impact of unfamiliar, very intense painful stimuli on the electrodermal activity.
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Next, in order to equate for the acquired familiarity with the electrocutaneous stimulus, the control picture was presented twice. Finally, participants were introduced to the discrimination task and were instructed to respond to the tones as quickly as possible without sacrificing accuracy. Participants practised the task (15 low and 15 high pitch tones) without any distractors (control picture or electrocutaneous stimulus).
2.3.2. Experimental phase For both the Control and the Threat Group the intensity of the electrocutaneous stimulus was always 20 (0.63 mA). The Electrocutaneous Stimulus and the picture of a human face (Control Stimulus) were each presented 16 times for 1.5 sec duration. The Electrocutaneous Stimulus and the Control trials were never presented together. Participants were not informed when distractors would be applied. During some of the Electrocutaneous Stimulus and Control trials, a tone probe was presented at one of three temporal positions, resulting in 6 different types of experimental events. Time 1: During four of the electrocutaneous/control stimulus trials a tone was presented 250 ms after electrocutaneous/control onset. Time 2: During four other electrocutaneous/control trials a tone was presented at 750 ms after electrocutaneous/ control onset. Time 3: During a further four electrocutaneous/control trials a tone was presented 250 ms after the electrocutaneous/control offset. Baseline: 160 tones were presented in the absence of distractors. The reaction time to the tone presented immediately prior to each electrocutaneous/control stimulus was used as baseline. Finally, in order to avoid the electrocutaneous/control stimuli becoming perfect predictors of tones, four electrocutaneous/ control stimuli without tone probes were presented. The distractors were presented in an individually determined random sequence with the restriction that in the first block of the experiment each type of experimental event was presented twice. Of the total of 184 tones presented, half were high in pitch. The inter-stimulus interval for the tones varied between 1200 and 1800 ms. Before the presentation of each distractor, the number of tone alone trials varied between 4 and 6. No more than three consecutive trials consisted of a tone with the same pitch. Reaction times and discrimination errors were recorded by the computer.
2.3.3. Postexperimen tal phase Following the experimental phase participants were required to complete a number of selfreport instruments. Graphic Rating Scales (GRSs) of 10 cm in length were used (Jensen and Karoly, 1992). Participants reported 4 aspects of their experience of the experiment. (1) The intensity of the electrocutaneous stimulus was reported using a verbal GRS [using the adjectives "weak" ( = 0 cm), "moderate", "intense", "enormous" and "unbearable" (--10 cm)]. (2) Whether the intensity of the electrocutaneous stimulus was higher or lower than expected, was reported using a numerical GRS (anchored by + 5 = higher than expected and - 5 = lower than expected). (3) Each participant rated how distracted he/she was by the electrocutaneous stimulus using a numerical GRS (anchored by 0 = not at all distracted and 10 = very strongly distracted). (4) Each subject also rated how distracted he/she was by the control stimulus using the same scale. After completion of the self-report measures participants were informed about the aim of the experiment. In order to control for the possibility of other participants learning about our
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primary interest in task interference, the aim of the experiment was explained without reference to the reaction time measures. Instead the purpose of the experiment was explained while viewing a computer stored profile of electrodermal activity from a previous similar threat experiment (Crombez, 1994). Participants were led to believe that they were viewing their profile of electrodermal activity.
3. Results 3.1. Verbal reports
Before the experiment, participants evaluated the electrocutaneous stimulus as mildly aversive. There was no significant difference between the Threat Group (mean = - 9 . 3 7 ) and the Control Group (mean = - 9 . 1 7 ) (t(35) = - 0 . 8 , NS). Also, after the experimental phase participants from the Threat Group (mean = 1.6) and from the Control Group (mean = 1.56) rated the electrocutaneous stimulus as equally intense (t(35)= 0.08, NS). As expected, the participants of the Threat Group rated the electrocutaneous intensity as lower than expected (mean = - 2.7) than participants of the Control Group (mean = - 1.5) (t(35) = 1.8, P < .05). In comparison with the participants in the Control Group, participants from the Threat Group did not report having been more distracted by the control stimulus (mean of Control Group = 2.64, of Threat Group = 3.04; t(35) = - 0 . 9 7 ) or by the Electrocutaneous Stimulus (mean of Control Group = 3.35, of Threat Group = 3.36; t(35) = - 0.16). 3.2. Behavioural Measures
The overall percentage of errors in the discrimination task was 3.4%. The total number of errors during the Electrocutaneous Stimulus (N = 18) almost equalled the number of errors during the Control Stimulus (N = 19). No difference between the Threat and the Control Group was found (Mann-Whitney test). For the analysis of the reaction times (RTs), the RTs to the tones during the experimental trials (Distractor Tones) and to the tones immediately prior to these events (Baseline Tones) were taken into account. Only 0.5% of the RTs were missing or invalid (RT less than 150 ms or greater than 2000 ms). Valid RTs for each type of experimental event were averaged over the four trials. A 2 × (Group: Control Group and Threat Group) ×2 (Tone Type: Baseline Tone and Distractor Tones) x2 (Distractor Type: Electrocutaneous and Control Stimulus) ×3 (Time of Tone Presentation: Time 1, Time 2, Time 3) analysis of variance was performed on the RT data. The first variable was between-subject. All other variables were within-subject. 3.2.1. General interference effects A significant main effect of Tone Type appeared (F(1,35)= 79.67, M S E = 13691, P < 0.001) which was due to the fact that, averaged over Electrocutaneous and Control Stimuli, the presentation of a Distractor interfered with the discrimination task (Baseline Tone: mean = 430 ms; Distractor Tone: mean = 530 ms). Both the RTs to the tones during the Control Stimulus (t(35)= 6.66 P < 0.001) (mean = 508 ms) and the Electrocutaneous
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Stimulus (t(35) = 6.56 P < 0.001) (mean -- 550 ms) were significantly slower in comparison with the baseline measures (respectively, mean = 431 ms and mean = 429 ms). There was also a significant interaction between Tone Type and Distractor Type (F(1,35) = 4.35, M S E = 12720, P < 0.05). Furthermore, a significant interaction between Distractor Type and Time of Tone presentation (F(2,70)= 6.05, M S E = 6214, P < 0.005) emerged. Despite the fact that the interaction between Tone Type, Distractor Type and Time of Tone presentation was not significant (F(2,70) = 1.96, M S E = 5418, P = < 0.15), analysis of the latter interaction was necessary to interpret the interaction between Distractor Type and Time of Presentation (Bobko, 1986). In order to further interpret this effect, RTs were expressed as change scores from baseline measures. This way interference scores were obtained. Figure 1 displays these interference scores. Pairwise comparisons revealed that the interference during the Electrocutaneous Stimulus was significantly larger than during the Control Stimulus at Time 1 (t(36) = 3.24 P < 0.01) and at Time 2 (t(36) = 1.86 P < 0.05), but not at Time 3 (t(36) = 0.44, NS).
3.3. Threat manipulation effects Of particular interest to our hypothesis was the significant G r o u p × Tone Type × Distractor Type x Time of Tone Presentation interaction (F(2,70) = 3.42, MSE = 5419, P < 0.04). No other effects of the threat manipulation reached statistical significance. In order to further interpret the significant four-way interaction, interference scores were calculated. These interference scores are displayed in Fig. 2. This figure illustrates that the corruption of the primary task was especially large during the onset of the Electrocutaneous Stimulus in the Threat Group. This observation was confirmed by pairwise comparisons using the least
Interference (ms) 150
100
50
Time 1
Time 3
Time 2
Time of Tone Presentation I
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Electrical Stimulus
Fig. 1. The interference scores for tone probes that are presented at 250 ms after the electrocutaneous/control stimulus onset (Time 1), at 750 ms after the electrocutaneous/control stimulus onset (Time 2) and at 250 ms after the electrocutaneous/control stimulus offset (Time 3).
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250
-
Interference
201
(ms)
]
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15o
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50 2®
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i
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Fig. 2. The interference scores for tone probes that are presented at Time 1, Time 2 and Time 3 as a function of the threat manipulation.
significant difference test (Fisher, 1935). In the Threat Group, the deterioration was significantly larger for the Electrocutaneous Stimulus than for the Control Stimulus at Time 1 (P < 0.001), but not at Time 2 (P = 0.36) or Time 3 (P = 0.30). In the Control Group the deterioration in the RT was not different between the Control Stimulus and the Electrocutaneous Stimulus at Time 1 (P = 0.82), Time 2 (P = 0.23) nor Time 3 (P = 0.47). Comparing the interference scores between the Threat and the Control Group only one pairwise comparison was significant: at Time 1 the deterioration during the Electrocutaneous Stimulus was significantly larger in the Threat Group than in the Control Group (P < 0.01). This was not the case at Time 2 (P = 0.15) and at Time 3 (P = 0.36). During the Control Stimulus there were no significant differences between the Control and Threat Group at Time 1 (P = 0.11), at Time 2 (P = 0.23) nor at Time 3 (P = 0.92).
4. Discussion
The primary focus of this investigation was the putative influence of the threat of intense pain on attention. As predicted, those participants who were threatened, showed pronounced task disruption during the electrocutaneous stimulus. As predicted, the differential disruptive effects of threat could be wholly accounted for by the strong disruption at the beginning of the electrocutaneous stimulus. In other words, disruption was highly pronounced at the onset of the electrocutaneous stimulus, but dissipated quickly afterwards. In the context of threat of imminent pain one might expect a global attentional redeployment. Eysenck (1992) has argued that fear and anxiety are characterized by a general distractibility. In discussing the relationship between affective distress and health complaints, Watson and Pennebaker (1989) have suggested that a nonspecific hypervigilance develops in
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which individuals scan their body for possible threat. In the present study, however, no general effects of threat were found. The threat manipulation did not result in an overall detriment of task performance, or in an enhanced general distractibility. Threat resulted in a specific attentional bias to the electrocutaneous stimulus, only disrupting task performance at Time 1. It seems that in normals attentional disruption in response to the threat of intense pain is specific rather than global. In this study, it is clear that this cannot be due to the stimulus characteristics of the electrocutaneous stimulus alone as those in the control group did not show differential task disruption. One possible explanation for the attentional interference due to threat is via the amplification of the perceptual characteristics of the electrocutaneous stimulus (see Arntz, 1996; Barsky and Klerman 1983; but see Crombez et al., 1996b). However, self-report data show that the threatened group and the control group judged the electrocutaneous stimulus to be of a similar intensity. A more plausible explanations for these effects stresses not the perceptual components of the invading stimulus but the appraisal, or the meaning of electrocutaneous stimulus. A number of authors have argued for the importance of such appraisal processes. Ohman (1979; Ohman, 1988; Hermans et al., 1994) stemming from a conditioning background of psychology, argues that all incoming stimuli are automatically appraised for their possible threat value. Cognitive psychologists interested in motivation for action have stressed the importance of attentional priorities and the appraisal of novel information in line with these priorities (Norman and Shallice, 1986). We propose that the threat of intense pain primes the attentional system for the interruption of the primary task. When an electrocutaneous stimulus is delivered, a new priority is imposed and attention is switched to the object of threat for further investigation. When the electrocutaneous stimulus is appraised as non-threatening, attention returns to the primary task and further disruption is avoided. If the object of threat is not selected via somatic amplification, why then is it selected? We suggest that the object of threat is selected because it urges to (re)act/escape. This view implies a close link between attentional interference and the disposition to (re)act. Although evidence is lacking in the pain literature, this view is congruent with Lang's affective-motivational theory of emotions (Lang, 1995; Lang et al., 1992). In this theory threatening stimuli prime a primitive behavioral repertoire of avoidance and escape. Of importance for our argument are the recent findings (1) that also non-painful affective stimuli interfere with task performance, (2) that the task interference is most marked early after stimulus onset and (3) that variations in the task interference are wholly accounted for by variations in arousal (Bradley et al., 1996a; Bradley et al., 1996b). According to Lang's theory, attentional interference is then owing to a strong and primitive disposition to act. In the context of pain, it may be hypothesized that attentional interference is strongly related to the urge to escape from pain (see Crombez et al., 1997). In line with this reasoning, is the clinical finding that chronic low back pain patients who try to avoid back straining activities do not only report high fear of pain and of (re)injury, but also being very alert for back sensations (Crombez et al., in press). An unexpected finding in our study was the divergence between the behavioral and the selfreport measure of attentional interference. Indeed, although the task interference during the electrocutaneous stimulus was larger in the threat group than in the control group, the threat group did not report being more distracted by the electrocutaneous stimulus. As yet we do not have a full explanation for this divergence. One reason, we suspect, is that the self-report
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measure is less sensitive than the behavioral measure. Error variance in the self-reports may have been high because participants had to report their experience only after an extended series of electrocutaneous stimuli, and because it was left unclear which out of the 16 electrocutaneous stimuli had to be evaluated. Also, the self-report measure was a global measure and did not allow to assess the differential pattern of attentional interference during the electrocutaneous stimuli. Despite this remark, it is noteworthy that in this study a significant correlation between the reported distractibility and the task interference during the electrocutaneous stimulus (r(37)= 0.41, P < 0.01) was obtained. This finding supports the construct validity of our behavioral measure of attentional interference. Adopting a functional view of attention focuses research interest upon the meaning of pain and the context in which it occurs. In future studies, the primary task paradigm will need to be adapted in order to study the malleability of attentional switching as a function of task priority (Eccleston, 1995b). Second, individual differences in attentional priorities will need to be accounted for. For example, the attentional bias due to threat may be a function of catastrophic thinking about pain (e.g. Heyneman et al., 1990) or negative affectivity (e.g. Eysenck 1992). Using an experimental model of pain with painfree humans allows for more accurate manipulation of pain, threat and attention. However, although there are similarities between experimental pain and clinical pain such as their limited escape potential, future research will need to address the complex interplay between attention and the range of cognitive functions inevitably triggered by the threat of pain. Rollman and Lautenbacher (1993), for example, have suggested that attentional biasing in the form of chronic hypervigilance may help us understand disability associated with chronic musculoskeletal pain disorders such as fibromyalgia (see also Crombez et al., in press). Primary task paradigms may offer one method to experimentally investigate the attentional nature of hypervigilance.
Acknowledgements This study was supported by the Academic Research Collaboration Programme between the Fund for Scientific Research (Flanders), Belgium, and the British Council. Geert Crombez and Frank Baeyens are postdoctoral researchers for the Fund for Scientific Research (Flanders) Belgium.
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