ORIGINAL ARTICLE

The effect of pain on involuntary and voluntary capture of attention S.J. Troche1,2, M.E. Houlihan3,4,5, J.F. Connolly4,6, B.D. Dick4,7, P.J. McGrath4,5, G.A. Finley4,5, G. Stroink4 1 2 3 4 5 6 7

Department of Psychology, University of Bern, Switzerland Center for Cognition, Learning, and Memory, University of Bern, Switzerland Department of Psychology, St. Thomas University, Fredericton, New Brunswick, Canada Department of Psychology, Dalhousie University, Halifax, Nova Scotia, Canada The Centre for Pediatric Pain Research, IWK Health Centre, Halifax, Nova Scotia, Canada Department of Linguistics & Languages, McMaster University, Hamilton, Ontario, Canada Department of Anesthesiology & Pain Medicine, University of Alberta, Edmonton, Alberta, Canada

Correspondence Stefan Troche E-mail: [email protected] Funding sources Dr. Houlihan was supported by an IWK Health Centre Research Grant. Dr. Connolly was supported by the Natural Sciences and Engineering Research Council (NSERC) and the Canadian Institutes for Health Research (CIHR). Dr. Dick was supported by an IWK Health Centre Graduate Student Research Scholarship. Dr. Finley is a Dalhousie University Senior Clinical Research Scholar. Dr. McGrath was supported by a Distinguished Scientist Award and research grant from the Canadian Institutes of Health. Dr. Stroink was supported by the Natural Sciences and Engineering Research Council (NSERC). Conflicts of interest None declared. Accepted for publication 22 May 2014 doi:10.1002/ejp.553

Abstract Background: There is converging evidence for the notion that pain affects a broad range of attentional domains. This study investigated the influence of pain on the involuntary capture of attention as indexed by the P3a component in the event-related potential derived from the electroencephalogram. Methods: Participants performed in an auditory oddball task in a pain-free and a pain condition during which they submerged a hand in cold water. Novel, infrequent and unexpected auditory stimuli were presented randomly in a series of frequent standard and infrequent target tones. P3a and P3b amplitudes were observed to novel, unexpected and target-related stimuli, respectively. Results: Both electrophysiological components were characterized by reduced amplitudes in the pain compared with the pain-free condition. Hit rate and reaction time to target stimuli did not differ between the two conditions presumably because the experimental task was not difficult enough to exceed attentional capacities under pain conditions. Conclusions: These results indicate that voluntary attention serving the maintenance and control of ongoing information processing (reflected by the P3b amplitude) is impaired by pain. In addition, the involuntary capture of attention and orientation to novel, unexpected information (measured by the P3a) is also impaired by pain. Thus, neurophysiological measures examined in this study support the theoretical positions proposing that pain can reduce attentional processing capacity. These findings have potentially important implications at the theoretical level for our understanding of the interplay of pain and cognition, and at the therapeutic level for the clinical treatment of individuals experiencing ongoing pain.

1. Introduction Eccleston (1994) proposed that pain demands attentional resources by interrupting current activities to avoid further harm. Consistent with this assumption, attentional deficits were reported in patients suffering 350 Eur J Pain 19 (2015) 350--357

from chronic pain (Moriarty et al., 2011) and in healthy individuals exposed to a painful procedure (Buhle and Wager, 2010). Some studies, however, failed to observe this effect (Seminowicz et al., 2004; Pud and Sapir, 2006; Seminowicz and Davis, 2007; Coen et al., 2008). These inconsistencies were © 2014 European Pain Federation - EFICâ

Effect of pain on attention

What’s already known about this topic? • Pain affects a broad range of attentional domains. • Most investigated domains refer to voluntary aspects of attention. What does this study add? • Involuntary capture of attention as indexed by the P3a in the event-related potential derived from the electroencephalogram was also reduced under pain conditions. • The results emphasize the benefit of concurrently investigating behavioural and electrophysiological measures to detect accurately overt and covert effects of pain on cognitive functioning.

explained by differences in the attentional demands of different experimental tasks (Buhle and Wager, 2010). Accordingly, cognitive tasks must tax attentional resources so much that the capacity limit is exceeded when pain simultaneously demands these resources. Furthermore, because behavioural measures of attention are sensitive to strategy changes (e.g., speed– accuracy tradeoffs) performance deficits due to pain may be masked (Houlihan et al., 2004). An alternative approach to the effect of pain on attention, rather unaffected by strategies, is to employ event-related potential (ERP) methods, particularly the P300 component which is closely related to the allocation of attentional resources (Johnson, 1986; Polich, 2007, 2012). A common differentiation associated with P300 refers to P3a and P3b (Polich and Criado, 2006). P3b reflects inhibitory attentional processes facilitating consolidation of a target’s mental representation in working memory and, thus, serving memory storage (Polich, 2007). P3a, in contrast, is elicited by novel, unexpected stimuli and considered a psychophysiological index of orienting and involuntary capture of attention (Friedman et al., 2001). P3a has a shorter latency and a more anterior topographical distribution than the later and more posterior P3b (Courchesne et al., 1975; Squires et al., 1975; Simons et al., 2001). In accordance with Eccleston’s (1994) proposal that pain demands attentional resources, P3b amplitude to target tones in an auditory oddball task was found to be smaller in patients suffering from pain (Alanog˘lu et al., 2005). This was also observed in healthy participants experiencing experimentally induced pain during performance on auditory oddball (Rosenfeld and Kim, 1991; Lorenz and Bromm, 1997) and © 2014 European Pain Federation - EFICâ

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memory scanning tasks (Lorenz and Bromm, 1997; Houlihan et al., 2004). These results suggest that attentional processes serving memory storage are impaired by pain. The present study expands this research by investigating the influence of pain on the involuntary capture of attention as indexed by the P3a component, which, to the best of our knowledge, has not yet been investigated regarding changes due to pain experience. We expected the P3a amplitude to be reduced in an experimental pain condition compared with a painfree condition, indicating reduced capacities for involuntary orienting to new, unexpected events. To exclude the possibility that any observed reductions in P3a amplitude were attributable to a more generalized, nonspecific task effect rather than due to a specific attention-related effect, the N1 component was also analysed. Compared with P3a or P3b, the N1 is more sensitive to stimulus characteristics than to cognitive processes (Stelmack and Houlihan, 1995) although it is not free from attentional effects (Barry et al., 1992).

2. Methods 2.1 Participants Twelve volunteers (six women) ranging in age from 18 to 26 years [mean (M) = 19.5; standard deviation (SD) = 2.1 years] participated in the study. All participants had normal hearing and did not report to be suffering from any pain. They were asked to refrain from alcohol for at least 24 h, and from caffeine and nicotine for at least 1 h. They received 10 CAD/h for their participation. Participants were informed about the study protocol as well as the procedures applied and gave their written informed consent. The study was approved by the local research ethics committee.

2.2 McGill Pain Questionnaire (MPQ) To obtain a measure of the subjectively experienced pain, the McGill Pain Questionnaire (MPQ; Melzack, 1975) was administered. The MPQ presents 78 words characterizing pain in 20 categories. Participants were asked to read the words of each category and, if appropriate, to choose the word that described their pain experience. Categories 1–10 refer to the sensory properties of experienced pain while categories 11–15, 16 and 17–20 refer to affective, evaluative and miscellaneous properties, respectively. Scores on the four subscales are added to a total score with a reliability of rtt = 0.83 (Love et al., 1989). The MPQ also possesses high convergent validity with other measures of pain (Gagliese et al., 2005).

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2.3 Oddball task 2.3.1 Apparatus and stimuli Standard and target tones were sine-waves tones of 300 ms duration (including rise and fall times of 10 ms) with a pitch of 1000 and 700 Hz, respectively. Novel stimuli were 48 different types of environmental sounds such as a passing car, a horn, a human yell, animal sounds or synthesized sounds. Their duration ranged between 100 and 400 ms with an average duration of 300 ms. Stimuli were presented binaurally via headphones with an intensity of 70 db sound pressure level. Behavioural responses were recorded by a response pad with an accuracy of ±1 ms.

2.3.2 Procedure The task consisted of two blocks of 400 tones (76% standard, 12% target and 12% novelty tones). Each of the 48 novel stimuli appeared once in each block. Order of tones/novel stimuli was pseudo-randomized such that no two consecutive targets or two consecutive novel stimuli were presented. The stimulus onset asynchrony was fixed at 1000 ms. After about 6.5 min, a short break was given between the first and the second block. Participants were instructed to concentrate on the sounds and to press a labelled key on the response pad when a target tone had been presented and to ignore all other tones and sounds. Instruction emphasized responding as fast as possible but to avoid errors. As measures of performance, response time and hit rate were recorded.

2.4 Electroencephalogram recording Electroencephalogram (EEG) activity was recorded using a Neuroscan SynAmps amplifier and a Neuroscan Quick-Cap electrode cap (Neuroscan, Charlotte, NC, USA) with 128 Ag/AgCl electrodes referenced to the ear lobes. Horizontal and vertical EOG was recorded by four electrodes placed about 1 cm from the outer canthi of the eyes (horizontal EOG) and on the supra- and infraorbital ridges of the left eye (vertical EOG). Impedance was kept below 5 kΩ. EEG and EOG were digitized at a rate of 500 Hz and offline filtered (0.5 to 30 Hz). Raw data were visually inspected for movement artefacts. When movement artefacts were found, they were excluded. Using a regression-based procedure (Neuroscan’s regression-type algorithm), raw data were corrected for eye movements. Subsequently, EEG was segmented 100 ms before and 1000 ms after stimulus onset and these epochs were baseline corrected from the prestimulus interval. Epochs including voltage changes exceeding ±50 μV at the horizontal EOG electrodes or ±75 μV at any other channel were rejected to exclude artefacts. Visual and automatic artefact rejection resulted in the loss of 12 ± 9% of the epochs in the pain-free condition (14 ± 9% target, 13 ± 9% novel and 9 ± 9% standard) and 15 ± 9% of the epochs in the pain condition (19 ± 13% target, 13 ± 9% novel and 352 Eur J Pain 19 (2015) 350--357

13 ± 10% standard). In all participants the number of standard, target and novelty stimuli epochs clearly exceeded the number of 20 epochs recommended by Cohen and Polich (1997) for a reliable measurement of P3 components. Separate averages were constructed for standard, target and novelty stimuli. Target-related waveforms revealed a prominent positive wave identified as the P3b, which was maximal at Pz and occurred between 250 and 600 ms after stimulus onset (Polich, 2007). A clear positivity in the novelty-related waveforms was identified as P3a, which was maximal at Cz and occurred between 220 and 420 ms after stimulus onset (Simons et al., 2001). The N1 component was identified as the most negative peak between 75 and 150 ms after stimulus onset in the individual standard-related averaged waveforms at the Fz electrode site.

2.5 Time course of study and pain induction procedure About 1 week prior to the testing session, participants were invited to the laboratory. They read the study protocol and gave their written informed consent. Afterwards, they were asked to submerge their non-dominant hand in cold 1°C water for 60 s. Participants were excluded if they could not tolerate the pain for 60 s. At the beginning of the testing, participants were asked whether they suffered from any pain but none reported pain. Participants performed in the oddball task on two occasions – a pain-free condition and a pain condition during which they submersed their nondominant hand in cold 1°C water. The water was kept circulating by means of a pump to ensure that the hand did not warm the water immediately surrounding the limb. During the break in the oddball task, participants removed the hand from the water to recover. After a 5-min break allowing the arm to warm sufficiently, participants were asked to submerge the hand again in the cold water and to start the second block of the task. The order of the pain and pain-free conditions was counterbalanced across participants. After completing the pain condition, they removed their hand from the water and completed the MPQ.

3. Results To examine whether the experimental manipulation led to an increase of pain under the pain condition, scores on the MPQ were tested against zero (as no participant reported any pain at the beginning of the testing session). Mean MPQ scores in the pain condition were 41.33 (SD = 24.82; min = 12; max = 91) and differed significantly from zero [t(11) = 5.77; p < 0.001; d = 1.67]. Thus, the cold pressor test indeed induced pain in the pain condition. Mean and standard deviations of the behavioural data (hit rate and reaction time) as well as the psychophysiological data (amplitudes and latencies of P3a, P3b and N1, respectively) in the pain and pain-free © 2014 European Pain Federation - EFICâ

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Table 1 Mean (M) and standard deviation (SD) of hit rate and reaction time for target detection in the oddball task as well as for psychophysiological measures P3a, P3b and N1 in the pain and pain-free conditions, respectively. Also provided are t-tests and effect sizes (Cohen’s d) for the comparison of the two conditions. Pain condition

Hit rate Reaction time [ms] P3a (at Cz) Amplitude [μV] Latency [ms] P3b (at Pz) Amplitude [μV] Latency [ms] N1 (at Fz) Amplitude [μV] Latency [ms]

Pain-free condition

M

SD

M

SD

94.45 446

3.68 49

92.53 448

6.50 53

12.58 287

8.32 49

18.93 291

8.79 43

−5.06*** 0.71

−2.06 −0.26

13.90 362

5.15 47

19.33 372

5.99 63

−5.43*** 0.56

−1.69 −0.24

−4.39 116

1.89 15

−5.17 115

2.51 12

−2.39 0.19

t(11)

d

1.12 0.12

0.48 −0.06

1.17 0.10

To avoid alpha inflation, alpha was set to α = 0.00625. ***p < 0.001 (two-tailed).

conditions are given in Table 1. Also reported in Table 1 are t-tests and effect sizes for the comparisons of the dependent variables in the pain and pain-free conditions. To avoid alpha inflation, Bonferroniadjusted alpha level of α = 0.00625 per comparison (0.05/8) was employed. Neither rate of correct responses to the target stimuli (hit rate) nor reaction time differed significantly between the pain and the pain-free condition (see Table 1). The scalp distribution of the three ERP components are presented in Fig. 1 and justify the choice of Cz, Pz and Fz electrode sites for deriving P3a, P3b and N100, respectively. The target-related P3b amplitude was significantly smaller in the pain compared with the pain-free condition while the latency did not significantly change (see left panel of Fig. 2). The novelty-related P3a amplitude was significantly smaller in the pain condition and latencies in the pain and pain-free conditions again did not differ significantly from each other (see middle panel of Fig. 2). An exact binomial sign test indicated that P3a amplitude was reduced after pain in 11 out of 12 participants (p = 0.003). Likewise, P3b

µV

A Target-related ERP at Pz

µV

B Novel stimuli-related ERP at Cz

µV

amplitude was reduced following pain in 10 out of 12 participants. The exact binomial sign test confirms this with p = 0.016. Finally, the above-mentioned effects cannot be attributed to sensory reactivity since the N1 to the standard stimuli showed no differences between the two conditions in latency and – after alpha correction – in amplitude (see right panel of Fig. 2). A Target tones

B Novel tones

C Standard tones

Pain-free condition

Pain condition

–20.0 µV

20.0 µV

–10.0 µV

10.0 µV

Figure 1 Scalp topographies of the (A) P3b to target tones 367 ms after onset, (B) P3a to novel tones 287 ms after onset and (C) N1 to standard tones 115 ms after onset in the pain-free condition and the pain condition.

C Standard-related ERP at Fz

–16 N1

–8 0 8 P3b 100

300

500

700

ms

© 2014 European Pain Federation - EFICâ

Pain-free condition Pain condition

P3a

16 100

300

500

700

ms

100

300

500

700

ms

Figure 2 Grand averages for (A) the targetrelated P3b (left panel), (B) the P3a related to the novel stimuli (intermediate panel) and (C) the standard-related N1 (right panel) in the pain-free condition (solid lines) and the pain condition (dotted lines).

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The order with which the pain and the pain-free conditions were presented had no significant effect on the dependent variables reported above with exception of the N1 amplitude. The N1 amplitude was larger in individuals who were first assigned to the pain condition compared with individuals who were first assigned to the pain-free condition. This order effect, however, did not interact with the difference of the N1 amplitude between the pain and the pain-free condition. Despite the small age range in the present sample, age was significantly negatively correlated to the P3b amplitude in both the pain-free (r = −0.58; p < 0.05) and the pain condition (r = −0.65; p < 0.05). The pain minus pain-free difference scores for the P3b amplitude, however, were not significantly correlated with age (r = −0.03; p = 0.93), indicating that the reduction of P3b in the pain condition was unrelated to age. No age effects were observed for P3a or N1 amplitudes.

4. Discussion Previous research obtained good evidence for Eccleston’s (1994) proposition that pain demands attentional resources so that patients suffering from pain or individuals exposed experimentally to a painful procedure are limited in their cognitive functioning (Buhle and Wager, 2010). The present study investigated the effect of pain on the P3a and P3b components of the ERP as markers for the involuntary capture of attention (P3a) and attentional processes serving memory storage (P3b). Our results indicated that pain reduced both P3a and P3b amplitudes whereas the N1 amplitude was not influenced by pain. Hit rate and reaction time did not vary with pain. According to Johnson’s (1986) triarchic model, P3 amplitude increases with decreasing subjective target probability and with increasing subjective stimulus meaning. Johnson’s third dimension is information transmission, referring to the proportion of received information in relation to the total amount of information presented. As long as the information is presented unambiguously, information transmission depends on the amount of attention directed to the stimuli (Johnson, 1986). Since both target probability and stimulus meaning did not vary between the pain and the pain-free conditions, the smaller P3 amplitudes in the pain compared with the pain-free condition must be considered to be due to decreased attentional resources in the pain condition. This conclusion is corroborated by our finding that P3 amplitudes, as attention-related ERP components, were reliably reduced in the pain condition but not the N1 amplitude. The N1 amplitude is sensitive to stimulus 354 Eur J Pain 19 (2015) 350--357

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characteristics such as intensity and frequency and is less influenced by higher-order cognitive processes reflected by P3a and P3b (Pritchard, 1986; Barry et al., 1992). Thus, the lack of an effect of pain on the N1 amplitude indicates that pain did not generally affect the ERP but rather specifically reduced the attentionrelated components. Our finding that P3a and P3b amplitudes as attention-related ERP components were reduced by pain is consistent with the growing number of studies on the detrimental effect of pain on different aspects of attention. For example, patients suffering from chronic pain were impaired in selective attention (Grisart and Plaghki, 1999), sustained attention (Oosterman et al., 2011), attentional switching and vulnerability to interference (Eccleston, 1994; Bosma and Kessels, 2002) as well as in everyday attentional functioning and working memory (Dick and Rashiq, 2007). Also, experimentally induced pain has been shown to impair aspects of attention such as vulnerability to interference (Seminowicz et al., 2004) and selective attention as it is required by simple visual discrimination (Crombez et al., 2002) as well as attentional switching and executive aspects of attention (Bingel et al., 2007; Moore et al., 2013). The reduced P3a amplitude in the pain compared with the pain-free condition suggests that the involuntary capture of attention and orienting to novel and unexpected events is impaired by pain. This function of attention plays an important role when ongoing information processing has to be interrupted to direct attention to new information, as is the case in many daily life situations such as driving in traffic or any other situation that requires sudden attentional shifts (Friedman et al., 2001). While there are some studies on orienting towards painful stimuli (e.g., Dowman, 2004) and the involuntary capture of attention by pain as a disruption of ongoing cognitive activity (Legrain et al., 2009), the present study indicates the impairment of orienting towards new events during pain experience. Carter Kuhajda et al. (2002) have suggested that attentional deficits in patients suffering from headache may contribute to pain-induced memory deficits due to encoding difficulties. The decreased P3b amplitude in the pain compared with the pain-free condition in our study is consistent with this assumption. The P3b component reflects attentional processes serving memory storage of target stimuli (Polich, 2007). The reduction of the P3b amplitude in the pain condition therefore indicates that attentional resources, required for consolidating mental representations of target stimuli in working memory, are diminished by pain. This result is © 2014 European Pain Federation - EFICâ

Effect of pain on attention

consistent with previous studies (Rosenfeld and Kim, 1991; Lorenz and Bromm, 1997; Houlihan et al., 2004; Alanog˘lu et al., 2005) and could represent a functional link between pain-related attentional and memory deficits (Moriarty et al., 2011). Although we did not expect to observe age effects in our age range-restricted sample, it is well known that P3b decreases with increasing age (e.g., Fjell and Walhovd, 2001; Pontifex et al., 2009; Eppinger et al., 2010). There is also some evidence for the notion that (depending on the modality) pain sensitivity increases with age (e.g., Woodrow et al., 1972; Cole et al., 2010). The difference of the P3b amplitude between the pain and the pain-free condition, however, could not be explained by the influence of age as the effect disappeared in the pain–pain-free difference comparison. The finding that age was associated with P3b but not P3a amplitude corroborates that these two ERP components reflect clearly dissociable aspects of the attentional system (cf. Polich and Criado, 2006). In contrast to the attention-related psychophysiological measures, hit rate and reaction time in the oddball task did not differ between the pain and the pain-free conditions. Some might suggest that attention-based cognitive strategies to cope with the processing of pain could provide an explanation for this finding (Eccleston, 1995). From this perspective, it is conceivable that individuals are able to actively control (at least to a certain degree) the amount of attention directed to the task and/or away from pain. For participants in the present study, directing attention away from pain and towards the cognitive task might have been a possible strategy for alleviating the pain experience (Dubreuil et al., 1987/1988; Devine and Spanos, 1990). In this way, they prevented performance decrements in the pain compared with the pain-free condition, and the reduced attentional capacities in the pain condition might have been compensated for through increased concentration on the oddball task. An increase in hit rate might have been anticipated if this indeed occurred. The failure to observe differences in hit rate between the pain and pain-free condition may have been due to a ceiling effect. However, if attention was directed away from pain and towards the task, larger rather than smaller P3b amplitudes should have resulted in the pain compared with the pain-free condition, as the P3b reflects the inhibition of task-irrelevant information supporting the direction of attention to task-relevant information. Thus, considering behavioural and psychophysiological data together, attention-based cognitive strategies cannot plausibly explain the pattern of results obtained in the present study. © 2014 European Pain Federation - EFICâ

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Instead, it seems more likely that the absence of a pain effect for the behavioural data is due to the ease of discrimination of target from standard tones, as reflected in the high hit rate in both conditions. Hence, the attentional demands of the task and the concurrent processing of pain did not tax the attentional capacities such that a performance difference could not be observed, as has been reported in many studies using task conditions with low attentional demands (cf. Eccleston, 1994; Buhle and Wager, 2010). Furthermore, hit rate and reaction time reflect behavioural measures of discrimination performance and cannot be considered pure measures of attention, although the process of discrimination probably requires attention as reflected by the P3b component. Proceeding from this idea, the P3b amplitude provides more direct access to the attentional aspects of the discrimination process so that the influence of pain on attention during discrimination can be observed better with the P3b component than with behavioural measures (cf. Houlihan et al., 2004). This conclusion also underscores that a combination of behavioural and psychophysiological measures can be of particular importance for an unambiguous interpretation of obtained results (Eccleston and Crombez, 2005). As a limitation of the present study, it should be noted that we investigated individuals who were able to keep their hand in cold water for more than a minute. Pain-tolerant individuals can be distinguished from pain-sensitive individuals who withdraw their hand earlier (Chen et al., 1989a). Future studies have to examine whether our results can be generalized to pain-sensitive individuals. This is of particular interest since pain-sensitive individuals seem to differ from pain-tolerant individuals in cortical activity (Chen et al., 1989b) as well as in cognitive coping styles (Geisser et al., 1992). To summarize, the present study provides converging evidence for the notion that pain requires attention (Eccleston, 1994). While most previous studies investigated the effect of pain on voluntary attention serving the maintenance and control of ongoing information processing, the present study indicated that the involuntary capture of attention and the orienting towards new, unexpected events is also affected by pain. Furthermore, information consolidation in working memory was markedly reduced, pointing to a functional relationship between the impact of pain on attention and memory. Behavioural measures were not impaired by pain, probably because the attentional demands by pain and by the experimental task did not exceed the attentional capacities. Such dissociation between behavioural and psychophysiological meaEur J Pain 19 (2015) 350--357

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sures emphasizes the benefit of their concurrent investigation to detect accurately overt and covert effects of pain on attention and cognitive functioning. Author contributions Stefan Troche was responsible for the major portion of writing the manuscript together with Michael Houlihan. The main design and data collection of the project were the responsibility of Michael Houlihan, with expert advice from Patrick McGrath regarding the psychological impact of pain and John Connolly with his expertise in the event-related potential methodology. Bruce Dick also contributed to the design and data collection. Allen Finley contributed to the knowledge of pain and Gerhard Stroink contributed to the understanding of the methodology from the biomedical engineering perspective. All authors contributed to a certain degree in the manuscript writing.

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Eur J Pain 19 (2015) 350--357

357

The effect of pain on involuntary and voluntary capture of attention.

There is converging evidence for the notion that pain affects a broad range of attentional domains. This study investigated the influence of pain on t...
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