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1 This article was downloaded by:[universitat Wurzburg] On: 12 November 2007 Access Details: [subscription number ] Publisher: Psychology Press Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Cognition & Emotion Publication details, including instructions for authors and subscription information: Independent effects of emotion and attention on sensory and affective pain perception Ramona Kenntner-Mabiala a ; Peter Weyers a ; Paul Pauli a a University of Würzburg, Würzburg, Germany First Published on: 06 July 2007 To cite this Article: Kenntner-Mabiala, Ramona, Weyers, Peter and Pauli, Paul (2007) 'Independent effects of emotion and attention on sensory and affective pain perception', Cognition & Emotion, 21:8, To link to this article: DOI: / URL: PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material.

2 COGNITION AND EMOTION 2007, 21 (8), Independent effects of emotion and attention on sensory and affective pain perception Ramona Kenntner-Mabiala, Peter Weyers, and Paul Pauli University of Würzburg, Würzburg, Germany The present study investigated whether attention and emotion independently influence sensory and affective pain ratings. Fifty-four (27 female) participants rated sensory and affective pain in response to painful mechanic pressure stimulation while exposed to positive, neutral and negative slides from the International Affective Picture System. In doing so, participants were assigned to one of three groups, which focused attention either on the pictures or on the sensory or on the affective aspects of the pressure stimulation. Consistent with the motivational priming hypothesis, sensory and affective pain ratings were generally lower during exposure to positive compared to negative and neutral slides. In line with our assumptions, attention modulated sensory pain ratings with lowest ratings in the picture focusing group and highest in the affective pain focusing group. No attention effect for affective pain ratings and no interactions between emotional and attentional effects on pain perception were found. INTRODUCTION The nervous system incorporates several pain modulatory mechanisms, which may be activated through psychological manipulation. Especially, emotion and attention are discussed as powerful pain modulators (Fields, 2000). The motivational priming hypothesis (Lang, 1995) offers a theoretical framework to explain the influence of emotions on pain perception. According to this hypothesis, positively or negatively valenced background stimuli activate the appetitive or the defensive part of a biphasically organised motivational system, respectively. So, the response to a new stimulus is augmented if its valence is congruent with the activated part of Correspondence should be addressed to: Ramona Kenntner-Mabiala, Department of Psychology (Biological Psychology, Clinical Psychology, and Psychotherapy), University of Würzburg, Marcusstraße 911, D Würzburg, Germany. kenntner@psychologie.uni-wuerzburg.de This work was supported by the German Research Foundation (DFG, Pa 566/32). We thank Roswitha Gerhard for data collection, and those who kindly volunteered to participate in the study. # 2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business DOI: /

3 1616 KENNTNER-MABIALA, WEYERS, PAULI the motivational system and reduced if it is incongruent. This hypothesis has been extensively investigated with the acoustic startle reflex (e.g., Vrana, Spence, & Lang, 1988). Thereby, the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 1995)*a standardised set of picture stimuli, which systematically vary on the dimensions of valence and arousal*proved to be a useful tool for affect induction. Recently, we validated the assumption of affective pain modulation by measuring pain intensity ratings and somatosensory evoked potentials in response to painful electrical stimuli during processing of positive, neutral, and negative pictures (Kenntner-Mabiala & Pauli, 2005). Positive as compared to negative pictures were associated with lower pain intensity ratings and lower N150 amplitudes. This indicates that already relative early stages of cortical pain processing are modified by the valence of affective background stimuli. In addition to supraspinally mediated pain, affective pictures also seem to modulate spinally mediated nociception: Rhudy et al. (2005) found that nociceptive flexion reflex magnitudes and pain ratings were modulated by picture valence in a parallel manner with higher nociceptive flexion reflex magnitudes and pain ratings during negative pictures in comparison to positive pictures. However, a possible limitation of these findings is that pain responses to electrical stimuli are quite different from clinical situations, since electrical stimulation bypasses the nociceptors and activates the fibres directly (Staahl & Drews, 2004). Further evidence for the validity of the motivational priming hypothesis for pain perception is provided by studies using the cold pressor test for pain induction: Viewing negative pictures in comparison to positive pictures caused a decrease in pain tolerance (de Wied & Verbaten, 2001) and in pain threshold (Meagher, Arnau, & Rhudy, 2001). However, cold pressor pain and emotional pictures both cause vascular reactions (Lang, Greenwald, Bradley, & Hamm, 1993; Staahl & Drews, 2004). For example, heart rate systematically varies with affective picture valence. This might have systematic effects on the cold pressor test. Hence, pain tolerance and threshold findings in the studies described above might not directly be caused by picture valence but indirectly by the effects of affective pictures on the cardiovascular system. Therefore, the finding that emotional valence modulates cold pressor pain needs to be extended to another pain model such as tonic pressure pain, which does not involve strong cardiovascular reactions. In addition to emotion, attention is probably the most studied variable that affects pain (Villemure & Bushnell, 2002): Distracting participants attention from a painful stimulation reduces perceived pain (e.g., Johnson, Breakwell, Douglas, & Humphries, 1998; Lautenbacher, Pauli, Zaudig, & Birbaumer, 1998; Miron, Duncan, & Bushnell, 1989), whereas focusing attention on the painful event exacerbates pain perception (Levine, Gordon,

4 INDEPENDENT EFFECTS OF EMOTION AND ATTENTION ON PAIN 1617 Smith, & Fields, 1982). Interestingly, however, there is also evidence that the attentional effects depend on whether the participants focus on the sensory or on the affective aspects of pain. Ahles, Blanchard, and Leventhal (1983) instructed participants to attend to the sensory pain aspects or to express emotions during a cold pressor test. They found that attentional focus on the sensory as compared to the affective pain aspects was associated with less distress. Also, focusing on the threatening and emotional value of painful sensations caused more pain reports during a cold pressor test than concentrating on the concrete sensory aspects (Bishop, 1999). Furthermore, it is still a matter of debate whether attentional and emotional effects on pain perception interact. Villemure, Slotnick, and Bushnell (2003) suggested that attention and affect differentially alter pain perception and thus invoke at least partially separable neural modulatory circuits. They independently manipulated direction of attention and emotional state and found that positive stimuli reduced pain unpleasantness ratings as compared to negative stimuli, but there was no stimulus valence effect on pain intensity ratings. In contrast, attention altered pain intensity ratings without significantly influencing pain unpleasantness ratings. The present study was conducted in order to replicate and extend prior findings on the affective and attentional modulation of pain perception. The first objective was to extend the experimental findings that affect modulates cold pressor pain to a more naturalistic pressure pain model. The second objective was to examine how three different attentional foci (sensory pain vs. affective pain vs. pictures) affect pain perception. Finally, we investigated whether the effects of attention and emotion on pain interact or not. We expected (1) an affective modulation of sensory and affective pain with higher pain ratings during presentation of negative as compared to positive pictures, and (2) an attentional modulation of sensory pain ratings only with highest ratings with attention focused on affective pain and lowest ratings with attention focused on external stimuli, i.e., the affective pictures. However, we expected (3) no interaction between emotional and attentional effects on pain perception. Finally, we exploratively investigated gender effects since several studies found that attentional manipulations affect pain perception differentially in men and women (see Keogh, Hatton, & Ellery, 2000). METHODS Participants and experimental design Fifty-four paid volunteers (27 females and 27 males, aged between 18 and 40 years) free of neurological, psychiatric or chronic pain disease signed informed consent and participated in the experiment. A 332 mixed factorial design was realised with Picture Category (positive vs. neutral vs.

5 1618 KENNTNER-MABIALA, WEYERS, PAULI negative) as within-factor and Attention Focus (pictures vs. sensory pain vs. affective pain) and Sex as between-factors. Participants were equally distributed to the three attention focus groups. One woman from the picture focusing group and one man from the affective pain focusing group were excluded because after the experiment they reported that they had been unable to focus attention in the instructed direction. Stimulus material Eighteen colour pictures, 6 pleasant (4680, 5260, 5621, 8170, 8200, 8370), 6 neutral (7002, 7004, 7006, 7031, 7100, 7150), and 6 negative (2730, 2800, 6212, 6313, 9600, 9910), were chosen from the IAPS. Selection criteria were normative ratings on the dimensions of valence and arousal (Lang et al., 1995). The negative and the positive pictures were chosen to have similar arousal ratings but markedly different valence ratings. The neutral pictures were chosen to have low arousal and intermediate valence ratings. Three additional pictures (2840, 8540, and 9911) served as examples in a practice block. The IAPS-pictures were presented on a 19-inch computer screen. Presentation was controlled by the computer software Experimental Run Time System 3.32 (BeriSoft Corporation). Algesimetry Painful stimulation was delivered with an electronically driven device developed in our own laboratory according to the apparatus described by Ellermeier and Westphal (1995). Triggered by a button press of the experimenter a lever lowered a flat-tipped stylus with a diameter of 3 mm applied on the phalanx of the ring finger, the middle finger or the index finger of one or the other hand. The weight of the lever is continuously adjustable between 0 and 970 g (resulting in a constant pressure of 0 to 1339 kpa). Based on previous studies (Göbel, 1986; Göbel & Westphal, 1987), we choose a weight of 550 g, resulting in a constant pressure of approximately 690 kpa, to result in a moderately painful sensation for most participants. Following Villemure et al. (2003), visual analogue scales were used to assess the sensory and affective pain aspects of the pressure stimulation. The 200 mm sensory pain rating scale was anchored with 0no pressure, 100just noticeable pain, 120slight pain, 180strong pain, and 200unbearable pain. The 200 mm affective pain rating scale was anchored with 100very unpleasant and 100very pleasant. For analysis, all ratings were recoded to a scale ranging from 0 to 200.

6 INDEPENDENT EFFECTS OF EMOTION AND ATTENTION ON PAIN 1619 Procedure After reception, the participants read an information sheet about the experimental procedure, gave their informed consent, completed the State and Trait Anxiety Inventory (STAI; Laux, Glanzmann, & Schaffner, 1981) and the Positive and Negative Affect Schedule (PANAS; Watson, Clark, & Tellegen, 1988) and provided demographic information. Following this, the algometer was calibrated to the individual finger size, and the experimenter marked three different positions for the pressure applications on the dorsal sides of the middle phalanges of the index, the middle and the ring fingers of the non-dominant hand. The site of the pressure stimulation was changed after each block in order to prevent repetition effects; the sequence of measurement sites was balanced across participants. The practice block was performed at the middle phalanx of the index finger of the dominant hand. Then participants read a computer-presented instruction for the experimental procedure. Participants were instructed that one assessment block included the simultaneous exposure to affective pictures and painful pressure stimulation. Depending on which attention focus group the participants were randomly assigned to, they were also instructed to focus their attention during each assessment block either on the pictures or on the sensory or on the affective aspects of the pressure pain stimulation. We stressed the differences between sensory and affective pain using instructions taken from Price, McGrath, Rafii, and Buckingham (1983). Following this, the practice block was run and, if necessary, the pressure applied by the algometer was adjusted, i.e., since in 10 participants (5 females, equally distributed across the attention conditions) sensory pain ratings in the practice block were below 100 (meaning just noticeable pain ), we augmented the weight of the algometer lever to 700 g, according to the work by Göbel (1986). Thereafter the three experimental blocks were conducted. Sequence of picture valence was balanced across participants. Following the experimental procedure, participants were asked if they were effective in focusing attention on either the pictures or the sensory or the affective pain. The sequence of all blocks was as follows: The participant was requested to adduct the specified finger phalanx at the stylus of the algometer. Thereby the participant was reminded to focus attention on the pictures, the sensory pain, or the affective pain. Then the experimenter started the pressure stimulation and the presentation of the pictures. During each block, six pictures of the same valence were presented for 8 seconds each. After the presentation of the third and sixth picture, the visual analogue scales were presented for 14 seconds, and the experimenter asked the participants to verbally rate the sensory and affective pain aspects of the pressure stimulation. After the last VAS rating the pressure stimulation was finished

7 1620 KENNTNER-MABIALA, WEYERS, PAULI and the participant was requested to rate valence and arousal of the pictures. The Self-Assessment Manikin (SAM; Lang, 1980) was used to obtain subjective ratings of valence and arousal for the pictures on scales ranging from 1 to 9. A detailed description of the SAM-rating procedure was given verbally by the experimenter before the experiment. Data analysis Ratings were analysed with repeated-measures ANOVAs. If necessary, Greenhouse Geisser corrections were applied. Significant effects were followed up by comparisons of means using the Bonferroni procedure. Significance level was set to pb.05. If not otherwise indicated, all data are presented as means9sds. RESULTS Picture ratings Figure 1 depicts the mean valence and arousal ratings for the three picture categories. ANOVAs with Picture Category as within factor and Attention Focus and Sex as between factors for SAM valence and SAM arousal ratings revealed significant main effects of Picture Category, valence rating F(2, 92)367.3, pb.001; arousal rating F(2, 92)84.3, pb.001. No other main or interaction effect reached significance. 9 Rating (1-9) Picture content Positive Neutral Negative Valence Arousal Figure 1. Mean valence and arousal ratings with standard error for positive, neutral and negative pictures. The scores ranged from 1 (low pleasure, low arousal) to 9 (high pleasure, high arousal).

8 INDEPENDENT EFFECTS OF EMOTION AND ATTENTION ON PAIN 1621 Follow-up comparisons for the three picture categories showed that for valence as well as arousal ratings all pairs of means were significantly different from each other (all psb.001). Polynomial ANOVAs revealed for valence ratings significant linear, F(1, 46)600.2, pb.001, and quadratic trends, F(1, 46)14.6, pb.001, and also for arousal ratings significant linear, F(1, 46)74.0, pb.001, and quadratic trends, F(1, 46)104.2, pb.001. Pain ratings Figure 2 depicts the mean sensory and affective ratings as a function of Picture Category, Figure 3 the sensory and affective ratings as functions of Attention Focus. An ANOVA with Rating (sensory vs. affective) and Picture Category as within factors and Attention and Sex as between factors revealed a significant main effect of Rating, F(1, 46)52.7, pb.001, with higher scores for affective pain ratings ( ) than for sensory pain ratings ( ), and a significant main effect of Picture Category, F(2, 92) 14.1, pb.001. Follow-up comparisons for the three picture categories showed overall lower scores for the positive ( ) as compared to the neutral ( ) or the negative pictures ( ), with no 180 Pain rating Picture content Positive Neutral Negative Sensory pain rating Affective pain rating Figure 2. Mean sensory and affective pain ratings with standard error as function of picture content.

9 1622 KENNTNER-MABIALA, WEYERS, PAULI 180 Figure 3. focus. Pain rating Attention focus 175 Pictures Sensory pain 170 Affective pain Sensory pain rating Affective pain rating Mean sensory and affective pain ratings with standard error as functions of attentional significant differences between the neutral and the negative pictures (see Figure 2). Polynomial ANOVA revealed a significant linear, F(1, 46)17.9, pb.001, and a marginally significant quadratic trend, F(1, 46)3.2, pb.051. Furthermore, the ANOVA revealed significant RatingAttention Focus, F(2, 46)3.3, pb.048, and SexAttention Focus interactions, F(2, 46)3.6, pb.036. The Rating Attention Focus interaction was followed-up by separate ANOVAs for each rating scale, which revealed a significant effect of Attention Focus for sensory pain ratings, F(2, 49)3.3, pb.044, but not for affective pain ratings, F(2, 49)2.5, pb.092 (see Figure 3). Follow-up comparisons for the sensory ratings revealed higher ratings in the affect focusing group than in the picture (pb.05, one-sided) or in the sensory focusing group (pb.04, one-sided), but no significant difference between the sensory focusing and the picture group. The SexAttention Focus interaction was followed-up by separate ANOVAs for men and women revealing a significant effect of Attention Focus for women, F(2, 23)7.7, pb.003, but not for men, F(2, 23)0.4 (see Figure 4). Follow-up comparisons for the women revealed a significant difference between the picture focusing and the affective pain focusing group (pb.002) with all other comparisons not being significant.

10 INDEPENDENT EFFECTS OF EMOTION AND ATTENTION ON PAIN Pain rating Supplementary analysis Females Attention focus Pictures Sensory pain Affective pain Males Figure 4. Mean pain ratings with standard error of female and male participants as functions of attentional focus. Since the arousal ratings for positive pictures were significantly lower than for negative pictures, we conducted a supplementary analysis of picture and pain ratings with those 15 participants (8 females; 3 subjects from the picture focus condition, 7 subjects from the sensory pain focus condition, and 5 subjects from the affective pain focus condition) who rated positive and negative pictures as equally arousing. ANOVAs revealed significant effects of Picture Category for valence ratings, F(2, 28)114.5, pb.001, arousal ratings, F(2, 28)47.6, pb.001, as well as pain ratings F(2, 28)4.6, p.022. As to be expected, arousal ratings were higher for positive (M ) and negative pictures (M ) than for neutral pictures (1.59.8). Follow-up comparisons for the arousal ratings showed that the mean difference between positive and negative pictures did not reach significance (p1), but that the other differences were significant (all psb.001). Polynomial trend analyses for arousal ratings revealed a significant quadratic trend, F(1, 14)63.2, pb.001, but no significant linear trend, F(1, 14)0.04, p.86. Valence ratings were highest for positive pictures (M ) and lowest for negative pictures (M ) with valence ratings for neutral pictures being in between (M ). Follow-up comparisons for the

11 1624 KENNTNER-MABIALA, WEYERS, PAULI valence ratings showed that all pairs of means were significantly different from each other (all psb.001). Pain ratings were lower for positive pictures (M ) than for neutral (M ) and negative pictures (M ). Polynomial trend analyses for pain ratings revealed a significant linear trend, F(1, 14)7.3, p.017, but no significant quadratic trend, F(1, 14)0.9, p.364. DISCUSSION The present study investigated the effects of affect and attention on sensory and affective pain perception. Consistent with our predictions based on the motivational priming hypothesis (Lang, 1995), which proposes that responses triggered by aversive stimuli are facilitated in the context of a negative emotional state and inhibited in the context of a positive emotional state, the same pressure stimulus elicited lowest pain ratings (sensory and affective) while participants viewed positive pictures and highest ratings while participants viewed negative pictures. Pain ratings while viewing neutral pictures fell in between although only the difference to positive pictures reached significance. These findings confirm previous reports based on electrical stimuli (Kenntner- Mabiala & Pauli, 2005; Rhudy et al., 2005) and the cold pressor test (de Wied & Verbaten, 2001; Meagher et al., 2001) and extend it to a pressure pain model. Although we have chosen positive and negative pictures with similar normative arousal levels, the subjective arousal ratings in the present study were very dissimilar for positive and negative pictures. One might assume that picture valence is less important in influencing pain than picture arousal. However, pain ratings were lowest during positive picture viewing but arousal ratings were lowest during neutral picture viewing. This indicates that arousal does not seem to be that important for affective picture pain modulation. Furthermore, in order to contradict the assumption that the pain modulation is due to arousal effects, we conducted a supplementary data analysis with only those participants who had rated positive and negative pictures as equally arousing. This analysis revealed that pain perception was lower during positive than during negative picture viewing. Since for this subgroup picture arousal was constant and picture valence was the only varying variable, the picture content effect on pain perception can only be an effect of picture valence and not of picture arousal. An important new finding of the present study is that both sensory and affective pain ratings were modulated by the valence of the affective pictures in a similar way. This is in contrast to Villemure et al. (2003), who found that

12 INDEPENDENT EFFECTS OF EMOTION AND ATTENTION ON PAIN 1625 emotional manipulations only affected the affective but not the sensory pain perception. This discrepancy may be explained by different affect induction methods, different pain assessments or differences in statistical power (in contrast to the present study with 52 participants, Villemure et al. examined only 15 participants). Attentional focus on the pictures was associated with lower sensory pain ratings than attentional focus on the affective pain aspect. However, attentional manipulations did not significantly modulate affective pain ratings. These findings are consistent with Villemure et al. (2003) and Keogh et al. (2000), who also found that attentional manipulations particularly modulated the sensory pain aspect, while affective pain ratings were either less or not affected. However, Lautenbacher et al. (1998) found that attentional manipulations similarly influenced both pain components. As a matter of fact, the effect of attention focus on affective pain ratings just missed significance in the present study as well as in the study of Villemure et al. Therefore we conclude that attentional manipulations affect both sensory and affective pain ratings, but affective pain ratings to a lesser degree. The affective dimension of pain is composed of feelings of unpleasantness and emotions associated with future implications, whereas the sensorydiscriminative dimension of pain comprises spatial, temporal, and intensity properties (Price, 2000). On the one hand, the dissociation of these two components was empirically demonstrated by studies using multivariate statistics, signal detection theory, and unidimensional scaling. In line with these findings, Villemure et al. (2003) interpreted their observation that emotional and attentional manipulations modulate affective and sensory pain differently, as evidence for the existence and the measurability of these two dimensions of pain. On the other hand, Fernandez and Turk (1992) reviewed the literature and concluded that although these pain components are separable, they are not necessarily independent. Chapman et al. (2001) even argued that the sensory and affective dimensions of pain are indistinguishable when using self-reports. However, nearly all of the participants in the present study declared that they were able to focus on the sensory or the affective aspects of the painful pressure sensation in particular, indicating that the differentiation between the sensory and the affective pain component is not just a theoretical construct but is comprehensible by psychological and medical laities. The important finding that affect and attention did not interact provides further evidence for the independence of these two factors. The attentional and affective modulation of pain perception is presumably based on the involvement of different neural modulatory circuits. However, up to now, these neural circuits are only partially known, and some anatomical structures are apparently involved in both the attentional and the affective modulation of pain. The periaqueductal grey (PAG) may be critical for the

13 1626 KENNTNER-MABIALA, WEYERS, PAULI attentional control of pain. So, in a recent functional magnetic resonance imaging (fmri) study, Tracey et al. (2002) found a significant increase in activation associated with noxious thermal stimulation within the PAG when subjects were distracted from pain. In addition, Porro (2003) reviewed the literature and identified the anterior cingulate cortex (ACC), the amygdala, and the primary and secondary somatosensory cortex (SI and SII) as brain structures possibly involved in the attentional modulation of pain. The neural mechanisms underlying the influences of affect on pain perception have not been directly examined until now. Yet, there is indirect evidence demonstrating pain-related activity in the ACC, which is specifically modulated by changes in pain unpleasantness (Rainville, Duncan, Price, Carrier, & Bushnell, 1997). This finding suggests that the ACC might not only be important for attentional but also for affective pain modulation. The prefrontal cortex is activated by stimuli with either positive or negative hedonic value (Royet et al., 2000), and these areas are also related to pain perception (Coghill, Sang, Maisog, & Iadarola, 1999). Another important finding of the present study is that females and males differ with respect to the effect of attention focusing on pain perception: Females in the picture focusing group had significantly lower pain ratings than those in the affective pain focusing group, pain ratings in the sensory pain focusing group were in between. For men, there was indeed no significant attention effect on pain perception but the descriptive inspection of the data revealed lower pain ratings in the sensory focusing group than in the picture and in the affective pain focusing group. Keogh et al. (2000) compared the effects of two different attentional strategies (focused vs. avoidance) in males and females using the cold pressor test. Focusing attention on pain in comparison to avoidance was useful for men, but there was no significant effect in women. With these and our results, it seems that both males and females can benefit from attentional coping strategies depending on which strategy is proposed. The most appropriate pain reduction strategy for women may be to distract attention away from the painful event while men may profit from focusing on the sensory pain aspects. Focusing attention on the affective pain component presumably is a non-adaptive coping strategy for both males and females. A limitation of this study is that we did not record any physiological measures of arousal. Although Lang et al. (1993) found a correlation of.81 between skin conductance reactions and subjective arousal ratings in response to positive, neutral and negative IAPS pictures, self-reported arousal and physiological arousal do not necessarily always correlate. Therefore, it would be valuable for further research to also examine physiological arousal measures in order to find out whether valence is the sole contributor to affective pain modulation and whether arousal is a confounding variable.

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