COGNITION AND EMOTION, 2015 Vol. 29, No. 5, 910–922, http://dx.doi.org/10.1080/02699931.2014.954529

BRIEF REPORT The effect of pain and the anticipation of pain on temporal perception: A role for attention and arousal Ruth S. Ogden1,2, David Moore1,2, Leanne Redfern2, and Francis McGlone1,2 1 2

Research Centre for Brain and Behaviour, Liverpool John Moores University, Liverpool, UK School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK

The overestimation of the duration of fear-inducing stimuli relative to neutral stimuli is a robust finding within the temporal perception literature. Whilst this effect is consistently reported with auditory and visual stimuli, there has been little examination of whether it can be replicated using painful stimulation. The aim of the current study was, therefore, to explore how pain and the anticipation of pain affected perceived duration of time. A modified verbal estimation paradigm was developed in which participants estimated the duration of shapes previously conditioned to be associated with pain, compared to those not associated with pain. Duration estimates were significantly longer on trials in which pain was received or anticipated than on control trials. Slope and intercept analysis revealed that the anticipation of pain resulted in steeper slopes and greater intercept values than for control trials. The results suggest that increased arousal and attention, when anticipating and experiencing pain, result in longer perceived durations. The results are discussed in relation to internal clock theory and neurocognitive models of time perception. Keywords: Time perception; Pain; Attention; Arousal; Emotion.

A robust finding within the temporal perception literature is that our experience of time is influenced by emotion. The most consistent finding is that negative, fear-inducing stimuli are perceived as lasting for longer than neutral stimuli of the same duration (see Droit-Volet & Gil, 2009; Droit-Volet & Meck, 2007 for reviews). This

effect is observed with static visual stimuli (e.g., Gil & Droit-Volet, 2011, 2012) and emotional auditory stimuli (e.g., Droit-Volet, Mermillod, Cocenas-Silva & Gil, 2010; Mella, Conty, & Pouthas, 2011); however, research using somatosensory stimuli is rare, and findings are often conflicting. Longer duration estimates for painful

Correspondence should be addressed to: Ruth S. Ogden, School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK. E-mail: [email protected] This work was funded by an Experimental Psychology Society Summer Studentship awarded to Dr Ruth Ogden and Leanne Redfern. © 2014 Taylor & Francis

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than neutral stimuli have been reported in animals (Meck 1983) and humans (Falk & Bindra, 1954; Hare, 1963). However, shorter estimates for painful than neutral stimuli have also been observed (Hellstrom & Carlsson, 1997). Such disparity may reflect the methods used; in Hare (1963) and Hellstrom and Carlsson (1997), participants judged long durations (>20 seconds and 120 > 300 seconds, respectively) without being prevented from counting. The studies also used different methods of pain induction: electric shock (Hare, 1963) and hand submersion in cold water (Hellstrom & Carlsson, 1997). Thus, whilst our understanding of how auditory and visual emotional stimuli influence timing is well established, there is a lack of clarity surrounding how emotional painful stimulation may influence temporal perception. The current study therefore aimed to explore the effect of painful stimulation on perceived duration by using modified versions of paradigms used when exploring auditory and visual temporal perception. One reason to suspect that painful stimulation may not affect duration perception in an identical way to negative emotional auditory and visual stimuli is that it is interoceptive in nature. Vision and audition are classed as exteroceptive senses in that they provide the brain with information about the environment (Craig, 2002). Some aspects of somatosensory stimulation are classed as interoceptive as they provide the brain with information about the body itself (Craig, 2002), i.e., serve an interoceptive function. It has been suggested that temporal perception and interoceptive selfrepresentation may share a common neural basis (Wittmann, 2009) in the insular cortex (Craig, 2009). The anterior insular cortex has been shown to be activated during temporal perception (Livesey, Wall, & Smith, 2007) and emotional experience (Craig, 2002), leading Craig (2009) to suggest that emotion-induced activation of the anterior insular cortex could influence concurrent temporal processing by the insular cortex, resulting in emotion-induced distortions to time. Because the insular cortex is also thermosensitive (Craig, Chen, Bandy, & Reiman, 2000) and activated during pain and the anticipation of pain (Ploghaus

Figure 1. A modified schemata of SET.

et al., 1999), painful stimulation is likely to have a significant effect on time perception via this mechanism. Within the framework of internal clock theory, the arousing, attention-grabbing nature of pain suggests that it is likely to affect timing. According to Scalar Expectancy Theory (SET; see Figure 1; Gibbon, Church, & Meck, 1984), perceived duration is based on the output of a pacemaker– accumulator clock, whereby more output corresponds to more perceived time. The rate at which the pacemaker emits ticks is sensitive to arousal, with increases in arousal leading to increases in output and a longer perceived duration. Stimuli such as angry faces and emotional sounds are therefore thought to affect perceived time because they evoke negative affect. This increases arousal, leading to an increase in pacemaker rate and a longer perceived duration (Gil & Droit-Volet, 2012). This is thought to occur because fearinduced amygdala activation influences subsequent subcortical processing related to duration (Gil & Droit-Volet, 2012). Pain and the anticipation of pain produce feelings of fear, anger, anxiety and frustration (Rhudy & Meager, 2000). This increases physiological arousal, resulting in increased pupil diameter and other autonomic responses (see Norton & Asmundson, 2003, for review). Pain anticipation and experience also produce amygdala activation (Bornhovd et al., 2002); thus there is a physiological and neural mechanism for pain to alter perceived duration. If, as Gil and Droit-Volet (2012) suggest, arousal is the primary mechanism by which emotion affects COGNITION AND EMOTION, 2015, 29 (5)

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time perception, the arousing nature of pain means that its duration should be overestimated in a manner consistent with that observed for negative auditory and visual stimuli. Internal clock theory also suggests that the amount of attention paid to time will influence perceived duration (Wearden, O’Rourke, Matchwick, Min, & Maeers, 2010). Attention affects timing because it influences the operation of the switch connecting the pacemaker and the accumulator. When this connector is closed, pacemaker output is transferred to the accumulator, enabling timing. Rapid orientation to the start of a to-be-timed event is therefore critical for accurate timing as missing the onset of an event may increase the latency with which the switch closes, resulting in a shorter perceived duration. Attentional processing is influenced by emotion, with more rapid orientation being observed for fearinducing than neutral stimuli (Vuilleumier, 2005). Because pain and the anticipation of pain are invasive, they have a high threat value, which rapidly and effectively captures attention (Eccelston & Crombez, 1999; Van Damme, Crombez, & Eccleston, 2004). Thus, the attentional effects of pain may also alter perceived duration. Although Gil and Droit-Volet (2012) suggest that arousal is the primary mechanism by which emotion influences timing, recent literature suggests that attention and arousal may work together to produce the effects observed (Burle & Cassini, 2001; Ogden, 2013; Wittmann, 2009). For example, fear-inducing stimuli may capture attention effectively, enabling a rapid and efficient onset to the timing process, whilst also increasing arousal, leading to a change in pacemaker speed. The potential for interactive effects between arousal and attention may have been somewhat overlooked in the existing literature because of the nature of the stimulus employed. Yiend (2010) suggests that for emotion to modulate attention, the threat level induced must be sufficiently high. In previous studies using auditory and visual stimuli, it is possible that threat levels may not have been sufficiently high to allow the attentional effects on timing to be observed. The high threat level of pain means that its use as a stimulus may

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highlight a role for attention in the emotional modulation of duration. Isolation of arousal and attentional affects can be achieved mathematically; changes in pacemaker rate are multiplicative, i.e., the magnitude of the effect increases with the duration of the stimulus being timed (Meck, 1983). Attentional effects are, however, additive, producing constant effects on perceived duration regardless of the duration being timed (Wearden et al., 2010). Thus, it is possible to establish whether any effects of pain on timing are a consequence of pacemaker operation in isolation, attention in isolation or a combination of the two.

THE CURRENT STUDY Given the lack of clarity surrounding the effects of painful stimulation on the perception of time, which may be in part due to the methodological weaknesses of existing studies, the current study sought to re-examine how painful thermal stimulation influenced perceived time using paradigms akin to those used with auditory and visual stimuli. To do this, a modified verbal estimation paradigm was developed. The paradigm first involved a learning phase in which two shapes were presented, and participants learned to associate one of the shapes (e.g., square) with the concurrent occurrence of a painful sensation on their right arm and the other shape (e.g., triangle) with no pain. Following this learning phase, participants completed a timing task (verbal estimation) in which they estimated the presentation duration of the shapes previously learned to be associated with pain (e.g., square) and no pain (e.g., triangle). During this phase of the experiment, there were three trial types: control trials in which pain was neither expected nor delivered, pain trials in which pain was expected and experienced and anticipation trials in which pain was expected but not experienced. During pain trials, pain was only delivered for the final 300 ms of visual stimulus presentation. Thus, throughout an anticipation trial, participants would have been expecting the potential arrival of pain.

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This design enabled three things: (1) examination of how the experience of a noxious somatosensory stimulus alters perceived duration; (2) examination of how the anticipation of a noxious somatosensory stimulus affects perceived duration; and (3) examination of the effect of emotion on timing when there are no significant physical differences in the stimuli employed in the emotional and neutral conditions. This final point is critical because the majority of existing studies exploring the effect of emotion on timing have used different physical stimuli in the emotional and neutral conditions (e.g., neutral and negative images from the International Affective Picture System [IAPS]) (Lang, Bradley, & Cuthburt, 2005). The perceived duration of auditory and visual stimuli can be altered by the properties of the stimuli, e.g., luminance and the numerosity of components (Xuan, Zhang, He, & Chen, 2007). Consequently, the effects observed in studies, where the stimuli in the emotional and neutral conditions are not similar, may be due to factors other than, or in addition to, emotion (Gil & Droit-Volet, 2012). The use of emotional faces goes some way to overcoming this issue because of the structural similarity of the stimuli in each condition. This too, however, is problematic because the emotional perception of faces is thought to be processed by distinct neural circuitry from other emotional stimuli (Kanwisher, McDermott, & Chun, 1997). Therefore, in addition to exploring the effect of negative tactile stimulation on timing, the current study also aimed to confirm whether the emotional modulation of timing observed with auditory and visual stimuli is a consequence of idiosyncratic differences the stimulus employed in the emotional and control conditions or a result of emotion itself. Because pain and the anticipation of pain are arousing, it is anticipated that longer perceived durations will be observed in pain and anticipation trials relative to control trials. In addition, because pain has a high threat value and rapidly captures attention, it is anticipated that both additive and multiplicative differences will be observed between the control and pain-related trials, thus

demonstrating both pacemaker and attentional effects on timing.

METHOD Participants Twenty-four Liverpool John Moores University female undergraduates participated (Mage = 23.17 years, SD = 5.65). Participants were paid £10 for taking part. All the participants provided written consent.

Apparatus and materials Pain induction Pain stimulation was achieved through the use of a Medoc PATHWAY—Contact Heat-Evoked Potential Stimulator. This has been designed for use in clinical and research settings and induces thermal pain through a 27 mm diameter Peltier thermode (572 mm2 contact area), which is placed on the skin. The temperature of the thermode is controlled through specialist hardware and software, designed for experimental purposes. The thermode was attached to the participant’s nondominant volar forearm. The thermode started from a baseline temperature of 32°C, and the temperature increased at a rate of 70°C/second to 52°C and decreased to baseline at a rate of 40°C/ second. Thermal stimulation of 52°C was applied in this manner for the final 300 ms of visual stimulus presentation. Verbal estimation An IBM compatible computer recorded all experimental events. To-be-timed stimuli were presented on the computer screen, and the keyboard recorded all responses. The programme used to run the experiment and record data was written in E-Prime (Psychology Software Tools, Inc., Pittsburgh, PA). Pain Catastrophizing Scale (PCS) The PCS is a 13-item self-report measure designed to measure rumination and COGNITION AND EMOTION, 2015, 29 (5)

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magnification of pain-related thoughts and perceived helplessness in relation to pain (Sullivan, Bishop, & Pivik, 1995). Participants are asked how strongly they agree with a range of statements, e.g., “When in pain, I cannot get it out of my mind”. The PCS has high internal reliability (Cronbach’s alpha = .87). Visual analogue scales To examine participants’ feelings about the pain sensation experienced during the experiment, participants completed three 100 mm visual analogue scales (VASs) upon completion of the experimental task. Participants were asked the following questions: (1) How much pain did you feel during the task? (2) How much distress did the pain you felt cause you? and (3) How aware of the pain were you during the tasks? Participants were instructed to base their responses on their experience throughout the whole experimental task.

Procedure The experiment had two parts: a learning phase and a timing phase. The learning phase was designed to develop an association between a particular visual stimulus and the experience of pain. The timing phase tested the effect of the learned association on perceived duration. Learning phase In the learning phase, participants were instructed that shapes would be presented on the computer screen, and their task was to indicate the number of corners in each shape using the computer keyboard. At the start of each trial, a stimulus (triangle or square) was presented on the screen for 1500 ms. To create an association between pain and a particular shape, pain was delivered for the final 300 ms of the presentation one shape (e.g., square) on 50% of its presentation. Pain was never delivered when the other shape was presented (e.g., triangle); these trials therefore constituted control trials. A total of 20 learning trials were conducted: 10 control trials in which pain was neither expected nor delivered, 5 pain trials in

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which a shape (e.g., square) was presented and pain was delivered for the final 300 ms of the shape’s presentation, and 5 anticipation trials in which the shape associated with pain was presented (e.g., square) and no pain was delivered. These trials were labelled as anticipation trials because participants would, in the timing phase, associate the stimulus with pain, but no pain would be delivered. Following the presentation of each shape stimulus, a 500-ms delay was interposed. Following this, participants were asked to indicate how many corners the stimulus had. Trials were presented in a random order. Following the completion of the learning phase, participants immediately performed the timing phase. Timing phase In the timing phase, participants were informed that the shapes seen in the learning phase of the experiment would be presented again; however, this time their task was to estimate, in milliseconds, how long each shape was displayed on the screen for. This method is known as verbal estimation. Participants were informed that as in the learning phase the appearance of a particular shape would sometimes be accompanied by a painful sensation on their right forearm. The control, pain and anticipation stimuli used in learning phase were used again in the timing phase. The basic trial structure was as follows: at the start of each trial, a shape was presented on the computer screen. A delay of 500 ms or 750 ms was then interposed. Participants were then instructed to type their estimate of how long the shape was presented for using the keyboard, having been informed that all shapes would be presented for between 100 ms and 1700 ms. Participants were instructed not to count when timing stimulus presentation. This method has been shown to be effective in suppressing counting (Rattat & Droit-Volet, 2012). The duration that the shape was presented on the screen for was determined by the trial type. In each experimental block, on anticipation and control trials, stimuli were presented for the following five standard durations: 242 ms, 455 ms, 767 ms, 1058 ms and 1296 ms. Comparison

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performance feedback was given. Table 1 shows information regarding the number and type of trials per block. Upon completion of the computer task, participants completed the three VASs and the PCS.

RESULTS All participants reported experiencing pain during the experiment (M = 51.83, SD = 13.99). Participants reported that the pain caused some distress (M = 18.46, SD = 15.52) and that they were aware of the pain throughout the experiment (M = 64.21, SD = 12.05).

1200 1000 Mean verbal estimate (ms)

of estimates given for these anticipation and control trials enabled examination of the effect of anticipating pain on perceived duration. Each experimental block also contained four additional trials: two additional control trials in which the control stimulus was displayed for 1500 ms and two 1500-ms pain trials. In these pain trials, the visual stimulus (shape or triangle) previously associated with pain in the learning phase was presented for 1500 ms, and for the final 300 ms of stimulus presentation, pain stimulus was applied (as described above). Comparison of estimates given in these trials enabled examination of the effect of pain experience on temporal perception. A single 1500 ms pain trial duration was used to ensure that participants continued to anticipate pain throughout all durations used in the shorter anticipation trials. In addition, each block also included six random duration trials. Their duration was drawn at random from a uniform distribution running from 50 ms to 1500 ms. Estimates of the duration of the random duration stimuli were collected as for the target stimuli, but these data were not analysed. Random stimuli were both control and anticipation trials. Random duration stimuli have previously been employed to prevent participants labelling stimuli as “short” and “long” (Ogden, Wearden, Gallagher, & Montgomery, 2011). Thus, in total, each block contained 20 trials: 5 anticipation trials, 7 control trials, 2 pain trials and 6 random duration trials. Within each block, the order of presentation of individual trials was randomised for each participant. A total of five blocks were presented giving a total of 100 trials (70 excluding random duration stimuli). No

800 600 400 Pain anticipated

200

Control 0 348

582 864 1183 Standard duration (ms)

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Figure 2. Mean verbal estimates (ms) plotted against the standard duration.

Table 1. The number of each trial type included in each timing block

Stimulus presentation duration (ms)

Control: Anticipation: Pain: + 52°C

242

455

767

1058

1296

1500

Random duration

1 1

1 1

1 1

1 1

1 1

2

3 3

2

Note: Trial order was randomised within each block. COGNITION AND EMOTION, 2015, 29 (5)

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Anticipation trials Figure 2 shows mean verbal estimates for the anticipation and control trials, plotted against the standard duration. Examination of Figure 2 reveals that stimuli associated with pain (anticipation trials) were judged as lasting for longer than stimuli not associated with pain (control trials) for all standard durations. A repeated measures ANOVA (analysis of variance), with within-subject factors of standard duration (242 ms, 455 ms, 767 ms, 1058 ms and 1296 ms) and condition (pain anticipated vs. control), revealed significant main effects of duration, F(4, 92) = 170.72, p < .001, g2p ¼ .88, and

condition, F(1, 23) = 26.39, p < .001, g2p ¼ .53. There was also a significant interaction between duration and condition, F(4, 92) = 5.45, p < .001, g2p ¼ .18. Post hoc tests (Bonferroni corrected) showed significant (p < .001) differences in estimates for all but the shortest standard duration (p = .064). To explore this interaction further, and to examine whether the differences in estimates for the control and anticipation conditions were multiplicative (slope) or additive (intercept), individual linear regressions were conducted on the mean verbal estimates produced by each participant for each condition. Figure 3 shows the slope

1 0.8

Slope

0.6 0.4

Anticipation Control

0.2

Difference 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 –0.2 –0.4

Participant

500 400

Intercept

300 200 Anticipation

100

Control

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

Difference

–100 –200 –300

Participant

Figure 3. Upper panel: Individual data for the slope values for the anticipation and control conditions and the difference between the two (anticipation slope, control slope). Lower panel: Individual data for the intercept values for the anticipation and control conditions and the difference between the two (anticipation intercept, slope intercept).

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(upper panel) and intercept values (lower panel) for the anticipation and control conditions and the difference between the two (anticipation, control) for each participant. Slope values were significantly steeper in the pain-anticipated condition (M = .71, SD = .21) than the control condition (M = .67, SD = .22), t(23) = 3.58, p < .05, g2p ¼ .18. Greater slope values in the anticipation than control conditions were given by 71% of the participants. Intercept values were significantly greater in the pain-anticipated condition (M = 99.04, SD = 156.81) than the control condition (M = −8.06, SD = 125.91), t(23) = 2.02, p < .001, g2p ¼ .38. Greater intercept values in the anticipation than the control condition were given by 79% of the participants. Comparison of the effect size for the slopes and intercepts confirms that pain anticipation had a greater effect on intercepts than slopes. The accuracy of estimates was calculated for each duration in each condition; [(estimate − standard duration)/standard duration × 100]. Mean accuracy was then calculated for each participant. Participants underestimated the duration of stimuli in the pain-anticipated (M = −12.99%, SD = 21.23) and control conditions (M = −34.90%, SD = 15.56). A paired samples ttest revealed that estimates were significantly more accurate in the pain-anticipated condition than the control condition, t(23) = 4.49, p < .001. To explore the relationship between fear of pain and perceived duration, the slope and the intercept of the verbal estimate functions were correlated with the PCS and the VAS scores using Spearman’s rho. A significant negative correlation was observed between slope values for the painanticipated condition and PCS scores (r = −.49, p < .02). There was also a significant negative correlation between self-reported pain-induced distress and intercept values in pain-anticipated trials (r = −.43, p < .05). There were no other significant correlations. Greater fear of pain and distress from pain were therefore associated with flatter estimate gradients and reduced intercepts when pain was anticipated. 1

Pain trials Participants gave longer estimates of duration for pain trials (M = 1119.28 ms, SD = 282.18) than control trials (M = 981.26 ms, SD = 220.26). A paired samples t-test confirmed that this difference was significant, t(23) = 6.27, p < .001. Great duration estimates were given in the pain than control condition by 88% of the participants. Correlational analysis revealed a significant negative relationship between self-reported distress from pain and mean verbal estimates for pain trials (r = −.44, p < .05). Increased distress from pain was therefore associated with shorter duration estimates on pain trials. There was no significant correlation between the other VAS measures, or PCS scores, and perceived duration.

DISCUSSION The results of this study show that both pain and the anticipation of pain alter perceived duration. Estimates of duration were greater when participants were anticipating the arrival of pain, and when they actually experienced pain, than under control conditions. Pain resulted in a 14% increase in perceived duration, and the anticipation of pain resulted in a 35% increase in perceived duration.1 This supports the findings of previous studies showing that the duration of painful stimuli is overestimated relative to the duration of neutral stimuli of the same duration (Hare, 1963; Falk & Bindra, 1954). Although it is not possible to isolate exactly why our findings differ from Hellstrom and Carlsson (1997), who reported an underestimation of duration for painful stimuli, there are a number of possible explanations: in the current study, pain was induced through a temperature increase, and the durations judged were short (120 seconds). This raises the possibility that pain induced through increases and pain induced

Average percentage difference between estimates given for each duration in the pain and anticipation conditions. COGNITION AND EMOTION, 2015, 29 (5)

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through decreases in temperature have different effects on duration perception, as has been demonstrated with increases and decreases in core body temperature (see Wearden & PentonVoak, 1995, for review). It also raises the possibility that when pain is experienced for multiple minutes, rather than multiple seconds, differential effects on timing are observed, perhaps because longer exposures to pain result in adaptation to the pain stimulus. The significant overestimation of duration for pain-related stimuli relative to control stimuli also confirms previous findings from studies using auditory and visual stimuli that induce fear (Gil & Droit-Volet, 2011, 2012) and the anticipation of fear (Droit-Volet et al., 2010). The fact that, in the current study, emotional modulation of timing occurred when participants were judging the duration of abstract stimuli, with a high degree of similarity between the pain-related and neutral conditions, suggests that the effects previously observed with auditory and visual stimuli are not a consequence of idiosyncratic differences in the stimuli employed in the emotional and control conditions. Comparison of the lengthening effect observed in this study with that obtained with visual images suggests that pain has a greater effect on perceived duration than visual induction of fear. Anticipation stimuli were judged to be 35% longer than the control stimuli (g2p ¼ 0.53). When visual stimuli are used, smaller increases in duration are typically observed: Gil and Droit-Volet (2012) reported that high-arousal disgust images were judged to be 20% longer in duration than neutral images, and the high-arousal fear images were judged to be 6% longer than the neutral images. Angry faces were judged to be approximately 5% longer than neutral images in Gil and DroitVolet (2011). Pain is therefore an effective way of inducing temporal distortion. This may be because, as suggested by Craig (2009), its experience produces activation in areas such as the anterior insular cortex which are known to be activated during temporal perception. Concurrent activation of the anterior insular cortex from pain anticipation or experience and temporal perception may therefore lead to a longer perception of duration.

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Within the framework of internal clock theory, longer perceived durations for negatively valenced stimuli are typically interpreted as a result of arousal-induced increases in internal clock speed (see Gil & Droit-Volet, 2012, for discussion). This is because comparison of the slope of response gradients for fear and neutral conditions suggests that the effect of fear is multiplicative, i.e., it is greater at longer durations than shorter durations. Attentional change is not thought to be causal. In the current study, slope values were greater in the pain-anticipated condition than the control condition, indicating that the anticipation of pain increased arousal leading to an increase in internal clock speed. Interestingly, however, there was also a difference in the intercept of the gradients for the pain-anticipated and control conditions; intercept values were greater in the pain-anticipated condition than the control condition. Differences in intercept indicate an additive effect on timing, i.e., constant across durations, and are therefore usually interpreted as indicating differences in switch latency (Wearden et al., 2010). The presence of an intercept difference suggests that the effect of pain and its anticipation were in part due to more rapid orientation to painrelated stimuli. This resulted in more rapid switch closure at the start of the to-be-timed event leading to greater accumulation and a longer perceived duration. Indeed, the greater effect of pain anticipation on intercepts (g2p ¼ .38) than slopes (g2p ¼ .18) suggests that pain anticipation had a greater effect on attentional mechanisms in timing than arousal/pacemaker mechanisms. This supports previous suggestions that attention and arousal are working together to produce the effects observed rather than in isolation (Burle & Cassini, 2001; Ogden, 2013; Wittmann 2009). One obvious question is why painful stimulation, but not negative fear-inducing auditory and visual stimulation, would produce attentional effects on timing. Emotion-induced attentional effects on timing have previously been observed using visual stimuli, however only when the stimuli were of low arousal (Angrilli, Cherubini, Pavese, & Manfredini, 1997). Here, Angrilli et al. (1997) suggested that low-arousal negative images

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required larger amounts of information processing, detracting attention away from timing resulting in a shorter perceived duration. Such a mechanism cannot explain the overestimation observed in the current study. Instead, it is suggested that the high threat value of pain and cues indicating its imminent arrival means that such cues capture attention rapidly (Ecceleston & Crombex, 1999; Van Damme et al., 2004). In the current study, this enabled rapid orientation to the start to the to-be-timed event, rapid switch closure and a resulting longer perceived duration. Pain may have been more likely to facilitate attentional processing during timing because the experience and anticipation of pain activate the amygdala (Bornhovd et al., 2002), part of a specialised neural circuitry responsible for enhanced “emotional attention” (Vuilleumier, 2005). Indeed, Yiend (2010) suggests that for emotional effects on attention to be observed, the threat level must be “sufficiently high”. Thus, the role of attention in the timing of emotional stimuli is perhaps more evident in this study because pain is a more effective way of inducing threat than visual and auditory stimulation. It is noteworthy that the perceived duration of all stimuli was underestimated relative to their actual duration. Consequently, the lengthening effect produced in the anticipation and pain conditions actually resulted in more accurate perceptions of duration than in the control conditions. Global underestimation of duration and increased accuracy for fear-inducing stimuli were also observed by Mella et al. (2011) when exploring the effect of emotional sounds on perceived duration. Mella et al. (2011) suggest that this perhaps reflects an emotional advantage for perception and cognition aiding processing. The attention-grabbing nature of pain (Eccleston & Crombez, 1999) and anticipated pain (Van Damme et al., 2004) may therefore have also enhanced the processing of duration, leading to more accurate estimations. Although pain and anticipation of pain both led to longer, more accurate estimates of duration, in pain trials this effect may have been driven by the anticipation of

impending pain, rather than the experience of pain itself. Although pain and its anticipation lengthen perceived durations of time, greater pain-induced distress was associated with shorter estimates. Distress, as measured by the PCS and VAS, correlated negatively with slope and intercept values for anticipation trials. Distress as measured by VAS also correlated negatively with perceived duration in pain trials. Sullivan, Rouse, Bishop, and Johnston (1997) suggest that pain catastrophisers may be impaired in diverting their attention away from thoughts about pain to other activities. Being highly distressed by pain may therefore have resulted in shorter perceived durations because pain-related distress, and thoughts about future pain, may have diverted attention away from monitoring perceived duration. This is consistent with Zakay and Block’s (1997) Attentional Gate Model, a proposed modification of switch operation in SET, which suggests that timing and other cognitive activity compete for attentional resources. When insufficient attention is paid to time, perhaps because attentional capacity is exceeded by another task, for instance catastrophising about future pain, the attentional gate is closed and pacemaker output is not transferred to the accumulator. This results in a shorter perceived duration. This theory is consistent with Angrilli et al.’s (1997) suggestion that when viewing emotional material, shorter perceptions of duration can result if attention is detracted from timing. The presence of attentional effects resulting in the lengthening and shortening of perceived duration highlights the bidirectional way in which attention can influence temporal perception.

LIMITATIONS In the current study, we did not directly assess whether participants were implicitly or explicitly aware of the association between the abstract cue (square or triangle) and the experience of pain following the learning phase. The absence of a manipulation check following the learning phase COGNITION AND EMOTION, 2015, 29 (5)

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and again at later points in the experiment means that it is possible that the strength of the association between the abstract visual cue and the experience of pain may have changed over the course of the experiment. This in turn may have affected responding across the experiment. Similarly, there was a greater proportion of pain trials in the learning phase than in the testing phase of the experiment. This may have weakened the strength of the association between the cue and pain over the course of the experiment. Future research should aim to assess how association strength influences duration judgements in this context, perhaps through the use of implicit measures of association strength such as physiological measures of arousal. Such an approach would also allow direct examination of the relationship between physiological arousal and perceived duration. A further limitation of the current study was that only a single duration, 1500 ms, was used for pain trials. Consequently, it was not possible to explore whether the experience of pain had consistent effects on different duration ranges or whether the effects were additive or multiplicative. Additionally, it is possible that the use of a single pain stimulus duration, which was longer than the stimulus durations employed in the anticipation condition, may have biased participants to believe that the likelihood of pain increased as cue presentation duration increased. Such a belief may have led to greater increases in arousal as stimulus duration increased. Future research should therefore explore the effect of pain on a range of duration judgements.

CONCLUSION This study demonstrates that pain and the anticipation of pain alter perceived duration. This confirms that the effects of negative affect (e.g., fear and threat) on timing, previously observed with auditory and visual stimuli, generalise to somatosensory stimulation such as pain. Interestingly, the overestimation of perceived duration observed appears to be the result of a combination of increased arousal and enhanced attention to stimuli associated with

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pain, leading to longer and more accurate estimates of duration. This further emphasises the importance of exploring attentional and arousal mechanisms in distortions to the perceived duration of time. Manuscript received 13 November Revised manuscript received 26 June Manuscript accepted 8 August First published online 5 September

2013 2014 2014 2014

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