Cold Pressor Pain Reduces Phobic Fear but Fear Does Not Reduce Pain by Stuart Derbyshire | Papers by Stuart

ARTICLE IN PRESS The Journal of Pain, Vol -, No - (-), 2009: pp 1-7 Available online at www.sciencedirect.com Cold Pressor Pain Reduces Phobic Fear but Fear Does Not Reduce Pain Gregory J. S. Hollin and Stuart W. G. Derbyshire University of Birmingham, School of Psychology, Edgbaston, Birmingham B15 2TT, United Kingdom. Abstract: Negative emotion has a variable effect on pain perception. This variability has been explained by the motivational priming hypothesis (MPH) which predicts that emotional stimuli generating low levels of arousal will facilitate pain, while stimuli generating high levels of arousal will inhibit pain. However, a study by Sneddon et al with rainbow trout discovers a relationship not found in the human literature, that fear-related behavior decreased in the presence of a nociceptive stimulus. The current experiment examined this possibility in humans. In Experiment 1, 30 healthy, female subjects with ‘‘at least a mild aversion to spiders’’ participated in 3 trials: 1 in which a Brazilian salmon pink tarantula was present; a second with the right hand immersed in a cold pressor; and a third with both the tarantula and the cold pressor present. Experiment 2 added distance as an extra variable to this methodology. In both experiments it was found that spider presence had no impact upon pain perception but spider fear was reduced by the cold pressor. There was no interaction between trial and either time or distance. These findings are novel in human subjects and not well accounted for by the MPH. We suggest that an explicitly evolutionary framework should be adopted, and that spider fear was reduced to facilitate escape from the more threatening cold-pressor experience. Perspective: This study examined the relationship between pain and fear. Subjects with an aversion to spiders sat next to a tarantula with their right hand in iced water. Subjects reported reduced fear but no change in pain. Consequently, the authors reevaluate the Motivational Priming Hypothesis and emphasize evolutionarily determined threat values. ª 2009 by the American Pain Society Key words: Attention, nociception, evolution, fish, spiders, phobia. T he extent to which fear might influence pain and pain might influence fear is of considerable interest.3 It has been suggested that fear and pain may be part of a larger behavioral framework—the aversive system—intended to ensure survival by avoiding danger.20,28 It has been shown that behaviors within the aversive system, including pain and fear, elicit similar physiological responses and share neurological and psychological function.5,21,25 Within this framework there is likely to be competition for influence and resources.4,27 The relationship between pain and fear is variable and complex, with different responses reported under different conditions. Pictures of negative events that evoke fear, disgust or anxiety create hyperalagesia.8,19,22 In vivo exposure to a stimulus that evokes fear, disgust or anxiety, however, creates analgesia.3,17,26 These differ- Received November 14, 2008; Revised March 13, 2009; Accepted March 26, 2009. Address reprint requests to Dr. Stuart Derbyshire, University of Birmingham, School of Psychology, Edgbaston, Birmingham B15 2TT, United Kingdom. E-mail: s.w.derbyshire@bham.ac.uk 1526-5900/$36.00 ª 2009 by the American Pain Society doi:10.1016/j.jpain.2009.03.015 ences in pain responses have been accounted for using the motivational priming hypothesis (MPH),20,27,34 which describes emotions as differing in valence and arousal. The MPH proposes that in a low valence-low arousal state such as when viewing a picture of a phobic object, pain facilitation occurs. In contrast, in a low valence-high arousal state such as when directly encountering a phobic object, pain inhibition occurs. In 2003, however, Sneddon et al31 demonstrated a complex behavioral response to nociceptive stimuli in the rainbow trout (Oncorhynchus mykiss) different to those reported in human studies, and conceivably at odds with the MPH. Trout were exposed to both a novel object shown to induce fear-related behavior, and to an acid shown to cause nociceptive behavior. It was found that, when stimuli were presented together, there was a substantial reduction in fear-related behavior but no significant change in nociceptive related behavior. Sneddon et al31 suggested 2 explanations. First, they suggested that rainbow trout do not have the cognitive capacity to respond to multiple stimuli simultaneously. This could potentially lead to a behavioral response quite different to that expected in humans. Second, they suggested that a ‘‘danger hierarchy’’ may be formed on the 1 ARTICLE IN PRESS 2 basis of threat values, in which the most dangerous, salient stimuli dominate attention to the detriment of any others. Such a relationship would be evolutionarily guided to promote survival. Humans and rainbow trout have similar nociceptors30 and, some have argued, similar brain regions necessary to process noxious information.9 It is possible, therefore, that a similar ‘‘danger hierarchy’’ will operate in humans as the result of a common ancestry with fish. This speculation does have some empirical support. Janssen and Arntz15 found no evidence of altered pain perception in spider phobics when pain was experienced in the presence of a spider, replicating the lack of phobic influence on nociceptive behavior reported by Sneddon et al.31 Janssen and Arntz15 were researching opioid-mediated analgesia, however, and were therefore not concerned with changes in fear. Thus, any changes in fear were left unrecorded. This follows a trend in the literature, with studies of pain and emotion, in general, failing to record the influence of pain on emotion.1,2,3,8, 15-17, 19, 22, 26 Here we describe 2 studies that combine important elements of the research described by Janssen and Arntz15 and Sneddon et al.31 Experiment 1 examines both pain and fear experiences when human subjects with ‘‘at least a mild aversion to spiders’’ are simultaneously presented with a tarantula and cold-pressor pain. Experiment 2 extends this investigation to examine changes in fear and pain as the tarantula is relocated closer or further from the subject. According to the MPH, the presence of an actual spider should reduce pain experience whereas, according to an evolutionary ‘‘danger hierarchy’’, the presence of the pain should, if subjects respond similarly to Sneddon et al’s trout, reduce fear of the spider. Pain and Phobic Fear Figure 1. A subject completing the SP trial. Image used with permission of the subject. water temperature was maintained at 4 C (61 C) according to standard procedures.13,36 The spider was a juvenile of the poisonous species Lasiodora parahybana (Brazilian salmon pink tarantula) and was approximately 15 centimeters in length and 10 centimeters in width. The spider was always completely encased in a small transparent carrying case (see Fig 1). Subjects were informed that the spider could kick off urticating hairs if annoyed and had the potential to deliver a bite. Design A within-subjects factorial design was employed with the presence and absence of the spider and cold pressor as the factors, and the ratings of fear and pain as the dependent variables. Fear perception was assessed via ratings on an 8-point numerical rating scale (0–7) of current fear of the spider. Pain intensity and unpleasantness were assessed using verbal descriptor scales.10,11 Zero was anchored with no sensation for the intensity scale and neutral for the unpleasantness scale and 20 was anchored with maximum intensity and maximum unpleasantness. Gracely et al10 report excellent reliability with a correlation across experiments of r = .99 for both scales. The order of conditions was counterbalanced across subjects and was included as an additional between-subjects factor for the data analysis. Methods Experiment One Subjects All procedures were approved by the University of Birmingham School of Psychology ethics committee. Work with invertebrates does not require a UK government license or other special permit. The 2 spiders employed for the study were only handled by qualified animal technicians at the University of Birmingham Biosciences Department. The spiders were provided to the experimenters in an appropriate transparent carry case and returned in the same case at the end of each study period. Thirty-four right-handed subjects provided written, informed consent and 30 subjects (all female, mean age 21 years, range 19–34) completed the study. All subjects reported having ‘‘at least a mild aversion to spiders’’ and were free from any clinical-pain disorder. Three subjects withdrew because they found the cold pressor too painful and 1 subject withdraw because they could not tolerate sitting next to the spider. Procedure Prior to the onset of any experimental procedures, all subjects were verbally informed that the spider was not in the room and that it would never be in the room without their knowledge. The absence of the spider was emphasized to reduce any spider-induced anxiety during the nonspider trials. All subjects initially completed the Fear of Spiders Questionnaire (FSQ)32 to assess global spider fear. All subjects were shown the Gracely scales, and the difference between intensity and unpleasantness scales was explained with general examples, although no indication of a specific sensation associated with the cold pressor was given. Subjects were made aware that they were permitted to ask for the removal of the spider or the cold pressor at any point during the experiment. Apparatus The cold pressor consisted of a 10-liter bucket half filled with ice and topped up with cold tap water. The ARTICLE IN PRESS Hollin and Derbyshire Subjects were also made aware that this would result in the termination of the experiment, which could not continue in the absence of either stimulus. The experiment was composed of 3 separate trials performed in a counterbalanced order: (1) pressor alone (PA); (2) spider alone (SA); and (3) spider and pressor concurrently (SP). The PA condition lasted for 5 minutes, during which time subjects placed their right hand into the pressor. After 30 seconds, subjects were asked to give pain ratings on the Gracely scales (hence referred to as PA1) using their left hand. A second set of Gracely scales were completed after 5 minutes (PA2) and then subjects removed their hand from the pressor and were able to dry and warm their hand. The SA trial lasted for 2 minutes while subjects sat with the encased spider on a table in front of them. The spider was brought into the room covered by a towel; the timing of the condition started upon the removal of this cover. Although the spider could not be physically touched, it was always placed well within the reach of the subject. After 30 seconds the subject was asked to rate their current fear of the spider (SA1) by circling a number between 0 and 7 on the rating scale. A second rating scale was completed after 2 minutes (SA2) and the spider was then covered and removed from the room. As in the PA condition, during the SP condition subjects placed their right hand in the cold pressor for 5 minutes; however, the spider was also in place on the table in front of them during this trial (see Fig 1). As in the SA condition, timing started upon the removal of the spider’s cover. Subjects completed the Gracely scales and the fear rating scale after 30 seconds (SP1) and again after 5 minutes (SP2). At least 10 minutes separated each trial to enable the subject to relax after the removal of the spider and to enable the right hand to return to normal following the pressor trials. 3 reveal one as obviously more poisonous or dangerous than the other. Design A within-subjects factorial design was employed with the presence and absence of the spider, distance of the spider from the subject, and the presence or absence of the cold pressor as the factors. The ratings of fear and pain were the dependent variables and were measured as before. Procedure The procedure contained the same trials (SA, PA, and SP) as Experiment 1 but the SA condition was increased to 5 minutes for better comparison with the other trials. Also, to control for carryover effects, a 60-second wordgeneration task was introduced between each trial. This was a filler task and results were not recorded. Subjects rated their fear and/or pain intensity (pain unpleasantness was not recorded) as each trial began and then rated both again every 20 seconds throughout each trial. The table directly in front of the subject was marked at 50-centimeter intervals (0 cm, 50 cm, 100 cm, 150 cm, and 200 cm). At the start of a fear trial, the spider was uncovered at either the 200-cm distance or at 0 cm directly in front of the subject. This starting position was counterbalanced across subjects. A fear rating was taken immediately and every 20 seconds for a total of 5 minutes. After each minute, the spider was moved 50 cm towards or away from the subject. Results Experiment One The average FSQ score was 71.2 (SD = 20.7). This score is lower than that reported in clinically diagnosed arachnophobics (eg,23 mean = 89.1, SD = 19.6) but considerably higher than that reported in nonphobics (mean = 3, SD = 7.8).23 Experiment Two Subjects Thirty-one right-handed subjects who had not participated in Experiment One provided written, informed consent and 30 (26 female, mean age 19 years, range 18–26 years) completed the study. All subjects met the same requirements as for Experiment One. One subject withdrew due to fear of the spider. Pain Scores Fig 2 illustrates that pain intensity and pain unpleasantness did not differ significantly across condition or time. Critically there was no main effect of spider presence on pain intensity (F1,29 < 1) or unpleasantness (F1,29 < 1) ratings. There were also no significant main effects of time of rating, order of presentation or interactions between condition and time of rating or order of presentation. Apparatus The cold pressor was as before. Due to availability, a comparably-sized adult Mexican redknee tarantula (Brachypelma smithi) was used instead of the salmon pink tarantula. The spider was housed in the same box as for Experiment One. The redknee tarantula is less venomous than the salmon tarantula but can still kick urticating hairs from its abdomen and deliver a bite. Subjects were not explicitly informed as to the relative danger posed by the redknee compared with the salmon tarantula and casual observation of the spiders does not Fear Scores Fig 3 shows a reduced fear of the spider when it was presented with the cold pressor both after 30 seconds (SP1, mean = 3.8, SD = 2.2; SA1, mean = 4.4, SD = 2.2), and at the second fear rating (5 minutes SP, 2 minutes SA) (SP2, mean = 3, SD = 2.3; SA2, mean = 3.5, SD = 2.2). A within-subjects 2-way ANOVA revealed a significant main effect of pain on fear ratings (F1,29 = 11.1; P < .05). There was also a main effect of time as subjects reported lower fear ratings on the second presentation of the spider (F1,29 = 33.6; P < .05); there was, however, no ARTICLE IN PRESS 4 Pain and Phobic Fear Figure 3. Fear ratings on an 8-point numerical rating scale in the presence (SP) and absence (SA) of the cold pressor. Error bars show standard deviations. Fear Scores Fear of the spider gradually reduced with time, with mean fear scores at the first time rating (SP condition = 3.9, SD = 2.3; SA condition = 4.3, SD = 2.4) noticeably higher than those at the last (SP condition = 2.5, SD = 2.5; SA condition = 3.1, SD = 2.8). This effect of time approached significance (F1.3,37.8 = 3.4, P = .06). As can be seen from Fig 6, fear with the cold pressor was rated lower than fear without the cold pressor at every time point. This main effect was significant (F1,29 = 4.8, P < .05) and there was no interaction of condition with time. Fear of the spider also reduced as the distance between the subject and the spider increased, with mean fear ratings substantially higher when the spider was directly in front of the subject (SP condition = 4.6, SD = 1.8; SA condition = 5.3, SD = 1.9) than when it was placed 2 meters away (SP condition = 1.6, SD = 1.9; SA condition = 2.3, SD = 2.3). This effect was highly significant (F2.4,69 = 67, P < .05). As can be seen from Figure 2. The difference in perceived pain intensity (top) and unpleasantness (bottom) in the presence (SP) and absence (PA) of the spider. Error bars show standard deviations. significant interaction between trial and time (F1,29 < 1). There was no main effect of the order of spider presentation on fear ratings but there was a significant interaction of order with the cold pressor (F 5,24 = 6.5; P < .05) as illustrated in Fig 4. Fear was disproportionately reduced by the cold pressor when the spider was first seen alone. Experiment Two The average FSQ score was 79.7 (SD = 20.8), an independent-samples t-test revealed that this group was not significantly different for those that took part in Experiment One (t (52) = À1.48, P >.05). Pain Scores When collapsed across time, the cold pressor was perceived as more painful when presented alone (mean = 13.7, SD = 3.4) than when it was presented concurrently with the spider (mean = 13.1, SD = 4.1). However, a 2-way within-subjects ANOVA found no significant difference (F1,29 = 1, P = > .05) between the trials. As can be seen from Fig 5, there was a significant effect of time (F1.6, 45.7 = 4.8, P = < .05) with pain scores increasing until around 1.5 minutes, before slowly decreasing again. This pattern was similar in both trials, however, and there was no significant interaction between time and presence of the spider (F2.2, 62.9 = 1.3, P = > .05). Figure 4. The interaction of the cold pressor with the order of spider presentation on fear ratings. Error bars show standard deviation. ARTICLE IN PRESS Hollin and Derbyshire 5 Figure 5. Changes in pain intensity rating over time with and without the presence of the spider. Error bars show standard deviation. Fig 7, fear with the cold pressor was rated lower than fear without the cold pressor at every distance. This main effect was significant (F1,29 = 6.5, P < .05) and there was no interaction of condition with distance. Figure 7. Changes in fear rating across distance with and without the cold pressor (pain). Distance from the subject is shown on the X-axis in cm. Three measures of fear were taken at each distance. Error bars show standard deviation. Discussion The present study examined the relative experiences of pain and fear during the simultaneous induction of pain and spider fear. The findings suggest that the induction of spider fear has no significant impact on pain experience from a standard noxious source. Fear responses, however, were significantly inhibited when the spider was presented during pain experience. This inhibition was maintained regardless of whether the fear was increased during immediate and close proximity of the spider or reduced by time and distance. The lack of any change in pain perception during the successful induction of fear is perhaps surprising and requires some explanation. One possibility is that the spider induced no negative emotions (ie, fear or anxiety) in the subjects during the spider trials and therefore no change in pain experience occurred. A related possibility is that the subjects simply ignored the spider. Both these suggestions are unlikely because the subjects continued to rate the spider as fearful during the pain trials. Further, predictable changes in fear as distance from the spider was altered in Experiment Two suggest that Figure 6. Changes in fear rating over time with and without the cold pressor (pain). Error bars show standard deviation. the spider was not merely a distraction but also evoked fear; this fear diminished in appropriate fashion as distance increased. Our findings are also consistent with those of Arntz et al,1,2,14-16 who failed to find evidence of stress-induced analgesia with arachnophobic subjects undergoing similar procedures. As noted previously, these findings have also been reported in similar scenarios using fish.31 The reports of similar findings in fish suggest the possibility that fear reduction during noxious stimulation is an evolutionary adaptation. The compulsion to escape sensations of fear and pain was recognized by Darwin as evolutionarily adaptive,7 and an evolutionary basis behind phobias has been considered for several decades29 with continued support today.24 While the MPH seems to evoke an evolutionary explanation on some level, the detail is scarce. Adopting a more transparently evolutionary perspective means that there should be at least some examination of the survival value of the fear and pain responses. In this instance, the spider is unlikely to be considered a significant bodily threat; both because it was necessarily behind a physical barrier, and because its removal could be instigated by the subject, a factor that has previously been demonstrated to reduce stimulus related anxiety.38 We therefore hypothesize that the need for the spider to dominate attention to the detriment of pain—as has been found in animals presented with a predator12,18— is minimal. Similarly, the spider is unrelated to the pain currently being experienced and the spider is therefore not providing useful information about the pain experience. Consequently, there is no reason why the spider should change pain perception from the cold pressor. The intense, novel pain is a more-pressing problem and so pain dominates attention to the detriment of spider fear in this instance. The hypothesis that threat values may explain the current findings is the same as that made by Sneddon et al31 to explain their results with rainbow trout. Indeed, the suggestion that threat values—directly evolutionary in origin or otherwise—are of importance in determining the response to pain has been stressed previously.6,33,35 That threat values are of importance in determining the nature of the response when fear and pain were ARTICLE IN PRESS 6 presented concurrently would require further research, although previous models have suggested such an impact.4 Subsequent research might alter the relationship between the aversive stimuli and the threat value of the fear-inducing stimulus. This could be done by utilizing a nonfearful control group by means of comparison, or by altering the fear-inducing stimuli. If responses are very stimulus specific, then changing spider species may be important, especially if the relative danger of the spiders is explained. For the current study, the subjects were not specifically informed of the relative danger posed by the specific spider used and generally accepted the ‘‘dangerous’’ nature of the spider. There were no obvious differences in subject responses to the spider used for Experiment One relative to the spider used for Experiment Two. Clearly the relationship between fear and pain is complex and dynamic and the MPH is 1 way to summarize the complexity. The findings of the current study, however, may not be borne out by the MPH. The MPH implies that emotion will influence or prime pain and tends to neglect the effect that pain might have upon emotion. Indeed, it is the authors’ opinion that the title of the MPH is itself potentially misleading, suggesting that motivational states are able to influence but not be influenced; they are priming and not primed. The current experiment demonstrates that this is not the case. One limitation of Experiment One is the comparison between fear at 2 minutes (SA) and 5 minutes (SP); given that spider fear could conceivably decrease significantly in the 3 minutes after the SA2 ratings, this comparison is problematic. This problem was rectified for Experiment Two, however, and similar results were found. A second limitation is the incomplete counterbalancing in Experiment Two. While the nearest and furthest spider locations were counterbalanced, the position of the spider changed in a linear fashion (near to far, or far to near) from this starting point. The middle distances are not therefore completely counterbalanced. This does not afPain and Phobic Fear fect the findings at the nearest or furthest distances. A final limitation is the presence of order effects that might have been more elegantly managed. Fig 4 demonstrates that when the cold pressor was introduced after seeing the spider alone, there was a disproportionate drop in fear of the spider; we hypothesize that this an habituation effect. Future studies might consider procedures to control for potential habituation or sensitization to the spider, as has been done with other fearinducing stimuli.35 Despite this potential limitation, the within-participants methodology used here is consistent with the literature in this field.1,14,15 It should also be noted that the current study was conducted with a specific sample (almost entirely young women) with a specific fear and may therefore not be generalizable, even to others with a fear of spiders. If evolutionary factors are as important as hypothesized, then it is quite possible that the subjects themselves may be important in determining the findings. Age, gender and personality values may all be crucial factors in determining threat value. The current study demonstrates that pain can reduce fear directed towards an unrelated, aversive stimulus. The findings of the MPH leave no doubt that levels of arousal and valence are defining factors in predicting the interaction between negative emotions and pain perception. However, other evolutionarily relevant variables such as the relatedness of the stimuli and the nature of the fearful stimulus may be important determinants or prerequisites in the relationship.37 Research into the relationship between pain and emotion should also take into account the effect of pain upon emotions. Acknowledgments Thanks to Jody Laronde for additional data collection and for comments and ideas relating to an earlier version of the manuscript. Thanks also to Peter Jones and Professor Jeff Bale in Biosciences for providing the spiders. 8. De Weid M, Verbaten MN: Affective picture processing, attention, and pain tolerance. Pain 90:163-172, 2001 9. Dunlop R, Laming P: Mechanoreceptive and nociceptive responses in the central nervous system of goldfish (Carassius auratus) and trout (Oncorhynchus mykiss). J Pain 6: 561-568, 2005 10. Gracely RH, McGrath F, Dubner R: Ratio scales of sensory and affective verbal pain descriptors. Pain 5:5-18, 1978 11. Gracely RH, Dubner R: Reliability and validity of verbal descriptor scales of painfulness. Pain 29:175-185, 1987 12. Hendrie CA: The calls of murine predators activate endogenous analgesia mechanisms in laboratory mice. Physiol Behav 49:569-573, 1991 13. Hilgard ER: The alleviation of pain by hypnosis. Pain 1: 213-231, 1975 14. Janssen SA, Arntz A: Anxiety and pain: attentional and endorphinergic influences. Pain 66:145-150, 1996 15. 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