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Sex Differences and Incentive Effects on Perceptual and Cardiovascular Responses to Cold Pressor Pain

From the Department of Psychology, University of Alabama at Birmingham (D.L., R.A.W.); and the Department of Operative Dentistry, University of Florida and Gainesville VA Medical Center (R.B.F.), Gainesville, Florida.

Address reprint requests to: Roger B. Fillingim, PhD, University of Florida College of Dentistry, Public Health Services and Research, 1600 SW Archer Road, Room D8-44A, PO Box 100404, Gainesville, FL 32610-0404. Email: rfillingim{at}dental.ufl.edu

	ABSTRACT

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OBJECTIVE: Sex differences in pain perception have been widely reported, with women typically displaying greater pain sensitivity than men, but the mechanisms underlying these differences remain unclear. One possible explanation suggests that men are more motivated to tolerate and suppress expressions of pain because of the masculine sex role, whereas the feminine sex role encourages pain expression and produces lower motivation to tolerate pain among women.

METHODS: To examine the influence of motivation on perceptual and cardiovascular responses to pain among women and men, different levels of monetary incentive (high vs. low incentive) were provided to a group of 81 healthy young adults undergoing the cold pressor pain procedure. It was anticipated that men would have greater endogenous motivation and would therefore be less affected by the external incentive.

RESULTS: Men had higher pain thresholds and tolerances and lower pain ratings than women, but the incentive condition produced no significant effect on pain responses. Resting blood pressure was positively correlated with pain tolerance among the low incentive group, whereas blood pressure reactivity to the cold pressor predicted pain tolerance in the high incentive group.

CONCLUSIONS: Thus, monetary incentive did not influence pain responses, but the relationship between cardiovascular measures and pain responses was influenced by the incentive manipulation. Potential explanations for the observed results are presented, and the implications for applying the biopsychosocial model to pain research are discussed.

Key Words: pain threshold, • pain tolerance, • sex differences, • incentive, • blood pressure.

Abbreviations: ANOVA = analysis of variance;; DBP = diastolic blood pressure;; FRIN = final rating of intensity;; HR = heart rate;; SBP = systolic blood pressure.

	INTRODUCTION

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Pain is a complex multidimensional experience influenced by physical, psychological, and social factors. In recent years sex differences in responses to pain have received increased attention. Multiple studies have investigated sex differences in experimental pain perception using a wide variety of noxious stimuli. The evidence consistently suggests that women show greater perceptual responses than men to mechanical pain, ischemic pain, and cold pressor pain; the results of studies examining heat and electrical pain are less consistent (1, 2) . A meta-analysis revealed that studies of sex differences in pain threshold and tolerance show moderate to large effect sizes across multiple stimuli (2). In addition, sex differences have been reported for cardiovascular (3), autonomic (4), neuromuscular (5), and cerebral responses (6) to experimentally induced pain.

Multiple mechanisms have been proposed to explain the differing response to experimental pain between the sexes, including hormonal factors, differences in pain modulatory systems, and genetic factors (7–9) . From a more psychosocial perspective, another potential explanation for the sex difference in pain responses involves social role expectancies, in that the stereotypic feminine role is associated with increased willingness to report pain, whereas the masculine role is characterized by stoicism and diminished responses to pain. Otto and Dougher (10) reported a significant correlation between pressure pain thresholds and masculinity-femininity scores for men but not for women. However, the sex difference in pain threshold remained significant even after accounting for masculinity-femininity scores. Similarly, Myers et al. (11) recently reported that higher masculinity was associated with greater cold pressor pain tolerance but did not account for the sex difference. Levine and De Simone (12) found that men reported significantly lower cold pressor pain ratings when in the presence of a female vs. a male experimenter, whereas the sex of the experimenter did not affect women ’ pain ratings. These findings lend support to the influence of sex roles on experimental pain responses such that social role expectancies may cause men to be more motivated than women to tolerate and suppress experimentally induced pain. Thus, motivation may mediate the effect of sex roles on pain tolerance.

Several studies have investigated general motivational influences on experimental pain. These are relevant to a social role analysis insofar as sex roles may dictate how motivated men and women are to tolerate painful tasks. Cabanac (13) used a monetary incentive and found that subjects’ pain tolerance times increased linearly in relation to the logarithm of the amount of payment they received, suggesting that the monetary incentive influenced the subjects’ performance on the pain tolerance task. In another study, it was reported that providing specific quotas for pain tolerance performance increased subjects’ cold pressor pain tolerances, although the addition of monetary reinforcement did not produce an additional effect (14). Finally, Baker and Kirsch (15) found that both the cognitive coping instruction and monetary incentive increased pain tolerance. The monetary incentive was more effective, but the two strategies combined produced additive effects. Thus, incentives can increase pain tolerance.

In addition to its influence on task performance, motivation may increase task engagement or effort, and Obrist (16) has theorized that task engagement can affect cardiovascular responses. In support of this theory, several studies assessing cardiovascular responses to nonpainful stressors have indicated greater cardiovascular reactivity under conditions of high task engagement than low engagement (17–20) .

The current study was conducted to determine whether monetary incentive would differentially affect pain tolerance and cardiovascular responses to the cold pressor task in women and men. We hypothesized that incentive would produce greater effects among women because men possess high levels of endogenous motivation due to the demands of stereotypic male sex role. Similarly, it was hypothesized that greater effort, produced by the high incentive condition, would be associated with more robust heart rate and systolic blood pressure responses in women than men for the same reason. The decision to use monetary incentive was based on previous studies revealing that monetary inducements increase pain tolerance times (13, 15) .

	METHODS

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Subjects
Participants consisted of 39 female and 42 male undergraduate students at the University of Alabama at Birmingham. All participated to obtain class credit. Subjects were healthy adults free of any pain or other medical conditions. All procedures were approved by the university’s institutional review board.

General Procedures
On arrival, participants provided written informed consent and completed a health history questionnaire. After a 10-minute seated rest period, baseline blood pressures were taken every minute for 5 minutes by an automated blood pressure cuff (Dinamap SX1846, Critikon, Tampa, FL) placed around the subject’s left arm. Subjects were randomly assigned to incentive condition, resulting in cell sizes of 20 men and 19 women in the low incentive group and 22 men and 20 women in the high incentive group. Participants were randomly assigned to either a male or female experimenter, with approximately half of the participants assigned to each.

In the low incentive group, subjects were informed that they would receive 5 cents for every 15 seconds that they kept their hand submerged in the cold water. Participants in the high incentive group were informed that they would receive $1 for every 15 seconds that they kept their hand submerged. Subjects were told that the maximum time limit was 5 minutes; therefore, the maximum monetary rewards for the low and high incentive groups were $1 and $20, respectively. The maximum amount of money that participants could earn was placed in front of them during the cold pressor task for visual inspection, and they were informed that they would receive their reward immediately after the experiment.

After the instructions were given but before the cold pressor task, participants completed numerical ratings (from 0 to 10) of 1) pain expectancy ("How painful do you expect the cold water procedure to be?"); 2) predicted performance ("How well do you think you will be able to tolerate the cold water procedure compared with others your age?"); 3) total motivation ("How motivated are you to tolerate the cold water procedure for as long as possible?"); and 4) motivation other than from money ("How motivated would you be if there was no monetary reward?"). To derive an index of the extent to which the monetary incentive was a motivator, a difference score was computed by subtracting the response to question 4 (motivation other than money) from the response to question 3 (total motivation). Each question was answered on a 0 to 10 Likert scale.

After participants completed the questionnaire, the experimenter placed a countdown timer set for 30 seconds in front of the subjects and informed them that when the timer reached 0, they were to begin the cold pressor procedure. The experimenter informed the subjects that they should use the 30-second time period to mentally prepare themselves for the cold pressor task. During the 30-second countdown procedure, the experimenter recorded subjects’ blood pressure and heart rate as a measure of anticipatory cardiovascular reactivity.

After the cold pressor procedure, subjects completed the following questionnaire items: 1) stress rating ("How stressful was the cold water procedure?"); 2) performance appraisal ("How well do you feel you performed on the cold water procedure?"); 3) effort ("How hard did you try to tolerate the water as long as you could?"); and 4) monetary motivation ("During the cold water procedure, how much did the money motivate you to keep going?"). Because of the specific nature of the pre- and posttask questions, these instruments were developed for this study; therefore, reliability and validity data are not available for these measures. Additionally, after the cold pressor procedure, the McGill Pain Questionnaire was administered (21). This is a well-validated instrument used to assess pain. Subjects selected from a list of 78 adjectives those that best described their pain, and four subscales were computed: affective, sensory, evaluative, and miscellaneous.

Cold Pressor Procedure
The cold pressor procedure was chosen as the pain tolerance task for two reasons. First, sex differences in response to this procedure have been reported consistently (11, 22–24) . Second, the cold pressor procedure produces tonic pain that may be more amenable to the influence of incentive compared with brief pain tasks. The procedure was completed using a refrigerated circulating water bath (Neslab Instruments, Portsmouth, NH). The water temperature was maintained at 5°C, and the bath circulated the water to prevent local warming. Participants were instructed to place their right hand into the cold water up to their wrist and to leave it submerged until they were no longer able to tolerate the pain. Additionally, they were told to keep their hand open rather than closed in a fist while it was in the water. Several measures were taken during the procedure, including pain threshold, pain tolerance, and pain ratings. Participants were asked to rate their pain intensity on a combined verbal and numerical box scale (25, 26) ranging from 0 to 20 every 30 seconds while their hand was underwater. In addition, participants were asked to provide final pain intensity ratings at tolerance (FRIN), just before removing their hand from the cold water. Pain threshold was recorded as the time at which the subject first reported pain. Pain tolerance was defined as the length of time the participant’s hand remained underwater. Blood pressure and heart rate measurements were obtained each minute, starting 1 minute after the cold pressor procedure began. Subjects were informed that the cold pressor procedure would be stopped after 5 minutes if they had not reached tolerance.

Data Analysis
Descriptive data are presented as means and standard deviations unless otherwise indicated. Analysis of variance (ANOVA) was used to determine the reliability of group differences for continuous variables. The five baseline measures for each cardiovascular measure were averaged to produce a composite baseline score for systolic and diastolic blood pressure and for heart rate. Two cardiovascular reactivity indices (change scores) were computed. Anticipatory reactivity was computed by subtracting each baseline cardiovascular variable (systolic pressure, diastolic pressure, and heart rate) from the value obtained during the anticipatory period. Task-induced reactivity, the only time period during the cold pressor task for which all subjects had data, was calculated by subtracting the baseline value from the value obtained at minute 1 for the cold pressor task. No significant correlations between cardiovascular baseline and cardiovascular reactivity measures emerged; therefore, baseline values were not used as covariates. To explicate significant findings, t tests were used to analyze simple effects.

	RESULTS

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Demographics and Baseline Measures
Demographic information is shown in Table 1. Participants ranged in age from 16 to 53 with a mean age of 23 years. There were no overall group or sex differences in age (p > .10); however, women were older than men in the high incentive group but not in the low incentive group (p < .05). For this reason, age was used as a covariate in subsequent analyses. There were also proportionately more African American subjects among women than men, but this difference was not statistically reliable (p > .4).

View larger version (12K): [in this window] [in a new window]   Fig. 1. Mean (SEM) log-transformed pain tolerance for women and men in the high [] and low [] incentives groups. The sex difference was significant (p < .005), but no effect of incentive group emerged.

Pretask Questionnaire Data
Means and standard deviations for pre- and posttask questionnaire data are shown in Table 4. Participants in the high incentive group reported slightly but not significantly lower pain expectancy (p = .08) than subjects in the low incentive group. Men reported higher predicted performance scores compared with women, and the sex-by-incentive group interaction for predicted performance approached significance (p < .07). Inspection of the means revealed that high incentive women had higher predicted performance scores than low incentive women (p < .01), whereas high and low incentive men did not differ (p > .8). No sex or group differences in total motivation or motivation other than from money emerged (p values > .2); however, the high incentive group had higher values on the computed monetary incentive score (p < .05).

Posttask Questionnaire Data
After the cold pressor task, the high incentive group, compared with the low incentive group, reported higher performance appraisal and greater effort (p < .04), and subjects in the high incentive group reported greater monetary motivation compared with the low incentive group (p < .0001). No sex differences or interactions emerged for any of the questions (p values >0.15). Correlation analyses for posttask questionnaire data indicated that performance appraisal was positively correlated with pain threshold (r = 0.44, p < .0001) and pain tolerance (r = 0.71, p < .0001) in both groups. For high incentive subjects, reported effort was associated with FRIN scores (r = 0.39, p < .05), and monetary motivation was positively correlated with pain tolerance (r = 0.36, p < .05). For low incentive subjects, performance appraisal was negatively correlated with pain ratings at 30 seconds (r = -0.47, p < .005) and with FRIN (r = -0.50, p < .005), whereas effort was positively correlated with FRIN scores (r = 0.40, p < .05).

	DISCUSSION

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Our initial hypothesis predicted that incentive would produce greater effects in women than in men because men had greater endogenous motivation to tolerate pain because of the influence of the masculine sex role. These data provided no support for this hypothesis. Similar to previous studies of cold pressor pain (11, 22–24) , men had higher pain thresholds and tolerances than women; however, monetary incentive had no effect on pain responses in either sex. Similarly, women provided higher ratings of cold pressor pain 30 seconds into the task and on the posttask McGill Pain Questionnaire. Also, contrary to our hypotheses, cardiovascular responses to the cold pressor task were not affected by the monetary incentive manipulation. Thus, neither pain responses nor cardiovascular reactivity to the cold pressor was influenced by the level of monetary incentive.

Several possible explanations for this pattern of results can be offered. First, it is possible that the incentive actually produced the anticipated sex-related effect but our sample was too small to detect it. Inspection of the means suggests that this is unlikely, because the difference in pain tolerance between high and low incentive groups is actually larger for men than for women, with high incentive men having slightly longer tolerance times. Another possibility is that a ceiling effect prevented the hypothesized incentive effect from emerging. To address this possibility, the proportion of subjects reaching the cutoff time for the cold pressor in each group was computed. The numbers of subjects in each group were high incentive men (13 of 22, 59%), low incentive men (9 of 20, 45%), high incentive women (7 of 20, 35%), and low incentive women (7 of 19, 37%). Again these data suggest that if anything, there was a greater effect of incentive in men than women since the greatest number of subjects reaching the cutoff were in the high incentive male group.

Another possibility is that the incentive chosen was not sufficient to increase motivation in the high incentive group. However, this seems unlikely. Baker and Kirsch (15) demonstrated that incentive condition influenced female participants’ pain tolerance performance, and they paid subjects substantially less than in the current study, $2 for keeping their hand immersed in the ice water for 4 minutes and an additional dollar for each additional minute up to a maximum of 8 minutes. They found that subjects in this condition were able to significantly increase their pain tolerance times from baseline. Also, questionnaire data obtained before and after the cold pressor task indicate greater monetary motivation among high incentive subjects, and self-reported effort after the task was significantly greater in the high incentive subjects. Thus, both previous research and the self-report data obtained in the present study suggest that this incentive manipulation provided sufficient motivation to enhance effort. After the cold pressor task, high incentive subjects reported both greater effort and greater monetary motivation than low incentive subjects; however, the group difference was greater for monetary motivation than for effort. This suggests that factors other than money served to increase effort in the low incentive group, thereby reducing the disparity in effort between groups.

One of our hypotheses was that systolic blood pressure reactivity, considered an index of effort, would be affected by incentive, especially among women. The data indicated that systolic and diastolic blood pressures and heart rate increased equally across all groups during the cold pressor. Although this might suggest that effort was not different across groups, it is important to recognize that blood pressure responses to the cold pressor procedure are complex and could be largely independent of effort. The cold pressor is generally considered a passive coping task that produces increased blood pressure through vasoconstriction due to -adrenergic receptor stimulation. It has been demonstrated that both cardiac output and total peripheral resistance increase during the cold pressor and that both components of the cardiovascular response are associated with the painfulness of the task (27). Indeed, exploratory correlational analyses in our data revealed no relationship between self-reported effort, before or after cold pressor, and cardiovascular responses in either incentive group. Thus, systolic blood pressure may be a poor indicator of effort for the cold pressor task.

Although neither pain nor cardiovascular responses to the cold pressor procedure were influenced by incentive, the patterns of correlations between cardiovascular and pain response variables differed across groups. For low incentive subjects, higher baseline blood pressure was associated with decreased pain ratings and increased pain threshold and tolerance. This is consistent with previous reports of an inverse relationship between resting blood pressure and pain sensitivity (11, 28–32) . However, this association was not observed in high incentive subjects. For high incentive subjects, systolic reactivity was positively correlated with pain tolerance. This is consistent with previous research, which has demonstrated negative correlations between cardiovascular reactivity and pain sensitivity (33). Thus, the observed relationships between cardiovascular and pain responses have been previously reported, but the differing patterns of association across incentive conditions suggest that the determinants of pain responses may have been influenced by the incentive manipulation.

Relationships between pain perception and pre–cold pressor questionnaire responses were relatively similar across groups. For both high and low incentive subjects, pretask pain expectancies and predicted performance correlated with pain responses. In general, subjects who expected less pain and better performance had longer tolerance times and lower pain ratings. Surprisingly, self-reported motivation was associated with higher pain threshold and pain tolerance for low incentive subjects only. Associations with posttask self-report data were also relatively consistent across groups, as performance appraisal was associated with pain tolerance in both groups, and greater reported effort was associated with higher final pain ratings in both groups. For high incentive subjects only, monetary motivation was positively associated with pain tolerance. These data suggest that with the exception of monetary motivation, subjects’ expectancies and anticipated performance predicted pain responses regardless of the experimental condition.

The practical and conceptual implications of these results deserve mention. First, these findings suggest that motivation, whether experimentally manipulated or assessed by questionnaire, does not account for the sex difference in pain tolerance. Thus, if gender roles contribute to the observed difference, then this contribution must be mediated by factors other than motivation. Another important implication of these findings involves the associations between cardiovascular responses and pain measures in that the incentive condition seemed to alter the pattern of associations. One interpretation of these findings is that the low incentive subjects showed the typical relationship between resting blood pressure and diminished pain sensitivity, which may represent the functioning of a tonic pain regulatory system. The high incentive manipulation may have superseded this relationship by creating an association between pain responses and a more proximal cardiovascular response, blood pressure reactivity during the cold pressor task. This would be understandable if blood pressure reactivity reflected task engagement in the high but not the low incentive group, since greater task engagement would be expected to produce greater tolerance. However, perhaps more important than the specific pattern of results is the general message that psychological and attitudinal factors can influence the association between physiological responses and pain responses. Understanding these complex interactions among biological and psychosocial variables, rather than artificially separating their effects, embodies the biopsychosocial model applied to pain. Thus, when possible, investigators should explore the biological mediators of psychosocial influences (and vice versa) on pain responses.

Several limitations of this investigation should be mentioned. The age of the subjects is a potentially confounding factor because age was not equivalent in the four groups. However, all analyses were conducted using age as a covariate to control for this difference. In addition, most of these subjects were young adults, and the generalizability of the findings to adults in different age groups is unclear. Also, though not statistically different, there were proportionately more African American women than men; however, repeating the analyses using race as a covariate did not alter the results. Another potential problem involves ceiling effects. As mentioned above, 44% of the subjects, including more than half of the high incentive men, reached the cutoff time for the cold pressor. Although this likely did not prevent the detection of incentive effects among women, any incentive effect among men may have gone undetected. Finally, unlike previous research (15), we did not include a baseline cold pressor procedure and examine changes in pain tolerance as a function of incentive. Because it accounts for differences in baseline responses to the task, this approach reduces variability and may have yielded different results.

In summary, consistent with previous research, women demonstrated lower pain threshold and tolerance and higher ratings of cold pressor pain. However, contrary to our hypothesis based on social roles, incentive did not produce greater effects in women than men. In fact, any slight effect of incentive seems to have occurred in men. Likewise, no effects of incentive condition or sex emerged for cardiovascular responses. Of potential interest are the findings that significant correlations between resting cardiovascular measures and pain responses emerged for the low incentive group, whereas blood pressure reactivity was associated with pain tolerance among high incentive subjects. Similarly, posttask ratings of monetary motivation were correlated with pain tolerance among high but not low incentive subjects. These findings suggest that although incentive groups did not differ significantly in their pain responses, the determinants of pain responses may have differed as a function of incentive condition. Additional research is needed to replicate these findings and to further elucidate the relationships among motivation, gender roles, and pain responses.

	ACKNOWLEDGMENTS

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This material is the result of work supported with resources and the use of facilities at the Malcom Randall VA Medical Center, Gainesville, Florida. This work was supported by National Institutes of Health Grants DE12261 and NS41670.

Received for publication January 9, 2002.

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lowery, D. Articles by Wright, R. A. Search for Related Content PubMed PubMed Citation Articles by Lowery, D. Articles by Wright, R. A. Related Collections Blood Pressure Pain