Physiology & Behavior 124 (2014) 8–14

Contents lists available at ScienceDirect

Physiology & Behavior journal homepage: www.elsevier.com/locate/phb

There is no sweet escape from social pain: Glucose does not attenuate the effects of ostracism Holly C. Miller a,⁎, Camille Bourrasseau b, Kipling D. Williams c, Mikaël Molet b a b c

KU Leuven, Belgium University of Lille, France Purdue University, USA

H I G H L I G H T S • Participants were administered either 25 g of glucose or a sucralose placebo. • Participants were included or ostracized in a Cyberball game. • Glucose did not reduce the social pain in ostracized participants.

a r t i c l e

i n f o

Article history: Received 19 August 2013 Accepted 22 October 2013 Keywords: Ostracism Social pain Pain Glucose Cyberball

a b s t r a c t Ostracism causes social pain and is known to activate regions of the brain that are involved in the representation of physical pain. Previous research has observed that acetominophen (a common pain reliever) can reduce the pain of exclusion. The taste and consumption of glucose can also relieve physical pain, and the purpose of the current study was to examine whether it might also reduce the negative emotional effects of ostracism. In an appropriately powered experiment, participants were given 25 g of glucose or a sucralose placebo before being ostracized while playing Cyberball. Strong effects of ostracism were observed, however, there was no effect of glucose on immediate or delayed self-reported needs or mood. These results are discussed in reference to the possibility that social pain is unlike physical pain since the latter is affected by glucose, which is believed to lessen pain by increasing endogenous opioid activity. © 2013 Elsevier Inc. All rights reserved.

1. Introduction Considerable research attention has focused on the psychological impact of being ostracized (i.e., ignored and excluded) (see [1,2] for reviews). Consistent across several paradigms employed to induce ostracism, meta-analyses show increased distress, thwarted needs of belonging, self-esteem, control, and meaningful existence [3,4], and for some paradigms more than others, more negative affective states [4]. Neuroscience research indicates that verbal reports of distress are supported by activation of pain detection regions of the brain [5]. Suffice to say that being ostracized is painful and distressing, and can lead to many downstream emotional and behavioral consequences [2]. Methods employed to induce ostracism vary in power, but tend to show similar patterns of results. Thus, ostracism-induced distress is observed regardless of whether participants are reporting their reactions ⁎ Corresponding author at: Psychology of Learning and Experimental Psychopathology, KU Leuven, Belgium, Bureau 02.105, Tiensestraat 102, 3000 Leuven, Belgium. Tel.: +32 16 3 25742. E-mail address: [email protected] (H.C. Miller). 0031-9384/$ – see front matter © 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.physbeh.2013.10.032

to real-life episodes of ostracism [6], being excluded in a casual game of ball-toss while waiting in a laboratory with two others [7], finding out that others they have just met do not want to work with them [8], or even recalling events in their lives where they were excluded [9]. More powerful manipulations of rejection can lead to additional effects. If participants are shown a photo of a romantic partner responsible for recently ending a relationship, somatosensory pain regions of the brain are additionally activated [10]. If participants are told that they will lead a life-alone based on their responses to a personality assessment [11], emotional reactions can be temporarily shut down, resulting in an affective numbness [12]. The paradigm most widely used to investigate the impact of ostracism is known as Cyberball, a virtual variation on the ball-tossing paradigm [13–15]. Over 150 published studies have employed Cyberball to observe reactions in fMRI scanners, in laboratories, and even in field experiments (using an iPad; [16]; for a complete list, see: http:// www1.psych.purdue.edu/~willia55/Announce/Cyberball_Articles.htm). Participants are provided a cover story in which they are told the experimenters are interested in the effects of mental visualization on subsequent performance, and are told that to exercise their mental

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14

visualization abilities, it is useful to play Cyberball, in which they are playing ball toss with two or three others. They are explicitly told that it is of no importance to the experimenter who gets the ball; rather, it is important that they mentally visualize what the other players look like, where they are playing, what the weather and geography are like, and so on. The game shows animated characters throwing and catching a ball, and when the participant's character is thrown the ball, they are to click one of the other player's icons to indicate to which player the ball will be thrown. Unbeknown to the participant, the game is rigged such that it is programmed to either include the participant equally, or after a few catches, the participant never receives the ball again. After the game, participants are asked how they felt during the game, and their responses show large effect sizes (between 1.0 and 2.0) between those included and ostracized. This initial self-report (or brain images from an fMRI—e.g., [5], or dialed affect responses during the game; [17]) taken at Time 1 measures the immediate or reflexive response [2], and shows remarkable resistance to moderation by situational factors (e.g., whether the other players are similar or dissimilar, hated or liked, are computer generated or real people), or individual differences of the participants (e.g., low or high in social anxiety, depression, secure or insecure attachment orientation). Measures of distress and need-threat taken later, however, sometimes show moderation by situation and individual differences, such that some recover faster than others. For example, brief mindfulness training results in speedier recovery at Time 2, but just as much distress at Time 1 [18]. Some research suggests that one effect of ostracism is cognitive and emotional depletion [19–21]. Such depletion is theorized to occur when coping with social exclusion draws energy from a limited pool of mental resources, decreasing the energy available for subsequent complex tasks, emotional suppression, and pro-social responses. In one study, researchers found that cognitive depletion, induced by an attention control task, was prevented by providing individuals with glucose [22]. The authors argued that glucose replenished depleted resources, allowing for better decision-making and greater persistence. Our interest is in whether glucose also reduces the distress experienced by ostracism. Researchers have observed that the taste and consumption of glucose can lessen physical pain [23–26]. When infants undergo a painful medical procedure, for example, the taste of glucose reduces grimacing [27] and total crying time [28]. Similarly, the taste of sucrose (a disaccharide consisting of equal parts glucose and fructose) increases cold pain tolerance in young adults [29,30]. Participants tasting a sucrose solution are willing to keep their hands submerged in cold water for longer than those tasting a bitter solution or water. Research using functional magnetic resonance imaging (fMRI) has observed that the taste of glucose not only increases pain thresholds during the cold-pressor test, but it correspondingly reduces neural activity in pain-related brain regions (i.e., the anterior cingulate cortex, insula, posterior parietal cortex, and thalamus) more than a placebo [31]. Humans are not unique; the taste and consumption of glucose also appears to have analgesic properties for rats. It is worth noting that the duration of this antinociception is dose-dependent. When four different concentrations of a 400 μL sucrose solution were administered to rats (25 g/L, 50 g/L, 150 g/L, 250 g/L) only the solution with the highest concentration decreased the nociceptive threshold 15 min post-consumption [32]. It is likely that larger doses have longer lasting effects because they continue to be detected directly by sweet taste receptors in the digestive system and also indirectly through glucose gastrointestinal chemosensing mechanisms [33]. Such oral and gastrointestinal detection of glucose activates afferent vagus nerve fibers, which may contribute to the modulation of pain [34]. It is hypothesized that glucose reduces pain by increasing endogenous opioid release. The consumption of glucose is associated with acute binding of the endogenous opiate β-endorphin in the brain at μ-opioid receptors [35]. In rats, the consumption of sweet beverages increases endogenous opioid peptide activity in the brain, plasma and

9

cerebral spinal fluid [36]. There is also evidence that glucose can produce endogenous opioid dependence. Following a month of intermittent access to a 25% glucose solution, rats administered naloxone (an opiate receptor antagonist) or fasted from glucose show symptoms of withdrawal that mirror those from opiates such as morphine [37]. The observation that glucose decreases physical pain is relevant for research on ostracism since physical and social pain appear to share overlapping neural circuitry. This commonality has been proposed to account for why the consumption of acetaminophen (a pain reliever whose analgesic effects depend upon the cannabinoid 1 (CB1) receptor) attenuates the social pain induced by ostracism [38,39], and also why marijuana appears to do the same [40]. It also implies that glucose, which can decrease physical pain, should be able to attenuate the pain of social rejection. Of course, there are other reasons why glucose might affect reaction and recovery from exclusion. Glucose not only affects the opioid system, it also increases the release of dopamine (DA) in the anterior cingulated cortex (ACC), ventral striatum [41], and nucleus accumbens (NAcc) [42]. Such increases in dopamine are theorized to be responsible for replenishment by glucose, and have been implicated in the enhancement of motivation, persistence, and executive control [43]. The purpose of the current study was to examine whether glucose could decrease the social pain induced by ostracism. In order to accomplish this goal, participants were given either a glucose or calorie-free sucralose placebo beverage 10 min before being ostracized in the Cyberball game. This delay enabled glucose to be detected by both direct and indirect glucose sensing mechanisms [33]. Testing was conducted during digestion rather than during tasting because the sweet taste receptors in the mouth and the stomach are identical [34], and thus there was no inherent advantage to testing with an intraoral preparation. Moreover, this was the more pragmatic methodology because it allowed participants to experience the Cyberball task as those tested in previous experiments, without confounding the experience by requiring participants to hold a sweet liquid in the mouth while simultaneously playing the game. 2. Method 2.1. Power calculation A meta-analysis of previous research has reported a large, to very large overall effect size for ostracism by Cyberball on basic needs (d N 1) [44]. An a priori power calculation using G-power revealed that with an effect size of d = 1, and alpha set to .05 (two-tailed), and power set to .95, a sample size of 16 (n = 8 for each inclusionary condition) would be required for 96% power [45]. The effect size of glucose on social pain is as yet unknown, however, in terms of modulating physical pain, a recent Cochrane review on research with infants has reported medium to large effect sizes for the analgesic properties of sucrose [28]. For example, a medium effect size (d = .48) for sucrose on Premature Infant Pain Profile scores taken during intramuscular injections, venipunctures, and heel lances has been reported [46], along with a large effect size (d = 4.14) for glucose on total crying following heel lances [47]. In addition, a large omega squared value (ω2 = 0.16) has been reported for sucrose on cold pain tolerance in adults [48]. Taken together, these observations suggest that glucose has a sizeable effect on pain. Accordingly, we assumed a large effect size (d = .80) for glucose, ran an a priori power calculation using G-power with alpha set to .05 (two-tailed) and power set to .95, which revealed that a total sample size of 24 (n = 12 for each drink condition) would be required for 96% power. 2.2. Participants and design Forty-eight undergraduate students from the University of Lille participated in the study (32 females and 16 males, Mage = 20.69 yrs;

10

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14

SD = 2.17). A 2 (drink manipulation: glucose, placebo) × 2 (inclusionary status: ostracism, inclusion) × (2) (time of measurement: immediate, delayed) factorial design was employed, with repeated measures on the third factor. Maintaining the male/female ratio, eight females and four males were randomly assigned to each of the four betweensubject conditions. 2.3. Drink manipulation Following a randomized, double blind, placebo controlled, between subjects design, participants who had abstained from consuming anything caloric or caffeinated for 3 h were administered 25 g glucose or an inert sucralose placebo (that was matched for sweetness) in an isovolumic solution (300 mL). The beverages were matched for flavor by the infusion of caffeine-free Lipton® herbal peach and mango tea. Each participant attended one laboratory session after refraining from eating or drinking anything caloric or caffeinated for 3 h. Upon arrival, participants gave informed consent and demographic information. They were randomly assigned to a drink condition. Following drink consumption, they reported the extent to which they agreed, or disagreed, on a scale of 1–5 (with 1 = disagree strongly and 5 = agree strongly), with the following statements: “This drink contained calories”, “This drink contained a non-nutritive sweetener” and “I enjoyed this drink”. Higher values corresponded to greater perception of calories, similarity to non-caloric sweetener and higher likability, respectively. The purpose of the first two questions was to determine whether the basic taste of the drinks was similar. If participants evaluated drinks similarly, then it would evidence that glucose was not consciously detected and thus could not influence responding through expectations. The third question was included as a manipulation check. Since glucose stimulates the release of β-endorphins more than sucralose, it should be perceived as more palatable. Palatability itself affects opiate release [49]. The administration of naltrexone has been shown to reduce the pleasantness of sweet solutions without affecting basic taste detection or the recognition of basic tastes such as sweet, sour, bitter, and salty [50]. Afterwards they waited for 10 min so that the ingested glucose could be detected by sweet taste receptors in the digestive system and so that indirect glucose chemosensing could activate the vagus nerve [33]. This procedure was identical to that used by Miller et al. [51]. 2.4. Cyberball Following the digestive interim, participants were seated in front of a computer screen announcing that they would play Cyberball, an Internet ball-tossing game designed to help people practice mental visualization. In reality, the game manipulated ostracism versus inclusion (see [13]). Participants were led to believe that they were playing with three other students taking part in the experiment over the Internet. In actuality, a computer program controlled the other players. They were also told that throughout the game they would be represented by the animated figure on the bottom of the screen. The game began with one of the players throwing the ball to the participant. The participant was then required to indicate to whom they would like to throw the ball by clicking on the appropriate player icon. In the ostracism condition, the participant received the ball twice and then did not receive the ball ever again. In the inclusion condition, the participant randomly received the ball approximately 33% of the time. In both conditions, there were 30 ball tosses, which took approximately 4 min. 2.5. Manipulation checks After playing Cyberball, participants completed a standard postexperimental questionnaire that has been used in previous ostracism research (see [2]). They were asked to answer the questions based on how they felt during the game (see the Appendix A). Using 5-point scales, with 1 = not at all and 5 = very much, they completed 20 items

assessing their levels of belonging, self-esteem, meaningful existence, and control. They also completed four bipolar affect items presented on a 7-points scale to indicate their mood. There were three manipulation checks to confirm participants' perception of their inclusionary status, i.e., “I was ignored,” and “I was excluded,” both answered using the same 5-point scale described above, and an open question: “Assuming that 33% of the time you would receive the ball if everyone received it equally, what percent of the throws did you receive?” (see Appendix A for copies of the questionnaires). Participants were told that their data would be organized in preparation for a follow-up questionnaire, and that they should wait quietly until the second questionnaire was administered. About 3-minutes later, participants completed the ostracism questionnaire by answering the same need-satisfaction and mood items, but with the prefix: “How do you feel right now?” (see Appendix A). They were then debriefed, thanked, and dismissed. The experiment was conducted between the hours of 12:30 and 6:30 pm, and time of testing was balanced across conditions. 3. Results 3.1. Perceptions of drinks To assess taste similarity across conditions, we examined means of the three written questions concerning the drinks. A 2 (drink manipulation: glucose, placebo) × 2 (inclusionary status: ostracism, inclusion) MANOVA yielded a significant main effect of drink regarding the likability, F(1,44) = 7.27, p = .01, η2p = .15, suggesting that the participants preferred the glucose drink (MOstracized = 3.92 and MIncluded = 3.33, SDs = 0.90 and 1.50, respectively) more than the placebo (MOstracized = 2.75 and MIncluded = 2.42, SDs = 1.48 and 1.38, respectively) and indirectly evidencing differential β-endorphin activation by glucose. The main effect of status and the interaction between drink and status were not significant for the likability, Fs b 1.4, ps N .24, confirming no baseline differences between the participants assigned to the ostracism and included conditions. Concerning the two others questions, no effect was detected, Fs b 2, ps N .13, participants perceived the calorie content of the glucose and placebo drinks to be the same (glucose: MOstracized = 3.00 and MIncluded = 2.75, SDs = 1.04 and .87, respectively; placebo: MOstracized = 3.17 and MIncluded = 3.42, SDs = .83 and .99, respectively) and they were equally as likely to believe that each beverage was sweetened with artificial sweetener (glucose: MOstracized = 3.50 and MIncluded = 3.25, SDs = .90 and 1.05, respectively; placebo: MOstracized = 3.33 and MIncluded = 3.83, SDs = 1.23 and 1.03, respectively). 3.2. Perceptions of ostracism Because the feeling of being ignored and excluded was highly correlated (Cronbach's alpha = .93), they were averaged. As shown in Table 1, ostracized participants reported that they felt more ignored and excluded than those who were included, F(1,44) = 55.1, p b .001, η2p = .56. There was no significant main effect of drink or interaction between drink and inclusionary status, Fs b 1. Additionally, ostracized participants reported that they received the ball less often during the game than included participants, F(1,44) = 103.73, p b .001, η2p = .70. There was no significant main effect of drink or interaction between drink and inclusionary status on perceived ball tosses received, Fs b 1.9, ps N .17. Participants correctly perceived that they were included or ostracized during the game, and their perceptions were unaffected by drink condition. 3.3. Self-reported levels of needs Cronbach's alpha coefficients for each need after immediate test were: belonging = .81, self-esteem = .87, meaningful existence = .92, control = .71; and after the 3 min delay were: belonging = .75, self-

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14 Table 1 Means and standard deviations (in parenthesis) of manipulation checks regarding drink and inclusionary status. Glucose

a

The drink contained calories

The drink contained a non-nutritive sweetenera I enjoyed the drinka b

Excluded/ignored % Throws

Placebo

Ostracism

Inclusion

Ostracism

Inclusion

3.00 (1.04) 3.50 (.90) 3.92 (.90) 4.04 (.94) 7.67 (3.50)

2.75 (.87) 3.25 (1.05) 3.33 (1.50) 1.67 (.81) 22.67 (5.63)

3.17 (.83) 3.33 (1.23) 2.75 (1.48) 4.04 (1.20) 5.67 (4.27)

3.42 (.99) 3.83 (1.03) 2.42 (1.38) 2.04 (1.10) 20.58 (6.43)

11

make the groups nonequivalent” (p.554). We chose ±1.0 points as the equivalence interval between groups for the 5-point rating scale [53]. At the immediate test, equivalence can be concluded because the calculated 95% confidence interval was ±.42 and was contained within the equivalence interval. The same is true at the delayed test, since the confidence interval was ±.50. Thus, glucose did not reduce the negative effects of ostracism during the game nor did it aid recovery from an ostracism episode relative to a placebo. 3.4. Mood items

a Statements from the mini-questionnaire on drink presented on five-point scales (1 = disagree strongly, 5 = agree strongly). b This was an average of two questions presented on five-point scales (1 = not at all, 5 = very much so).

esteem = .80, meaningful existence = .79, and control = .70. The internal consistency across the four needs at both time points were reasonably high. Because they were all highly correlated at both time points (Cronbach's alphas = .91 and .84, respectively immediate and delayed), we calculated a need satisfaction index that averaged the items at both time points was used in the following analysis (see Table 2). The levels of needs were analyzed with a 2 (drink manipulation: glucose, placebo) × 2 (inclusionary status: ostracism, inclusion) × (2) (time of measurement: immediate, delayed) ANOVA, with repeated measures on the third factor. There was a significant main effect of inclusionary status, F(1,44) = 37.82, p b .001, η2p = .46, reflecting that ostracized participants (M = 2.48, SD = .11) perceived that their levels of needs were lower than included participants (M = 3.44, SD = .11). A main effect of time of measurement, F(1,44) = 29.81, p b .001, η2p = .40, indicated that the levels of needs increased from the immediate (M = 2.72, SD = .08) to the delayed rating (M = 3.15, SD = .09). Time of measurement interacted with inclusionary status, F(1,44) = 36.75, p b .001, η2p = .45, suggesting that the ostracized participants manifested an increase (i.e., a recovery) in the levels of the need satisfaction from the immediate to the delayed rating (MIM = 2.08 and MDE = 2.88, SDs = .48 and .57, respectively) whereas included participants' needs stayed relatively high across both times of measurement (MIM = 3.45 and MDE = 3.41, SDs = .64 and .58, respectively). There was no significant main effect for the drink on selfreported needs, nor did the inclusionary status and/or time of measurement interact with the drink, Fs b 1 and ps N .4. Taken together these analyses suggest that ostracized participants reported lower levels of needs independent of the drink. Said differently, the glucose drink did not appear to affect ostracized participants differently than the placebo. However, in order to evidence that the two critical groups were comparable, we conducted an equivalency test, as it is acknowledged to be a better alternative for demonstrating that the groups are comparable [52,53]. Equivalency is described by Rogers et al. [52] as “the minimum difference between two groups that would he important enough to

The four mood items were averaged to form a single score at both immediate and delayed ratings (Both Cronbach's alphas = .92). The mood scores (see Table 2) were analyzed similarly to the need satisfaction scores. The inclusionary status main effect was significant, with ostracized participants reporting more negative mood (M = 3.42, SD = .14) than included participants (M = 4.16, SD = .14), F(1,44) = 12.91, p = .001, η2p = .23. There was a main effect of time of measurement, F(1,44) = 15.42, p b .001, η2p = .26, reflecting that the levels of needs increased from the immediate (M = 3.58, SD = .12) to the delayed rating (M = 4.00, SD = .11). Time of measurement interacted with inclusionary status, F(1,44) = 16.60, p b .001, η2p = .27, such that mood scores increased in the ostracized participants from the immediate (IM) to the delayed (DE) rating (MIM = 3.21 and MDE = 3.63, SDs = .93 and 1.05, respectively) whereas included participants' moods stayed relatively high across both times of measurement (MIM = 4.27 and MDE = 4.15, SDs = .64 and .58, respectively). There were no significant main effects for the drink on self-reported needs, nor did the inclusionary status and/or time of measurement interact with the drink, Fs b 2, ps N .14. These results suggest that glucose does not affect mood, nor does it facilitate coping or recovery from an ostracism episode. 4. Discussion The motivation for this research was to investigate whether glucose could decrease the social pain induced by ostracism. Evidence suggests that glucose can reduce physical pain, and it is currently argued that physical and social pain are inherently similar, as they share overlapping neural circuitry. Accordingly, glucose should have reduced the negative effects incurred by playing the exclusionary version of the Cyberball game, and enhanced recovery. Surprisingly, no such effects were observed. In fact, an equivalency test evidenced that the effects of glucose were comparable to those of the placebo. One could argue that the failure to detect an effect was due to the fact that participants were tested during the digestive period, and not during the tasting of glucose. Research with infants has observed that the taste but not necessarily the consumption of glucose is responsible for decreasing pain [54], and intraoral preparations are typically used. We chose not to do similarly, thus we cannot discount the possibility that an intraoral preparation would have been more effective. However, we do argue that since the digestion of glucose increases endogenous

Table 2 Means and standard deviations (in parenthesis) of variables as a function of drink manipulation, inclusionary status, and time point of rating. Glucose

Placebo

Ostracism

a

Needs

b

Mood a b

Inclusion

Ostracism

Inclusion

Immediate

Delayed

Immediate

Delayed

Immediate

Delayed

Immediate

Delayed

2.07 (.53) 2.87 (.67)

2.80 (.68) 3.60 (.59)

3.54 (.48) 4.21 (.55)

3.45 (.55) 3.99 (.66)

2.09 (.45) 3.13 (1.07)

2.96 (.46) 4.09 (.90)

3.37 (.75) 4.14 (.92)

3.38 (.70) 4.32 (.88)

This was the average for the items assessing each need (higher scores indicate higher levels of the needs). Total mood score was an average of 4 seven-point bipolar items (higher scores indicate more positive mood).

12

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14

opioid peptide activity, and this is the mechanism through which glucose is supposed to lessen pain, there is no strong argument that the taste but not the consumption of glucose should be more effective, an assessment that is supported by rat research on glucose and antinociception [32]. Moreover, analogous research examining whether glucose can replenish depletion observed performance differences when participants were tested following consumption [22], and previous research using the same methodology adopted here observed strong effects of glucose on anagram problem solving by participants tested 15 min post consumption [51]. Chen et al. [55] has argued that physical and social pain are similar and yet different since one can be relived more than the other. The findings we obtained here argue that another distinction between the two is that physical pain can be modulated by glucose, which implies that endogenous opioid release can decrease physical but not social pain [56]. Research providing support for this hypothesis can be obtained in the animal literature on social distress. It appears that though morphine can reduce distress calling by socially isolated infant rats, it only does so at levels that also affect general functions such as locomotion. Opiate antagonists, that should increase distress, fail to affect responding. No alterations of in-vivo binding at opioid receptors have been observed during stressful social isolation [56]. The potentiation of isolated rat pup vocalization is also not decreased by morphine (an opiate) nor increased by naltrexone (an opiate antagonist) [57]. Given these observations, animal researchers have investigated the role of other neurotransmitters, and have observed that the dopamine (D2) neural receptor is most relevant for the expression of social distress. D2 receptor agonists decrease vocalization by isolated rat pups, and antagonists increase distress calls when pups are reunited with dams. In contrast, D1 agonists have nonspecific effects [58]. It was previously mentioned that glucose consumption might modulate the experience of and recovery from social pain by increasing motivation, persistence, and executive control through increased dopaminergic activity. This hypothesis was not sustained. This failure might be explained by the observation that the rewarding properties of glucose are dependent on D1, not D2, receptor activation in the medial prefrontal cortex [59] and the modulation of cognitive function and the replenishment of depletion are believed to rely on D1 receptor activity. Significant research has observed that D1 is involved in prefrontal cortex function (for a review see [60]), and D1 agonists enhance whereas antagonists impair executive function [60]. D2 is also involved, but its role is less clear [61]. Thus, if D2 agonism is necessary to decrease the experience of social pain, a failure to decrease the effects of ostracism with glucose is not surprising. The failure to reduce social pain by increasing motivation, persistence and executive control via D1 activation is largely consistent with behavioral research that has tried to reduce the negative effects of ostracism through motivational or cognitive manipulations [2]. In conclusion, though we observed no significant difference in social pain as a function of glucose consumption, the results presented here deserve attention. They suggest that social pain may be different from physical pain in terms of neural activity. Humans, like rodents, may experience reduced social pain from D2 agonists, but not through the increased endogenous opioid activity or activation of D1 receptors. This point deserves further investigation. Conflict of interest The authors declare no conflict of interest. Acknowledgments Preparation of this manuscript was supported in part by an F+ fellowship awarded to Holly Miller by KU Leuven and financed by the Center for Excellence on Generalization Research (GRIP.TT; KU Leuven grant PF/10/005).

Appendix A (R) indicates that the score should be reversed. Reflexive questionnaire

For each question, please circle the number to the right that best represents the feelings you were experiencing during the game.

Not at all

Belonging I felt “disconnected” (R) I felt rejected (R) I felt like an outsider (R) I felt I belonged to the group I feel the other players would interact with me a lot

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Self esteem I felt good about myself My self-esteem was high I felt liked I felt insecure (R) I felt satisfied

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Meaningful existence I felt invisible (R) I felt meaningless (R) I felt non-existent (R) I felt important I felt useful

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Control I felt powerful I felt I had control over the course of the game I felt I had the ability to significantly alter events I felt I was unable to influence the action of others (R) I felt the other players decided everything (R)

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Mood Good Bad Friendly Unfriendly Angry Pleasant Happy Sad

1 1 1 1 1 1 1 1

2 2 2 2 2 2 2 2

3 3 3 3 3 3 3 3

4 4 4 4 4 4 4 4

5 5 5 5 5 5 5 5

Extremely

Manipulation check For the next three questions, please circle the number to the right (or fill in the blank) that best represents the thoughts you had during the game. I was ignored 1 2 3 4 5 I was excluded 1 2 3 4 5 Assuming that the ball should be thrown to each person ____ % equally (33% if three people; 25% if four people), what percentage of the throws did you receive?

Reflective questionnaire

For each question, please circle the number to the right Not that best represents the feelings you are experiencing at all right now.

Extremely

Belonging I feel “disconnected” (R) I feel rejected (R) I feel like an outsider (R) I feel I belong to the group I feel the other players interact with me a lot

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Self esteem I feel good about myself My self-esteem is high I feel liked I feel insecure (R)

1 1 1 1

2 2 2 2

3 3 3 3

4 4 4 4

5 5 5 5

(continued on next page)

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14 Appendix (continued) A (continued) For each question, please circle the number to the right Not that best represents the feelings you are experiencing at all right now. I feel satisfied Meaningful existence I feel invisible (R) I feel meaningless (R) I feel non-existent (R) I feel important I feel useful

Extremely

1

2 3 4 5

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Control I feel powerful I feel I have control over the course of events I feel I had the ability to significantly alter events I feel I am unable to influence the action of others (R) I feel others decide everything (R)

1 1 1 1 1

2 2 2 2 2

3 3 3 3 3

4 4 4 4 4

5 5 5 5 5

Mood Good Bad Friendly Unfriendly Angry Pleasant Happy Sad

1 1 1 1 1 1 1 1

2 2 2 2 2 2 2 2

3 3 3 3 3 3 3 3

4 4 4 4 4 4 4 4

5 5 5 5 5 5 5 5

Note The questionnaires have been translated (from English to French) and back-translated (from French to English) until an agreement was found.

References [1] Williams KD. Ostracism: effects of being ignored and excluded. Int J Psychol 2008;43:398. [2] Williams KD. Ostracism: a temporal need-threat model. In: Zanna M, editor. Advances in experimental social psychology, 41. NY: Academic Press; 2009. p. 279–314. [3] Blackhart GC, Nelson BC, Knowles ML, Baumeister RF. Rejection elicits emotional reactions but neither causes immediate distress nor lowers self-esteem: a meta-analytic review of 192 studies on social exclusion. Pers Soc Psychol Rev 2009;13:269–309. [4] Gerber J, Wheeler L. On being rejected: a meta-analysis of experimental research on rejection. Perspect Psychol Sci 2009;4:468–88. [5] Eisenberger NI, Lieberman MD, Williams KD. Does rejection hurt? An fMRI study of social exclusion. Science 2003;302:290–2. [6] Nezlek JB, Wesselmann E, Wheeler L, Williams KD. Ostracism in everyday life. Group Dyn 2012;16:91–4. [7] Williams KD, Sommer KL. Social ostracism by one's coworkers: does rejection lead to loafing or compensation? Pers Soc Psychol Bull 1997;23:693–706. [8] Maner JK, DeWall C, Baumeister RF, Schaller M. Does social exclusion motivate interpersonal reconnection? Resolving the ‘porcupine problem’. J Pers Soc Psychol 2007;92:42–55. [9] Pickett CL, Gardner WL, Knowles M. Getting a cue: the need to belong and enhanced sensitivity to social cues. Pers Soc Psychol Bull 2004;30:1095–107. [10] Kross E, Berman MG, Mischel W, Smith EE, Wager TD. Social rejection shares somatosensory representations with physical pain. Proc Natl Acad Sci 2011;108:6270–5. [11] Twenge JM, Baumeister RF, Tice DM, Stucke TS. If you can't join them, beat them: effects of social exclusion on aggressive behavior. J Pers Soc Psychol 2001;81:1058–69. [12] Bernstein MJ, Claypool HM. Social exclusion and pain sensitivity: why exclusion sometimes hurts and sometimes numbs. Pers Soc Psychol Bull 2012;38:185–96. [13] Williams KD, Cheung CKT, Choi W. CyberOstracism: effects of being ignored over the Internet. J Pers Soc Psychol 2000;79:748–62. [14] Williams KD, Jarvis B. Cyberball: a program for use in research on ostracism and interpersonal acceptance. Behav Res Methods Instrum Comput 2006;38:174–80. [15] Williams KS, Yeager DS, Cheung CKT, Choi W. Cyberball (version 4.0) [Software]. Available from https://cyberball.wikispaces.com; 2012. [16] Hales, A., Williams, K.D., & Eckhardt, E. (2013). Feeling no pain: Effects of alcohol intoxication on reactions to ostracism. Unpublished manuscript, Purdue University, West Lafayette, IN. [17] Wesselmann ED, Wirth JH, Mroczek DK, Williams KD. Dial a feeling: detecting moderation of affect decline during ostracism. Personal Individ Differ 2012;53:580–6. [18] Molet M, Macquet B, Lefebvre O, Williams K. A focused attention intervention for coping with ostracism. Conscious Cogn 2013;22(4):1262–70. [19] Twenge JM, Catanese KR, Baumeister RF. Social exclusion and the deconstructed state: time perception, meaninglessness, lethargy, lack of emotion, and selfawareness. J Pers Soc Psychol 2003;85:409–23.

13

[20] DeWall CN, Baumeister RF. Alone but feeling no pain: effects of social exclusion on physical pain tolerance and pain threshold, affective forecasting, and interpersonal empathy. J Pers Soc Psychol 2006;91:1–15. [21] Oaten MR, Williams KD, Jones A, Zadro L. The effects of ostracism on self-regulation in the socially anxious. J Soc Clin Psychol 2008;27:471–504. [22] Gailliot MT, Baumeister RF, DeWall CN, Maner JK, Plant EA, Tice DM, Brewer LE, Schmeichel BJ. Self-control relies on glucose as a limited energy source: willpower is more than a metaphor. J Pers Soc Psychol 2007;92:325–36. [23] Blass EM, Hoffmeyer LB. Sucrose as an analgesic for newborn infants. Pediatrics 1991;87(2):215–8. [24] Blass EM, Shide DJ. Some comparisons among the calming and pain relieving effects of sucrose, glucose, fructose, and lactose in infant rats. Chem Senses 1994;19:239–49. [25] Carbajal R, Chauvet X, Couderc S, Olivier-Martin M. Randomised trial of analgesic effects of sucrose, glucose, and pacifiers in term neonates. Br Med J 1999;319(7222):1393–7. [26] Okan F, Coban A, Ince Z, Yapici Z, Can G. Analgesia in preterm newborns: the comparative effects of sucrose and glucose. Eur J Pediatr 2007;166(10):1017–24. [27] Blass EM, Watt LB. Suckling-and sucrose-induced analgesia in human newborns. Pain 1999;83:611–23. [28] Stevens B, Yamada J, Lee GY, Ohlsson A. Sucrose for analgesia in newborn infants undergoing painful procedures. Cochrane Database Syst Rev 2013;1:CD001069. http:// dx.doi.org/10.1002/14651858.CD001069.pub4. [29] Lewkowski M, Ditto B, Roussos M, Young SN. Sweet taste and blood pressure-related analgesia. Pain 2003;106:181–6. [30] Eggleston K, White TL, Sheehe PR. Adding cocoa to sucrose: the effect on cold pain tolerance. Chem Senses 2010;35(4):269–77. [31] Kakeda T, Ogino Y, Moriya F, Saito S. Sweet taste-induced analgesia: an fMRI study. Neuroreport 2010;21:427–31. [32] de Freitas RL, Kübler JM, Elias-Filho DH, Coimbra NC. Antinociception induced by acute oral administration of sweet substance in young and adult rodents: the role of endogenous opioid peptides chemical mediators and μ(1)-opioid receptors. Pharmacol Biochem Behav 2012;101:265–70. [33] Breer H, Eberle J, Frick C, Haid D, Widmayer P. Gastrointestinal chemosensation: chemosensory cells in the alimentary tract. Histochem Cell Biol 2012;138(1):13–24. [34] Busch V, Zeman F, Heckel A, Menne F, Ellrich J, Eichhammer P. The effect of transcutaneous vagus nerve stimulation on pain perception — an experimental study. Brain Stimul 2012;6(2):202–9. [34] Dyer J, Salmon K, Zibrik L, Shirazi-Beechey SP. Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem Soc Trans 2012;33:302–5. [35] Colantuoni C, Schwenker J, McCarthy J, Rada P, Ladenheim B, Cadet JL, Schwartz GJ, Moran TH, Hoebel BG. Excessive sugar intake alters binding to dopamine and muopioid receptors in the brain. Neuroreport 2001;12(16):3549–52. [36] Yamamoto T, Sako N, Maeda S. Effects of taste stimulation on beta-endorphin levels in rat cerebrospinal fluid and plasma. Physiol Behav 2000;69(3):345–50. [37] Colantuoni C, Rada P, McCarthy J, Patten C, Avena NM, Chadeayne A, Hoebel BG. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res 2002;10:478–88. [38] Mallet C, Daulhac L, Bonnefont J, Ledent C, Etienne M, Chapuy E, Libert F, Eschalier A. Endocannabinoid and serotonergic systems are needed for acetaminophen-induced analgesia. Pain 2008;139(1):190–200. [39] DeWall CN, Macdonald G, Webster GD, Masten CL, Baumeister RF, Powell C, Combs D, Schurtz DR, Stillman TF, Tice DM, Eisenberger NI. Acetaminophen reduces social pain: behavioral and neural evidence. Psychol Sci 2010;21(7):931–7. [40] Deckman T, DeWall CN, Way B, Gilman R, Richman S. Can marijuana reduce social pain? Soc Psychol Personal Sci 2013. http://dx.doi.org/10.1177/1948550613488949. [41] Chambers E, Bridge M, Jones D. Carbohydrate sensing in the human mouth; effects on exercise performance and brain activity. J Physiol 2009;587:1779–94. [42] Hajnal A, Smith GP, Norgren R. Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 2004;286:R31–7. [43] Molden DC, Hui CM, Scholer AA, Meier BP, Noreen EE, D'Agostino PR, Martin V. The motivational versus metabolic effects of carbohydrates on self-control. Psychol Sci 2012;23(10):1137–44. [44] Case TI, Williams KD. Ostracism: a metaphor for death. In: Greenberg J, Koole SL, Pyszczynski T, editors. Handbook of experimental existential psychology. NY: Guilford Press; 2004. p. 336–51. [45] Erdfelder E, Faul F, Buchner A. GPOWER: a general power analysis program. Behav Res Methods Instrum Comput 1996;28:1–11. [46] Taddio A, Shah V, Hancock R, Smith RW, Stephens D, Atenafu E, Beyene J, Koren G, Stevens B, Katz J. Effectiveness of sucrose analgesia in newborns undergoing painful medical procedures. Can Med Assoc J 2008;179:37–43. [47] Isik U, Ozek E, Bilgen H, Cebeci D. Comparison of oral glucose and sucrose solutions on pain response in neonates. J Pain 2000;1:275–8. [48] Mercer ME, Holder MD. Assessing the analgesic effects of sucrose to cold pressor pain in human adults. J Behav Brain Sci 2013;3:7–12. [49] Yamamoto T. Brain mechanisms of sweetness and palatability of sugars. Nutr Rev 2003;61(5):S5–9. [50] Arbisi PA, Billington CJ, Levine AS. The effect of naltrexone on taste detection and recognition threshold. Appetite 1999;32:241–9. [51] Miller HC, Bourraseau C, Blamplain J. Can you enhance executive control without glucose? The effects of fructose on problem solving. J Psychopharmacol 2013;27(7):645–50. [52] Rogers JL, Howard KI, Vessey JT. Using significance tests to evaluate equivalence between two experimental groups. Psychol Bull 1993;113:553–65. [53] Rusticus SA, Lovato CY. Applying tests of equivalence for multiple group comparisons: demonstration of the confidence interval approach. Pract Assess Res Eval 2011;16 [Available online: http://pareonline.net/getvn.asp?v=16&n=7].

14

H.C. Miller et al. / Physiology & Behavior 124 (2014) 8–14

[54] Barr RG, Pantel MS, Young SN, Wright JH, Hendricks LA, Gravel R. The response of crying newborns to sucrose: is it a “sweetness” effect? Physiol Behav 1999; 66(3):409–17. [55] Chen ZS, Williams KD, Fitness J, Newton NC. When hurt will not heal — exploring the capacity to relive social and physical pain. Psychol Sci 2008;19(8):789–95. [56] Winslow JT, Insel TR. Endogenous opioids: do they modulate the rat pup's response to social isolation? Behav Neurosci 1991;105:253–63. [57] Shair HN, Brunelli SA, Hofer MA. Lack of evidence for mu-opioid regulation of a socially mediated separation response. Physiol Behav 2005;83(5):767–77. [58] Muller JM, Moore H, Myers MM, Shair HN. Dopamine's role in social modulation of infant isolation-induced vocalization: II. Maternally modulated infant separation

responses are regulated by D1-and D2-family dopamine receptors. Dev Psychobiol 2009;51(2):158–72. [59] Touzani K, Bodnar RJ, Sclafani A. Acquisition of glucose-conditioned flavor preference requires the activation of dopamine D1-like receptors within the medial prefrontal cortex in rats. Neurobiol Learn Mem 2010;94(2):214–9. [60] Floresco SB. Prefrontal dopamine and behavioral flexibility: shifting from an “invertedU” toward a family of functions. Front Neurosci 2013;7(62). http://dx.doi.org/10.3389/ fnins.2013.00062. [61] Granon S, Passetti F, Thomas KL, Dalley JW, Everitt BJ, Robbins TW. Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J Neurosci 2000;20(3):1208–15.

There is no sweet escape from social pain: glucose does not attenuate the effects of ostracism.

Ostracism causes social pain and is known to activate regions of the brain that are involved in the representation of physical pain. Previous research...
261KB Sizes 0 Downloads 0 Views