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Social Neuroscience Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/psns20

Social exclusion induces early-stage perceptual and behavioral changes in response to social cues ab

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Taishi Kawamoto , Hiroshi Nittono & Mitsuhiro Ura

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Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima 739-8521, Japan b

Japan Society for the Promotion of Science, Tokyo, Japan Published online: 05 Feb 2014.

To cite this article: Taishi Kawamoto, Hiroshi Nittono & Mitsuhiro Ura (2014) Social exclusion induces early-stage perceptual and behavioral changes in response to social cues, Social Neuroscience, 9:2, 174-185, DOI: 10.1080/17470919.2014.883325 To link to this article: http://dx.doi.org/10.1080/17470919.2014.883325

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SOCIAL NEUROSCIENCE, 2014 Vol. 9, No. 2, 174–185, http://dx.doi.org/10.1080/17470919.2014.883325

Social exclusion induces early-stage perceptual and behavioral changes in response to social cues Taishi Kawamoto1,2, Hiroshi Nittono1, and Mitsuhiro Ura1

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Graduate School of Integrated Arts and Sciences, Hiroshima University, Higashi-Hiroshima 739-8521, Japan 2 Japan Society for the Promotion of Science, Tokyo, Japan

Social exclusion is so aversive that it causes broad cognitive and behavioral changes to regulate the individual’s belonging status. The present study examined whether such changes also occur at early neural or automatic behavioral levels in response to social cues. Event-related brain potentials (ERPs) and facial electromyograms (EMGs) were recorded during a task in which participants viewed smiling, disgusted, and neutral faces after experiencing social exclusion or inclusion. Social exclusion was manipulated using a simple ball-tossing game (Cyberball), and need threat was assessed after the game. We found that zygomaticus major muscle activity, which reflects facial mimicry, was larger in response to smiling faces after exclusion than after inclusion. In addition, P1 amplitude, which reflects visual attention, was larger for disgusted faces than for neutral faces following social exclusion. N170 amplitude, which reflects structural encoding of the face, was correlated with heightened need threat. These findings demonstrate that social exclusion induces immediate and rapid changes in attention, perception, and automatic behavior. These findings reflect the rapid and primary regulation of belonging.

Keywords: Social exclusion; Belonging regulation; Facial expression; Event-related potentials; Facial mimicry.

People have a fundamental need to belong with others or groups (Baumeister & Leary, 1995). This need comes from the evolutionary history of human beings (Baumeister & Leary, 1995; Macdonald & Leary, 2005). Social exclusion or ostracism thwarts this need and therefore has broad negative consequences, reducing feelings of belonging, self-esteem, control, and meaning (Gonsalkorale & Williams, 2007; van Beest & Williams, 2006; van Beest, Williams, & Dijk, 2011; Williams, 2009; Williams, Cheung, & Choi, 2000; Zadro, Williams, & Richardson, 2004), increasing depression (Nolan, Flynn, & Garber, 2003), and even inducing feelings of pain (Eisenberger,

Jarcho, Lieberman, & Naliboff, 2006; Eisenberger, Lieberman, & Williams, 2003). To avoid such injury, people change their cognition and behavior to regain acceptance or to avoid further rejection following social exclusion. For example, social exclusion has been shown to lead to increased prosocial behavior (Maner, DeWall, Baumeister, & Schaller, 2007) and preference for smiles (Bernstein, Young, Brown, Sacco, & Claypool, 2008; DeWall, Maner, & Rouby, 2009). On the other hand, social exclusion also causes aggression (Leary, Twenge, & Quinlivan, 2006; Warburtona, Williams, & Cairns, 2006; Wesselmann, Butler, Williams, & Pickett, 2010), which prevents

Correspondence should be addressed to: Taishi Kawamoto, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama Higashi-Hiroshima 739-8521, Japan. E-mail: [email protected] *Present affiliation for Mitsuhiro Ura: Department of Psychology, Otemon Gakuin University, Ibaraki, Japan This work was supported by a Grant-in-Aid for JSPS Fellows [24005780] from the Japan Society for Promotion of Science to the first author. This work was also supported by a Grant-in-Aid for Scientific Research (B) [90231183] from the Japan Society for Promotion of Science to the last author.

© 2014 Taylor & Francis

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opportunities to establish new relationships. These behaviors are modulated by signs of acceptance (Maner et al., 2007). That is, people adjust their behavior according to the social cues or situations that follow social exclusion, so as to regulate their belonging status (Gardner, Pickett, & Knowles, 2005; Pickett & Gardner, 2005; Smart Richman & Leary, 2009). A variety of research to date has revealed that social exclusion changes cognition and behavior in the regulation of belonging status. However, little is known about the early neural or automatic behavioral processes by which such changes occur. In their pioneering work, DeWall et al. (2009) conducted a series of experiments using diverse methods; and investigated how social exclusion affected selective attention in response to facial expressions. They found that social exclusion increased selective attention to smiling faces, but not to negative faces, such as disgusted or angry faces. However, several aspects of their findings are in need of further clarification. First, the time course of the stages of processing that were affected by social exclusion was not clarified in their study. Second, DeWall et al. reported no effect of the positive and negative affects that people felt during social exclusion on selective attention to emotional faces. Therefore, the effects of feelings that are specific to social exclusion, such as need threat (i.e., self-esteem, belonging, control, meaningful existence: Williams et al., 2000), remain unclear. Third, automatic responses and feelings of people to emotional faces following social exclusion have not been explicated. Early processes and automatic behaviors following social exclusion could reflect primary belonging regulation (Gardner et al., 2005; Pickett & Gardner, 2005). To examine primary belonging regulation and expand previous findings, we investigated neural and automatic behavioral responses to social cues following social exclusion, using event-related brain potentials (ERPs) and facial electromyograms (EMGs). ERP has high temporal resolution, and it is possible to investigate short and transient brain changes in a stage-by-stage sequentiation (Ibáñez et al., 2012) using this technique. Facial EMGs can be used as a tool for investigating affective responses (Dimberg & Thunberg, 1998; Larsen, Norris, & Cacioppo, 2003). Usage of these two techniques would allow us to investigate the effects of social exclusion on perception, cognitive processes, affect, and automatic behavior in more detail.

Social exclusion and inner/outer monitoring systems Because social exclusion is a quite distressing event, it is not surprising that people have an inner monitoring

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system that is highly sensitive to social exclusion or ostracism. According to sociometer theory, proposed by Leary and his colleagues, state self-esteem serves as a subjective monitor of the degree to which the individual is being accepted or rejected by others (Leary & Baumeister, 2000; Leary, Tambor, Terdal, & Downs, 1995). Ostracism decreases self-esteem and also threatens other fundamental needs (i.e., belonging need, control, and meaningful existence) (Williams, 2009; Williams et al., 2000). In support of sociometer theory, neuroimaging studies suggest that the dorsal anterior cingulate cortex (dACC) serves as a neural alarm system, which signals a relational threat (Eisenberger & Lieberman, 2004; Kawamoto et al., 2012). Because dACC activation is related to enhancement of need threats and decline in state self-esteem (Eisenberger et al., 2003; Eisenberger, Inagaki, Muscatell, Byrne Haltom, & Leary, 2011; Onoda et al., 2010), this activity is a neural index that reflects the individual’s current feeling about his or her belonging status. These findings suggest that people have a subjective or neurobiological system, which signals whether their belonging needs are met or unmet. When individuals are signaled by this inner monitoring system that their belonging needs are unsatisfied, they activate an outer monitoring system, the social monitoring system (SMS). The SMS is an adaptive system that precedes belonging regulation (Gardner et al., 2005; Pickett & Gardner, 2005). In fact, previous studies have revealed that social exclusion promotes performance or preference for social cues such as facial expression (Gardner, Pickett, & Brewer, 2000; Gardner, Pickett, Jefferis, & Knowles, 2005; Pickett, Gardner, & Knowles, 2004). In addition, some evidence indicates that individuals with loneliness or high belongingness need show heightened SMS activation (Gardner et al., 2005; Pickett et al., 2004). Therefore, whether or not fundamental needs are met is highly related to SMS activation. In research on social exclusion, facial expression has often been used as an index of social cues to examine behavioral and cognitive changes following social exclusion (Berenson et al., 2009; Bernstein et al., 2008; Bernstein, Sacco, Brown, Young, & Claypool, 2010; DeWall et al., 2009; Gardner et al., 2005; Pickett et al., 2004) and to evaluate representations of social rejection (Burklund, Eisenberger, & Lieberman, 2007). Smiling faces especially communicate friendliness or social acceptance, whereas disgusted faces communicate social threat or disapproval (DeWall et al., 2009; Parkinson, 2005; Rozin, Lowery, & Ebert, 1994). Thus, we focused on facial expression in order to examine neural or behavioral responses to social cues following social exclusion.

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Neural and behavioral responses to facial expression ERP can be used to investigate the time course of cognitive processes. Of the various ERP components, we focused on P1 and N170, both of which have been widely examined in studies of facial expression. P1 is a positive ERP component which occurs around 80– 100 ms at the lateral occipital site. This component has been linked to visual attention (Hillyard & AnlloVento, 1998). Its amplitude is higher in response to threatening faces as compared to neutral faces (Batty & Taylor, 2003; Holmes, Nielsen, & Green, 2008; Holmes, Nielsen, Tipper, & Green, 2009; Luo, Feng, He, Wang, & Luo, 2010; Pizzagalli, Regard, & Lehmann, 1999), based on rapid detection via a fast magnocellular route (Vuilleumier, 2005). N170 is a negative ERP component that occurs at around 170 ms at the occipitotemporal site. This component increases in response to faces, as compared to object stimuli (Bentin, Allison, Puce, Perez, & McCarthy, 1996). It is commonly held that N170 reflects early facial perception or structural encoding of faces (Bentin et al., 1996; Eimer, 2000), which precedes high-order processing of faces (e.g., identity, gender). A previous finding corroborated this idea by indicating that enhanced N170 amplitude predicted higher facial recognition accuracy (Tamamiya & Hiraki, 2013). Previous studies have reported that a higher N170 amplitude was observed for emotional than for neutral faces (Batty & Taylor, 2003; Blau, Maurer, Tottenham, & McCandliss, 2007) and for positive than for negative faces (Escobar et al., 2013; Ibáñez et al., 2010, in press; Ibáñez, Hurtado, et al., 2011; Ibáñez, Petroni, et al., 2011 Ibáñez, Riveros, et al., 2012; Ibáñez, Urquina, et al., 2012; Petroni et al., 2011). In exclusion studies using behavioral index, increased performance in response to facial expressions, such as identification of emotional faces, was observed following exclusion as compared to inclusion (DeWall et al., 2009; Pickett et al., 2004); similar responses were found in individuals who felt that their belonging need was unsatisfied (Gardner et al., 2005; Pickett & Gardner, 2005; Pickett et al., 2004). Thus, we predicted that N170 amplitude in response to facial stimuli would be larger for exclusion than for inclusion, and N170 amplitude would be related to the degree of need threat which individuals felt. We measured facial EMG activity as well as ERPs. Zygomaticus major activity reflects positive affect, whereas corrugator supercilii activity reflects negative affect (Larsen et al., 2003). Especially in response to facial stimuli, zygomaticus major activity reflects

facial mimicry (Dimberg & Thunberg, 1998). Facial mimicry is a nonverbal communication style that occurs within 1 second of the presentation of facial stimuli (Dimberg & Thunberg, 1998; Weyers, Muhlberger, Hefele, & Pauli, 2006). Prior studies have indicated that facial mimicry is an adaptive response that promotes positive social communication (Dimberg, Thunberg, & Elmehed, 2000; Lakin & Chartrand, 2003; Weyers, Muhlberger, Kund, Hess, & Pauli, 2009). In exclusion research, behavioral mimicry has been found to occur following social exclusion and to be related to the degree of need threat that individuals felt (Lakin, Chartrand, & Arkin, 2008). Thus, we predicted that social exclusion would enhance facial mimicry in response to smiles, and the intensity of mimicry would be related to the degree of need threat felt by individuals.

The present study The aim of the present study was to expose primary belonging regulation processes using electrophysiological methods. To this end, participants were required to play a ball-tossing game called Cyberball, (Williams et al., 2000) and were randomly assigned to exclusion or inclusion conditions. Participants then viewed facial stimuli, which were smiling, neutral, and disgusted. ERP and EMG were measured during the experiments. We hypothesized: (1) N170 amplitude in response to facial expressions would be larger in exclusion than in inclusion conditions. (2) N170 amplitudes would be negatively correlated with selfreported need threat (i.e., participants who reported higher need threat in Cyberball would present higher N170 amplitudes). (3) Zygomaticus major activity in response to a smile would be higher in exclusion than in inclusion conditions. (4) Zygomaticus major activity in response to a smiling face would be positively correlated with self-reported need threat (i.e., participants who reported higher need threat in Cyberball would present higher zygomaticus major activity in response to a smiling face). With regard to aversive responses (i.e., P1, corrugator supercilii), we predicted that neither P1 amplitude nor corrugtor supercilli activity, in response to disgusted faces, would differ between inclusion and exclusion conditions. This prediction was based on two previous studies. First, DeWall et al. (2009) found that social exclusion increased selective attention to smiling faces, but not to negative faces. Second, social inclusion did not have a protective effect, indicating that when inclusion occurred before exclusion, there was no protective benefit (Tang &

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Richardson, 2013). Both studies revealed that social exclusion, or cues of social exclusion were threats even after being included. Therefore, we anticipated that aversive responses would not differ between conditions.

METHOD

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Participants Forty-two healthy undergraduate students (20 females; M = 18.84, SD = .67) participated in the experiment. All of them were right-handed. The protocol was approved by the Research Ethics Committee of the Graduate School of Integrated Arts and Sciences, Hiroshima University. Participants gave written informed consent.

Design and procedure Participants performed two tasks during the experiment in a fixed order. First, they played Cyberball (Williams et al., 2000) with two other players. In this task, they were randomly assigned to either inclusion (N = 22) or exclusion (N = 20) conditions. Participants then performed a facial expression viewing task, which was similar to tasks in previous studies (Leppanen, Moulson, Vogel-Farley, & Nelson, 2007).

Cyberball We used Cyberball to manipulate social exclusion and inclusion (Williams et al., 2000). Cyberball was designed as an ostracism experience, in which participants perceive themselves to be excluded when they are not thrown the ball. Participants were told that Cyberball was a task which engaged “mental visualization”. Participants were instructed to focus on mentally visualizing themselves as tossing the ball back and forth in real life. Participants were tested individually, but were led to believe that they were playing with two other individuals who were taking part in the experiment via the university internet. In reality, the other players did not exist and were controlled by a computer program. Participants in the inclusion condition received the ball equally often throughout the game (i.e., 15 throws) from each of the two computercontrolled confederates, whereas participants in the exclusion condition received the ball once from each of the confederates at the beginning, and then never

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again. Both of the games lasted approximately 3 minutes (i.e., for a total of 45 throws). After finishing the Cyberball task, participants completed a need threat scale which has been widely used in previous studies (Kawamoto et al., 2012; Onoda et al., 2009, 2010; Williams, 2009; Williams et al., 2000). Need threat was measured using four statements designed to assess the participants’ subjective experiences: “I felt liked”, “I felt rejected”, “I felt invisible”, and “I felt powerful.” These experiences were rated on a 9-point scale ranging from 1 (not at all) to 9 (very much). Two items, “I felt liked” and “I felt powerful,” were reverse scored, such that higher scores for each item indicated a greater level of need threat. The average value of the four items was used as an index of need threat.

Facial expression viewing task ERP and EMG were recorded while participants viewed color pictures of individual female and male models (two females and two males) posing with neutral, smiling, and disgusted facial expressions. The pictures were selected from the ATR facial expression database (DB99, ATR Promotions, Kyoto, Japan). Stimulus presentation was controlled by Inquisit software (Millisecond Software, Seattle, Washington, DC, USA) running on a desktop computer, and the stimuli subtended approximately 12 × 16°, when viewed from a distance of 60 cm. The presentation of each facial stimulus was preceded by the presentation of a fixation cross on the center of the screen. After a randomly varying interval ranging from 1500 to 2500 ms, the fixation was replaced by a facial stimulus presented for 1000 ms. Each facial expression was presented 52 times, for a total of 156 test trials. In addition, 13 trials were run in which a checkerboard was presented on the screen to maintain the participants’ attention on the screen. The checkerboards served as target stimuli to which participants were asked to respond by a button press. A total of 169 trials were conducted for the task, which lasted about 8 minutes.

Physiological measurement, recordings, and processing An electroencephalogram (EEG) was recorded at 39 scalp sites using Ag/AgCl electrodes on an elastic cap. Vertical and horizontal electrooculograms were recorded from electrodes attached above and below the left eye and at the outer canthi. Electrode

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impedances were less than 20 KΩ. The signal was recorded with a bandpass filter of 0.016–60 Hz at a sampling rate of 1000 Hz (EEG1100, Nihon-Kohden, Japan) and re-referenced to the nose tip. A finite impulse response (FIR) filter of 0.1–30 Hz was applied to the ERP. Ocular artifacts were corrected using the method of Gratton, Coles, and Donchin (1983) implemented in Brain Vision Analyzer 2.02 (Brain Products, Germany). ERP waveforms were obtained by averaging a 1200 ms period 200 ms before and 1000 ms after the onset of a facial stimulus (i.e., smiling, neutral, and disgusted faces). Trials that contained nonocular artifacts were excluded from averaging. The mean percentage of artifact-free trials for each facial emotion category was 90.6% for smiling, 90.9% for neutral, and 91.6% for disgusted faces. No significant difference was found among facial emotion categories (F(2, 84) = 0.62, p = .54). The amplitude of P1 was measured at O1 and O2 as the mean amplitude 90–130 ms after stimulus onset, where it is typically maximum (Batty & Taylor, 2003; Luo et al., 2010). The N170 was measured at T5 and T6 as the mean amplitude 140–190 ms after stimulus onset, as reported in previous studies (Frühholz, Fehr, & Herrmann, 2009; Frühholz, Jellinghaus, & Herrmann, 2011). EMGs were recorded over the corrugator supercilii above the left eye and over the zygomaticus major using two pairs of miniature electrodes, according to the recommendation of Fridlund and Cacioppo (1986). Electrode impedances were less than 20 KΩ. The raw EMG signal was filtered with a 15 Hz highpass filter to reduce movement- and blink-related artifacts, and rectified. Data were then visually inspected, and data with remaining artifacts were excluded from subsequent analysis. The data were then logarithmically transformed to minimize the impact of extreme values. EMG reactivity was measured as the difference between activity during the 1000 ms stimulus period and activity during the 1000 ms period immediately prior to stimulus onset.

Data analysis To check whether the social exclusion manipulation was successful, an independent t-test (condition: exclusion vs. inclusion) was performed for need threat. For P1 and N170, we conducted 2 (electrode: O1 vs. O2 for P1, T5 vs. T6 for N170) × 2 (condition: exclusion vs. inclusion) × 3 (emotional face: smile vs. neutral vs. disgust) ANOVAs. For EMGs, we performed 2 (condition: exclusion vs. inclusion) × 3 (emotional face: smile vs. neutral vs. disgust)

ANOVAs. Significant results were followed by post hoc analyses. The Holm procedure was used for correcting multiple comparisons. To test our hypothesis, we examined the relationship between need threat scale scores and physiological responses to social cues. To reduce the number of statistical tests, we performed a priori comparisons based on the hypotheses. In the case of N170, the composite global score was calculated by averaging across different facial expressions. For zygomaticus major activity, only the response to smiling faces was used for calculating the correlation. Additionally, we have reported correlation coefficients between the need threat scores and the responses to each facial expression (i.e., smiling, disgusted, and neutral faces).

RESULTS Manipulation check Need threat scale scores were significantly higher in the exclusion condition (M = 7.40, SD = 1.24) than in the inclusion condition (M = 4.75, SD = 1.09), t(40) = 7.39, p < .001. Thus, the exclusion manipulation was successful.

Event-related brain potentials Figure 1 shows the results for P1 amplitude. ANOVA revealed the main effect of an emotional face, F(2, 80) = 3.56, p = .033, η2p = .08; P1 amplitude was larger for the disgusted face than for the neutral face (p = .030). In addition, the interaction between condition and emotional face was marginally significant, F(2, 80) = 2.47, p = .091, η2p = .06. Post hoc analysis revealed that P1 amplitude was larger for the disgusted face than for the neutral face in the exclusion condition (p = .004) but not in the inclusion condition. The main effect of condition was not significant (F(1, 40) = .01, p = .94, η2p < .01). Neither a significant main effect of electrode, F(1, 40) = 2.65, p = .11, η2p = .06, nor significant interactions, which included the factor of electrode, were observed, Fs < .68, ps > .51, η2p < .02. There were no significant correlations between need threat and P1 amplitude (for neutral faces, r = −.12; for smiling faces, r = −.04; for disgusted faces, r = .02). Figure 2 shows the results for N170 amplitude. The ANOVA did not reveal significant main effects, nor were interactions of condition and emotional face observed, Fs < .95, ps > .34, η2p < .02. In addition, we did not observe any significant main effect of electrode, F(1, 40) = .43, p = .52, η2p = .01, nor significant

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Figure 1. Results for P1. (A) Grand mean waveforms for facial expressions at O1 (left) and at O2 (middle), and topography map of each facial expression (right) for inclusion condition. (B) Grand mean waveforms for facial expressions at O1 (left) and at O2 (middle), and topography map of each facial expression (right) for exclusion condition. (C) Mean P1 amplitude as a function of condition and facial expression at O1 (left) and O2 (right). Error bars indicate standard error.

interactions, which included the factor of electrode, Fs < 1.08, ps > .35, η2p < .06. However, need threat was negatively correlated with global scores of N170 amplitude, r = −.34, p = .027 (for neutral faces, r = −.26; for smiling faces, r = −.36; for disgusted faces, r = −.32), indicating that participants who reported higher need threat in Cyberball produced higher N170 amplitudes in response to all faces.

Electromyograms Figure 3 shows the results for zygomaticus major (left) and corrugator supercilii (right) activities. The ANOVA on the measure of zygomaticus major activity revealed a significant two-way interaction, F(2, 80) = 3.29, p = .042, η2p = .08. Post hoc analysis revealed that zygomaticus major activity in response to smiling faces was higher in the exclusion than in the inclusion condition (p = .007). In addition, in the exclusion condition, greater zygomaticus major activity was observed in response to smiling faces compared to disgusted faces (p = .013). This difference

was not observed in the inclusion condition. These findings suggest that zygomaticus major activity selectively enhanced smiling responses following exclusion. The main effects of condition, F(1, 40) = .85, p = .36, η2p = .02, and emotional face were not significant, F(2, 80) = 1.38, p = 26, η2p = .03. There were marginally significant correlations between need threat and zygomaticus major activity in response to smiling faces, r = .29, p = .066 (for disgusted faces, r = −.27; for neutral face, r = −.07). The same analysis was conducted on corrugator supercilii activity. We found a significant main effect of emotional face, F(2, 80) = 3.81, p = .026, η2p = .09; corrugator supercilii activity was larger in response to disgusted faces than to smiling faces (p = .029). Neither the main effect of condition, F(1, 40) = .06, p = .80, η2p < .01, nor the interaction of condition and emotional face was significant, F(2, 80) = .23, p = 79, η2p < .01. Also, we did not observe any significant relationships between need threat and corrugator supercilii activities in response to emotional expressions (for neutral faces, r = −.03; for smiling faces, r = −.12; for disgusted faces, r = −.17).

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Figure 2. Results for N170. (A) Grand mean waveforms for facial expressions at T5 (left) and at T6 (middle), and topography map of each facial expression (right) for inclusion condition. (B) Grand mean waveforms for facial expressions at T5 (left) and at T6 (middle), and topography map of each facial expression (right) for exclusion condition. (C) Mean N170 amplitude as a function of condition and facial expression at T5 (left) and T6 (right). Error bars indicate standard error. (D) Zero-order correlations between need threat and neutral (left), smiling (middle), and disgusted face (right).

Figure 3. Mean zygomaticus major activity (left) and corrugator supercilii activity (right) as a function of condition and facial expression. Error bars indicate standard error.

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DISCUSSION The main goal of the current study was to identify the primary processes of belonging regulation, which are caused by social exclusion. Extending the pioneering work of DeWall et al. (2009), we focused on multiple processing stages and automatic behavioral responses and investigated how social exclusion affected primary perception, cognition, and affect in response to facial expressions. Using electrophysiological methods, we achieved three main results. First, P1 amplitude was larger in response to disgusted faces than to neutral faces, especially in the exclusion condition. Second, although N170 amplitude did not differ for the inclusion and exclusion conditions, N170 amplitude in response to all facial expressions was related to self-reported need threat. Finally, zygomaticus major activity, in response to smiling faces, was larger in the exclusion condition than in the inclusion condition, and this activity was positively correlated with self-reported need threat. These findings suggest that people rapidly and sensitively change their cognitive and behavioral responses after social exclusion and/or after experiencing need threat. Such changes occurred within 1 second following the presentation of social cues, supporting the supposition of previous studies that people have an outer monitoring system which is highly sensitive to social information (Gardner et al., 2000; Gardner Pickett, Jefferis, et al., 2005; Gardner, Pickett, & Knowles, 2005; Pickett & Gardner, 2005; Pickett et al., 2004).

ERP responses to social cues following social exclusion P1 amplitude was larger in response to disgusted faces than to neutral faces. This finding is consistent with prior studies, which revealed that P1 amplitude was larger for threatening faces than for neutral faces (Batty & Taylor, 2003; Pizzagalli et al., 1999). In addition, P1 amplitude was not affected by experimental condition. This concurs with previous findings that social exclusion did not increase attention to faces displaying expressions of threat (DeWall et al., 2009). Our results provide neural-level evidence that social exclusion does not heighten attention to social cues that signal relational threats. Threat-related expressions are assumed to be processed in a privileged fashion due to their high evolutionary relevance (Palermo & Rhodes, 2007; Schupp et al., 2007; Schupp, Junghofer, Weike, & Hamm, 2004; Vuilleumier & Pourtois, 2007); thus P1 amplitude, in

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response to disgusted faces, did not differ between conditions. Notably, an emotional difference was observed mainly for participants in the exclusion condition. Previous studies indicated that trait social anxiety modulates the emotional effect on P1 amplitude, with a remarkable effect of high trait anxiety on P1 amplitude (Holmes et al., 2008; Li, Zinbarg, Boehm, & Paller, 2008). Our findings imply that situational factors, in addition to individual differences, have emotional effects on P1 amplitude. In addition, to the best of our knowledge, the present study is the first to show an attentional difference between disgusted and neutral faces following social exclusion. Prior studies indicated that social exclusion leads to increased memory for social events or to better identification of facial expression, regardless of valence (Gardner et al., 2000; Pickett et al., 2004). Our results demonstrate that at early perceptual levels, social exclusion changes the allocation of attention to disgusted and neutral expressions. Such changes may lead to better performance in high-level processing, such as identification of facial expressions. Notably, N170 amplitudes in response to facial expressions were related to self-reported need threat. Previous studies found that heightened belonging need or loneliness promotes identification of emotional faces (Gardner et al., 2005; Pickett et al., 2004). Our results concur, and also provide evidence that need threat is related to enhancement not only of high-order behavioral responses but also to responses at early perceptual levels. Because N170 reflects structural encoding of faces, which precedes highorder processing of faces (Bentin et al., 1996; Eimer, 2000; Eimer & Holmes, 2007; Eimer, Holmes, & McGlone, 2003), our results may reflect the effort to regulate belonging status in advance of higher processing (e.g., identifying facial expression). Unexpectedly, however, we did not find significant differences between social exclusion and inclusion for N170 amplitude. This is inconsistent with prior studies, in which social exclusion increased preference or performance with respect to social cues (Bernstein et al., 2008, 2010; DeWall et al., 2009; Gardner et al., 2000). Here, social exclusion did not appear to promote processing with regard to primary facial encoding. Rather, whether or not a fundamental need is met may be highly related to primary processing of facial encoding. In line with this possibility, it has been shown that individuals high in the need to belong showed improved memory for social events and identification of emotional faces (Gardner et al., 2000; Gardner Pickett, Jefferis, et al., 2005; Pickett et al., 2004). Therefore, our

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results imply that primary processing of faces is sensitively related to the need threat experienced by individuals, rather than their experience of social exclusion.

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EMG responses to social cues following social exclusion Our EMG findings revealed that excluded people increased their zygomaticus major activity in response to smiles. Zygomaticus major activity tended to be positively related to the need threat which participants experienced during Cyberball. These findings align with past research, which revealed that social exclusion promotes behavioral mimicry (Lakin et al., 2008) and increases preference for smiles (Bernstein et al., 2008, 2010; DeWall et al., 2009). Facial mimicry, which is reflected in zygomaticus major activity, is a nonverbal behavior which occurs without consciousness and is closely related to empathy or emotional understanding of others (Dimberg et al., 2000; Lakin & Chartrand, 2003; Weyers et al., 2006). Unlike prior research that examined behavioral mimicry during face-to-face interactions (Lakin et al., 2008), our study used pictures of strangers, with whom participants would not expect to have future interactions. Our results therefore expand previous findings to suggest that people react at the automatic behavioral level to gain acceptance even when social affirmation is only a remote possibility. On the other hand, we did not observe a difference in corrugator supercilii activity between conditions, but there was difference between smiling and disgusted faces across conditions. This is consistent with our finding for P1 in response to disgusted faces, which also did not differ between conditions. Prior research has indicated that even the slightest hint of social exclusion causes increased need threat and/or negative affect (Gonsalkorale & Williams, 2007; van Beest & Williams, 2006; Wirth, Sacco, Hugenberg, & Williams, 2010; Zadro et al., 2004), and such effects do not diminish even with experiences of social inclusion beforehand (Tang & Richardson, 2013). Our findings also suggest that social exclusion cues are aversive even after the experience of social inclusion, because such social cues are evolutionarily highly salient (Eisenberger & Lieberman, 2004; Macdonald & Leary, 2005; Palermo & Rhodes, 2007; Schupp et al., 2004; Vuilleumier & Pourtois, 2007).

Limitations and future directions There were several limitations to this study. First, the present study focused on social cues and did not examine nonsocial positive or negative cues. Previous research has suggested that cognitive changes may not be observed in response to nonsocial positive/negative cues (DeWall et al., 2009; Gardner et al., 2000; Pickett et al., 2004). Therefore additional research is required to investigate whether our results apply only to social cues or may also apply to nonsocial cues. Second, although we revealed a particular effect of smiles on EMG activities following social exclusion, we did not observe an effect of smiles on ERP components. By contrast, a prior study observed selective attention toward smiles following social exclusion (DeWall et al., 2009). In this task, multiple faces were simultaneously presented, whereas a single face was presented in the present task. Therefore, it is possible that task differences may have led to different results. Future research using a selective attention task would more thoroughly examine the dominance of smiles following social exclusion. Third, in contrast to previous studies, we did not find any emotional category effects on N170. Previous studies have shown that N170 might become habituated after only a few types of face stimuli are used (Kuehl, Brandt, Hahn, Dettling, & Neuhaus, 2013; Maurer, Rossion, & McCandliss, 2008; Mercure, Cohen Kadosh, & Johnson, 2011). Our study used four types of faces, therefore, the lack of emotion category effects might be due to N170 habituation. Future studies would benefit from using more types of facial stimuli to investigate emotional category effects on N170. Finally, the P1 effect observed in this study was only a trend and its effect size was small. Further studies are needed to investigate if the results of this study can be replicated.

CONCLUSION In sum, the present research demonstrated that people rapidly and selectively changed their neural and behavioral responses in response to social cues following social exclusion and/or along with a felt need threat. In particular, excluded people changed their attentional allocation to emotional faces and also increased their behavioral mimicry of smiling faces. Furthermore, structural encoding of emotional faces, which is reflected by N170 amplitude, was modulated by the feeling of a need threat. We consider these

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findings to reflect the primary regulation of belonging at early perceptual and behavioral levels. Original manuscript received 9 June 2013 Revised manuscript accepted 9 January 2014 First published online 3 February 2014

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