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Emotion. Author manuscript; available in PMC 2017 October 01. Published in final edited form as: Emotion. 2016 October ; 16(7): 1033–1039. doi:10.1037/emo0000201.
Cultural Modes of Expressing Emotions Influence How Emotions Are Experienced Mary Helen Immordino-Yang1,2,3,*, Xiao-Fei Yang1,3, and Hanna Damasio1,3,4 1Brain
and Creativity Institute, University of Southern California, Los Angeles, CA 90089, USA
2Rossier
School of Education, University of Southern California, Los Angeles, CA 90089, USA
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3Neuroscience
Graduate Program, University of Southern California, Los Angeles, CA 90089,
USA 4Dornsife
Cognitive Neuroscience Imaging Center, University of Southern California, Los Angeles, CA 90089, USA
Abstract
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The brain’s mapping of bodily responses during emotion contributes to emotional experiences, or feelings. Culture influences emotional expressiveness, i.e. the magnitude of individuals’ bodily responses during emotion. So, are cultural influences on behavioral expressiveness associated with differences in how individuals experience emotion? Chinese and American young adults reported how strongly admiration and compassion-inducing stories made them feel, first in a private interview and then during fMRI. As expected, Americans were more expressive in the interview. While expressiveness did not predict stronger reported feelings or neural responses during fMRI, in both cultural groups more expressive people showed tighter trial-by-trial correlations between their experienced strength of emotion and activations in visceral-somatosensory cortex, even after controlling for individuals’ overall strength of reactions (neural and felt). Moreover, expressiveness mediated a previously described cultural effect in which activations in visceralsomatosensory cortex correlated with feeling strength among Americans but not among Chinese. Post-hoc supplementary analyses revealed that more expressive individuals reached peak activation of visceral-somatosensory cortex later in the emotion process and took longer to decide how strongly they felt. The results together suggest that differences in expressiveness correspond to differences in how somatosensory mechanisms contribute to constructing conscious feelings. By influencing expressiveness, culture may therefore influence how individuals know how strongly they feel, what conscious feelings are based on, or possibly what strong versus weak emotions “feel like.”
Correspondence to: Mary Helen Immordino-Yang, Brain and Creativity Institute & Rossier School of Education, University of Southern California, 3620A McClintock Ave, Room 267, Los Angeles, CA 90089-2921, [email protected]. Author Contributions MHI-Y and HD initiated a cross-cultural experiment. MHI-Y and X-FY designed the experiment, collected and analyzed the data. MHI-Y and X-FY wrote the paper, and HD provided critical feedback. All authors approved the final version of the manuscript for submission.
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Keywords East-West differences; subjective affect; insula; development; mental health
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In October, 2012, the world was swept by admiration for a Pakistani schoolgirl who resisted the Taliban. In December of that year, parents across the world were overwhelmed with compassion for the families of 20 American schoolchildren killed alongside their teachers. Upon learning of these events, some wept openly; others expressed their emotion more calmly, in a less behaviorally reactive manner. Cultural norms and values, such as individualism/collectivism (Markus & Kitayama, 1991), ideal affect (Tsai, 2007) and display rules, shape these styles of emotional expression (Ekman, 1971; Matsumoto et al., 2008; Mesquita & Frijda, 1992; Parkinson, Fischer, & Manstead, 2005). However, it is not clear whether these styles of expression correspond to differences in the way individuals experience their own emotions. Do calmer and more expressive individuals experience emotions in the same way?
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Emotions are, at their core, neural and somatic events whose evolutionary function is to prepare an organism to respond adaptively to a change in physical or social circumstances (Darwin, 1872; James, 1894). Once emotions are induced, people can become conscious of them (i.e., experience their emotions) by mentally constructing a feeling (Barrett, Mesquita, Ochsner, & Gross, 2007; Damasio, 1999). Neurobiologically, constructing feelings of emotions recruits brain systems that regulate and map body responses (Craig, 2002; Damasio & Carvalho, 2013). Psychologically, though, feelings are potentially as reliant on inferences and predictions about body states as on afferent interoceptive information (Seth, 2013). Feelings are socially and conceptually mediated, culturally variable, complex and dynamic, suggesting that they reflect context and development (Barrett et al., 2007; Barrett, 2012; Immordino-Yang, 2010).
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Given that feelings are supported by neural systems that map body states, and that feelings are conceptually mediated, could differences in how individuals habitually express emotions be associated with differences in the processes by which those individuals feel their emotions? Presumably, individuals whose emotions manifest in larger, more marked bodily/ behavioral responses would find those responses more salient and, potentially, informative. More expressive people could therefore learn to rely more heavily on the feeling of embodied reactions in deciding their current feeling strength. Over time, this difference could lead to a style of processing in which conscious feelings of emotion are more strongly associated with brain activity in somatosensory systems, whether this brain activity reflects real or simulated body states (Damasio, 1999; Seth, 2013). In essence, expressiveness could shift the sorts of embodied sensations, inferences and predictions that underlie conscious experiences of emotion (Immordino-Yang, 2010). We decided to investigate this possibility by testing whether behavioral expressiveness is associated with differences in how feeling strength correlates with fluctuations in neural activity in somatosensory cortices. Our region of interest was the dorsal Anterior Insula (dAI), a neural region important for interoception, emotion awareness, and social-emotional feelings (Craig, 2002; Critchley, Wiens, Rotshtein, Öhman, & Dolan, 2004; Damasio, 1999; Emotion. Author manuscript; available in PMC 2017 October 01.
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Immordino-Yang, McColl, Damasio, & Damasio, 2009; Zaki, Davis, & Ochsner, 2012). As the hub of the salience network, this region is heavily interconnected with frontal and limbic regions (Seeley et al., 2007). During emotion, the dAI can be thought of as providing a dynamic, integrative map of emotion-related body responses so that they have the possibility of informing conscious cognitive processing.
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Because emotional calmness is culturally valued in China while emotional expressiveness is valued in the United States (Bond, 1993; Markus & Kitayama, 1991; Tsai, 2007), we studied, as a first step, Chinese and American participants recruited from two similarly urban and academically competitive university communities, one in Beijing and one in Los Angeles. Additional investigations will be required to disentangle the multiple factors possibly contributing to differences in expressiveness, such as emotional ideals (e.g., those associated with individualism and collectivism), adaptation to cultural norms for emotion suppression and display, and individuals’ inherent biological reactivity and personal history. Here, we were interested to establish a link between natural emotional behavior and the neural correlates of emotional feelings in these two cultural contexts. We hypothesized that expressive people would feel their reactions differently—by a habitual psychological process that privileges embodiment—and that this difference would not be explained by expressive people reacting more strongly. We therefore tested the effect of behavioral expressiveness on the neural correlates of emotional feelings controlling for individuals’ average reported feeling strength and average neural activation magnitude during emotion processing.
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Overview of Procedures (1) During a videotaped two-hour private interview, participants reacted naturally to true stories inducing varieties of admiration and compassion. Participants’ behavioral reactions to a subset of stories involving painful physical injuries were used to index expressiveness (as these reactions are quick and relatively automatic). (2) During fMRI scanning, participants reacted again to the stories and reported their strength of feelings to each story in real time. For each participant, we calculated the strength of trial-by-trial correlation between neural activity fluctuations and reported feeling strength. Overview of Analytic Plan
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We tested whether: (a) the American group was more expressive than the Chinese group. We then tested whether individual differences in expressiveness predict: (b) the strength of feelings individuals experienced during scanning, and (c) the magnitude of the neural activation. Next, controlling for individuals’ average strength of feelings during scanning and average neural activation magnitude, we tested whether individuals’ expressiveness: (d) moderates the trial-by-trial correlation between dAI neural response and feeling strength. To test for the anatomical specificity of our effect, we: (e) analyzed the results from the ventral AI sector, involved in autonomic regulation and emotion induction (Kurth, Zilles, Fox, Laird, & Eickhoff, 2010; Mesulam & Mufson, 1982).
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The fMRI data were collected as part of a larger international project, briefly described below. An earlier study in this project examined the neural activity correlates of feeling strength at the group level (Immordino-Yang, Yang, & Damasio, 2014). Among other findings, it showed that activity in the dAI correlated with feeling strength in American groups (including in a group of East-Asian Americans), but not in Chinese groups. By contrast, activity in the vAI correlated with feelings in American and in Chinese groups. Because of that earlier finding, we expanded our originally planned analyses to: (f) test whether expressiveness would mediate the previously described cultural group difference in how dAI activity correlates with feelings. Finally, to strengthen our interpretation of the results, we conducted post hoc analyses of the effects of culture and expressiveness on time to emotion induction and awareness, presented in Supplemental Material.
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Statement on Sample, Measures, Manipulations and Data Exclusions The data for the current study were collected as part of a larger project investigating cultural influences on lifespan development of social emotion processing and its neurobiological correlates in multiple cultural contexts (n = 143). From the larger project sample we selected all Chinese and American young adults (aged 18–30) who had been born in the country where they currently live. (Participants who were not from a Chinese or an American background, who had immigrated, or who were outside this age range were excluded.) The sample partially overlaps with the sample used in Immordino-Yang et al., 2014. One qualified Chinese participant was excluded because she refused consent to be videotaped during the interview.
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Electrocardiograms (ECG) were collected simultaneously with neuroimaging in 44 of the participants (in all of the Americans and in 15 of the Chinese participants). All other manipulations, measures, and data exclusions in the study are reported. Participants Participants reported on a standard fMRI eligibility questionnaire that they were healthy, right-handed, neurologically normal, and with no history of psychiatric disorder, physical or emotional abuse. All reported normal hearing and normal or corrected-to-normal vision. All participants gave written informed consent in accordance with the requirements of the Institutional Review Boards of the University of Southern California (USC) or Beijing Normal University (BNU) and were compensated for their participation in accordance with their university’s norms.
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Chinese Group—28 Mandarin-speaking Chinese students from the BNU community (14 females; average age 22.9 years, SD = 3.1). All had been born and raised in mainland China. American Group—29 English-speaking American students from the USC community (16 females; average age 21.1 years, SD = 2.7; 12 participants identified as European-American, 13 as East-Asian, 2 as Latino and 2 as African-American). All had been born and raised in the U.S. Throughout the study, we tested our effects separately for the East-Asian Americans
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and for the Americans not of Asian descent. Since we found no differences in relations among expressiveness, feelings and neural activity, we collapsed the Americans into one group. For completeness, we also report the results from the East-Asian Americans for the major analyses. Stimuli
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All participants were presented with the same video stimuli, subtitled in the participants’ native language. (That is, participants saw half the videos in their native language and half in the other language, with all videos subtitled in their native language.) Subtitles were composed, translated and verified by native speakers. Narrative stimuli depicted compelling, true stories that unfolded like mini documentaries. Half of the stimuli featured Chinese protagonists and half featured Americans in equivalent situations (no American protagonists were of Asian descent). The corpus of 40 emotional narratives was balanced for positive and negative stories. (Stories had been piloted to induce varieties of admiration and of compassion/empathy.) 10 additional control narratives were piloted to be equivalently interesting but otherwise less emotion provoking, and were included to ensure that participants experienced a range of strengths of emotional reactions across the experiment. For example, one control stimulus featured the story of a professional man who decides to become a stay-at-home father. For additional details, see Immordino-Yang et al., 2014. Each video stimulus was prepared in two versions. A full length version (average length 43 seconds) was utilized in the pre-scan interview; a 5-second segment depicting the emotional crux of the narrative was shown in the scanner. Protocol
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Participants were told that they would be exposed to a series of true stories about real people’s lives, and that they should feel comfortable reporting their honest feelings in response to each. Participants were not told that we were studying emotional expressiveness.
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Adapting a previously developed protocol (see Immordino-Yang et al., 2009), participants were first introduced to the narrative stimuli in a private, videotaped interview in which an experimenter recounted each narrative verbally using a memorized script that began, “This is a story of a man/woman who…”, and included a brief description of the protagonist’s circumstances and accomplishments, followed by supplementary video images of the narrative protagonist shown on a laptop computer. Each narrative took between 60 and 90 seconds to present (including showing the full-length video) and finished with the experimenter asking, “How does this person’s story make you feel?” ”]. The experimenter then unobtrusively gazed downward into her [“ notebook and transcribed some words from the participants’ response as the participant described his/her reactions in an open-ended manner. Participants were told that the experimenter was taking notes in case the video camera failed. In actuality, this note-taking was also intended to standardize the experimenter’s behavior so that she would not inadvertently influence the behavior of the participant during the response phase. The interview took place in a quiet room on the university campus and was conducted by an experimenter of the same nationality as the participant (Immordino-Yang conducted the
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sessions in Los Angeles; Yang conducted those in Beijing). Narratives were presented in one of two counterbalanced orders. Prior to running the experiment, the experimenters extensively rehearsed the narrative scripts and reviewed together videotapes of practice preparation sessions with the aim of relaying the narratives consistently and equivalently. The interview lasted approximately 2 hours.
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Participants were then given a short break (~10 minutes). They then underwent BOLD fMRI as they viewed 5-second videos depicting the crux of each narrative with one sentence of verbal information from the preparation session delivered both auditorily (from a recording) and underneath the image in stationary Mandarin or English text, followed by 13 seconds of gray screen. A cross was shown for 2 seconds to separate trials. For each trial, participants reported via button press the real-time strength of their feeling once they became aware of it (one press per trial, at any point during the trial). Participants could report “no emotion,” “moderate emotion,” “strong emotion” or “overwhelmingly strong emotion.” Before the scanning session, experimenters stressed to participants that they should report their experienced strength of emotion at the current time. Participants confirmed their responses in a brief post-scan interview. Participants were shown each narrative twice over the course of the fMRI experiment for a total of 100 trials divided into four runs of approximately 9 minutes each. The two presentations of the same narrative were never shown during the same run. Analysis of Behavioral Expressiveness
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To gauge participants’ emotional expressiveness during the interview, participants’ reactions to narratives meant to elicit empathy/compassion for physical pain were coded. (These 10 narratives were a subset of the compassion stimuli, and depicted protagonists sustaining accidental painful injuries, e.g. a broken leg.) We chose to analyze only these interview trials for simplicity and reliability, as the phenotype of this emotion is relatively culturally universal and better known than the phenotypes of the other emotions induced. In addition, we had previously shown that behavioral responses to these videos were faster and that neural activity ramped up and dissipated more quickly (Immordino-Yang et al., 2009). We interpreted these findings as evidence that empathic reactions to physical pain are less nuanced and more automatic than reactions to admirable and socially painful stories. Coding the slower evolving admiration and compassion for social pain reactions could have made our results more susceptible to influence by display rules, suppression and other factors. For these reasons, we judged that the empathy for physical pain trials could capture participants’ natural behavior in a more direct way, and could provide a good, general, cross-culturally valid index of each participant’s natural behavioral reactiveness in this context. Each participant’s reactions were independently coded by at least one Chinese and one American expert rater blind to the study hypotheses. Coding was done with the sound off. Participants’ reactions to each stimulus were rated on a scale of 1–4 (the most expressive behavior evidenced determined the rating): 1.
Participant remained calm and showed no visible change in facial expression;
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2.
Participant tightened his/her facial muscles and noticeably blinked his/her eyes;
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Participant flinched, visibly lifted his/her shoulders, and/or covered his/her face with his/her hand(s);
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Participant displayed a strong facial expression and avoidant behavior, either pushing back his/her chair from the table or turning his/her upper body away from the stimulus.
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Inter-rater-reliability scores were all within the “excellent” range (Cohen’s Kappa > .84). Discrepancies between raters were resolved by discussion. As we were interested in a general index capturing the participants’ strongest reactions in this context, the three highest scores for each participant were averaged to produce an expressiveness score. (We did also test using the average of all trials, and the results remain significant, though variance explained decreased from approximately 18% to 10%.) fMRI data acquisition and processing Because the neuroimaging data for this study were collected as part of a larger project, the fMRI methods are only summarized here (for details see Immordino-Yang et al., 2014).
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The same scanner model and sequences were used to collect neuroimaging data at BNU Imaging Center for Brain Research and at USC Dana and David Dornsife Neuroimaging Center. Throughout the analyses, we implemented methods to account for brain size and shape differences. Data from one male Chinese participant were excluded due to excessive head movement (the participant coughed repeatedly). The remaining data underwent standard preprocessing and co-registration to the anatomical images in MNI space using SPM8 (Wellcome Department of Cognitive Neurology, London, UK). Calculating the effects of expressiveness on neural activity in the whole brain At the individual level, we modeled each participant’s task-related neural response using the method described in Immordino-Yang et al., 2014. For each participant, a contrast map of emotion versus implicit baseline was calculated. These contrast maps were entered into a group level whole-brain regression analysis, using expressiveness as the independent variable. Calculating the correlation between AI BOLD response and feeling strength for each participant
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The right and left dorsal and ventral AI volumes of interest were functionally defined using the contrast of emotion versus control for the conjunction of the groups, thresholded at p < . 005 uncorrected, then anatomically delimited and individually verified on each participant’s anatomy. See Figure 1 for views of the VOIs, and Immordino-Yang et al., 2014 for details. The time course of the BOLD signal for the average of the voxels within each volume of interest across each trial was extracted for each participant. To calculate each participant’s strength of trial-by-trial correlation between dAI BOLD response and reported feeling strength, we first averaged together the BOLD time courses
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corresponding to the two presentations of the same narrative stimulus (from different neuroimaging runs; this procedure served to improve the BOLD signal-to-noise ratio). Next, excluding the first two TRs (to accommodate the hemodynamic delay), we identified the peak value of the resulting time course (the local maximum of greatest magnitude). Finally, we averaged the button press values corresponding to the participant’s feeling strength during the two presentations of the same narrative. These procedures yielded 50 pairs of values for each participant from which to calculate the correlation coefficient. These procedures were then repeated for the vAI. (Parametric modulation analysis corroborated our findings; see Supplemental Material A). Testing the moderation hypothesis
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We tested whether expressiveness moderates the strength of correlation between dAI BOLD signal magnitude and feeling strength. To do this, the correlation coefficients calculated above were entered into a group-level linear regression model with behavioral expressiveness as the independent variable. Each participant’s average reported feeling strength, average peak BOLD magnitude in the dAI, and age were included in the model as covariates of no interest. (We controlled for age because the American group was slightly but significantly younger than the Chinese group.) Testing for the anatomical specificity of the moderation effect
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To test whether the moderation effect is specific to the dorsal sector of the AI, we tested whether expressiveness significantly moderates the strength of correlation between BOLD signal magnitude and feeling strength: first, in the vAI; second, in the vAI after partialling out variance in BOLD signal shared with the dAI; and third, in the dAI after partialling out variance in BOLD signal shared with the vAI. Testing the mediation hypothesis We have previously reported a cultural group difference in the strength of trial-by-trial correlation between dAI peak BOLD magnitude and participants’ feeling strength (Immordino-Yang et al., 2014). Here we wanted to establish whether participants’ expressiveness would mediate this group difference, controlling for participants’ average reported feeling strength, average peak BOLD magnitude in dAI and age. Using the biascorrected bootstrapping procedure described by Preacher & Hayes (2008) and implemented in SPSS 18, mediation effects were computed for each of 10,000 bootstrapped samples to determine the 99% confidence interval of the effect.
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Results Consistent with expectations, the American group was more expressive than the Chinese group (t[55] = 3.91, p < .001, Cohen’s d = 1.03, 99% CI [.16, .84]; we note that the EastAsian Americans were less expressive than the Americans not of Asian descent, t[27] = −2.13, p = .04, Cohen’s d = −.82, 95% CI [−.70, −0.01], and non-significantly more expressive than the Chinese group (t[39] = 1.94, p = .06, Cohen’s d = .68, 95% CI [−.01, .
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61]). Variance in expressiveness was equivalent between the American and Chinese groups (Levene’s test for equality of variances, F[1,55] = .80, p = .78). Neither cultural group nor gender experienced significantly stronger/weaker emotions. Men showed a greater effect of culture on expressiveness than women (interaction: F[1,56] = 12.58, p = .001, ηp2 = .183). See Table 1. Also consistent with expectations, more expressive participants did not report stronger feelings (r[54] = .02, p = .32, R2 = .00) and did not show greater neural responses in dAI, vAI or in any region of the brain involved in emotion or social processing, including in the amygdala, cingulate cortex, medial frontal cortex, precuneus, temporoparietal junction, or in other sectors of the insula (even using the lenient threshold of p < .01 uncorrected for multiple comparisons).
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However, as hypothesized, more expressive participants showed stronger trial-by-trial correlations between fluctuations in feeling strength and fluctuations in peak dAI BOLD magnitude (F[1,51] = 11.28, p=.001, ηp2 = .181). The relationship was positive for each variety of emotion induced when separately examined (ηp2admiration = .062; ηp2compassion = . 094). The effect was stronger for women (ηp2males = .123; ηp2females = .282; gender interaction: F[1,52] = 4.05, p = .049, ηp2 = .072). East-Asian Americans showed similar results to Americans not of Asian descent (i.e., no significant interaction: F[1,22] = .213, p = .649, ηp2 = .010). See also Figure 2.
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As evidence of the anatomical specificity of the effect, we found that expressiveness was related to the trial-by-trial correlation between feeling strength and BOLD magnitude in the ventral AI (the autonomic modulatory sector; F[1,51] = 5.34, p = .03, ηp2 = .095), but that this relationship became non-significant and small after controlling for variance shared with the dAI (F[1,51] = .88, p = .35, ηp2 = .017). By contrast, expressiveness significantly moderated the trial-by-trial correlation between feeling strength and BOLD magnitude in the dAI even after controlling for BOLD variance shared with the vAI (F[1,51] = 7.17, p = .01, ηp2 = .123). As illustrated in Figure 3, individual differences in participants’ expressiveness mediated the previously reported cultural group difference in the trial-by-trial correlation between dAI peak BOLD magnitude and feeling strength. The mean of the bootstrapped mediation effect was .09 with standard error .04; the 99% confidence interval ranged from .01 to .23 (statistically significant because it does not cross zero).
Post hoc analyses Author Manuscript
Given our positive results, we undertook a series of post hoc analyses to strengthen the interpretation that our findings are due to effects of expressiveness on the feeling process and not to effects of expressiveness on emotion induction. Emotions must be induced before they can be felt (Damasio et al., 2000) and constructing feelings (including neurally mapping or simulating the body response) takes time. We therefore reasoned that expressiveness should be associated with delays in emotion awareness and its neural correlate, dorsal AI activation (Craig, 2002; Immordino-Yang et al., 2014; Zaki et al., 2012).
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But, there should be no delays in emotion induction, i.e. in the time required for the initial cognitive appraisal of the stimulus and the subsequent induction of the vAI activation and psychophysiological response. Given these hypotheses, we returned to the data from the participants for whom we had collected ECG (see Supplemental Material B). We found that expressiveness was not associated with delays in peak cardiac response or vAI activation (indices of emotion induction), but that expressiveness was associated with delays in dAI activation and participants’ reports of feelings (indices of emotion awareness).
Discussion
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Culture is known to affect ideals for emotional arousal (Tsai, 2007) and norms for emotional display (Matsumoto, 1990), as well as how often and how strongly individuals experience emotions in their daily lives (Bond, 1993; Eid & Diener, 2001; Wallbott & Scherer, 1988). Here we show that cultural influences on emotional behavior also relate to differences in the process by which individuals feel emotions, once they are induced. By combining subjective reports of feeling strength with neuroimaging in participants whose natural emotional behavior we had characterized, we demonstrated that: (1) for both Chinese and American cultural groups (and for the sub-group of Americans of East-Asian descent), the more expressive an individual, the more tightly fluctuations in experienced feeling strength correlated with fluctuations in neural response magnitude in visceral somatosensory cortex (dAI); (2) expressiveness also mediated a previously reported cultural group difference in which dAI activity correlated with feeling strength only in American participant groups. Notably, the effects were consistent across the range of emotions induced, and held after controlling for individuals’ average emotional reactivity (neural and felt). Interestingly, we found no evidence that more expressive individuals (or that Americans) had stronger feelings or stronger neural responses to the stimuli—only that their feelings correlated with neural activity differently. Our post hoc analyses suggest that expressiveness influenced the processing of feelings, rather than the induction of emotion.
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More work is needed to understand the developmental origins and underlying mechanisms of these effects, and to disentangle effects of emotion regulation, ideal affect and other factors. Cultural and individual differences in the embodied experiences of emotion have long been a focus of inquiry (Barrett et al., 2007; Cohen & Leung, 2009; Dunn et al., 2010; Eid & Diener, 2001; Saxbe, Yang, Borofsky, & Immordino-Yang, 2013). Our findings collectively suggest that by modulating bodily expression, culture also influences how somatosensory neural activity becomes associated with subjective affect (i.e., how individuals know how strongly they feel, or what emotional feelings are based on, or possibly what strong versus weak emotions “feel like”). Our study is limited in that we did not seek to disentangle culture and nationality, or to probe the origins of the differences in expressiveness we measured. We also measured only emotional intensity and not which specific emotions participants experienced to each narrative. However, by connecting observable emotional behaviors to private emotional experiences and their underlying neural substrate, we aim to enhance understanding and appreciation of cultural learning and the diversity of human experiences. The findings have important implications for social
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development and education, for mental health and psychiatry, and for theoretical models of emotional feelings.
Supplementary Material Refer to Web version on PubMed Central for supplementary material.
Acknowledgments MHIY was supported by NSF CAREER 11519520; the Brain and Creativity Institute Research Fund; the University of Southern California Provost; the Rossier School of Education; H. Damasio and MHIY were supported by National Institute of Health [P01 NS19632] to H. Damasio and A. Damasio; X-FY was funded by the USC Neuroscience Graduate Program Fellowship and the USC US-China Institute Summer Fieldwork Grant.
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R. Zhou secured access to BNU Imaging Center for Brain Research and Chinese participants; We thank A. Damasio, S. Kitayama, The Stanford Culture Collab., Y. Chentsova-Dutton, J. Parvizi, L. Young, E. Winner, H. Gardner, D. Daniel for discussions; J. Kaplan, S. Wong, L. Zhu for neuroimaging advice; M. Lay, B. Sanders, D. Yeung, A. Goldman, E. O’Day, T. Nanda, R. Atticus, J. Flores for help with data analysis.
References
Author Manuscript Author Manuscript
Barrett LF. Emotions are real. Emotion. 2012; 12(3):413–29. DOI: 10.1037/a0027555 [PubMed: 22642358] Barrett LF, Mesquita B, Ochsner KN, Gross JJ. The experience of emotion. Annual Review of Psychology. 2007; 58:373–403. DOI: 10.1146/annurev.psych.58.110405.085709 Bond MH. Emotions and their expression in Chinese culture. Journal of Nonverbal Behavior. 1993; 17(4):245–262. DOI: 10.1007/BF00987240 Cohen D, Leung AKY. The hard embodiment of culture. European Journal of Social Psychology. 2009; 39:1278–1289. DOI: 10.1002/ejsp Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience. 2002; 3(8):655–66. DOI: 10.1038/nrn894 [PubMed: 12154366] Critchley HD, Wiens S, Rotshtein P, Öhman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nature Neuroscience. 2004; 7:189– 195. DOI: 10.1038/nn1176 [PubMed: 14730305] Damasio, AR. The feeling of what happens: Body and emotion in the making of consciousness. New York: Harcourt; 1999. Damasio AR, Carvalho GB. The nature of feelings: Evolutionary and neurobiological origins. Nature Reviews Neuroscience. 2013; 14(2):143–152. DOI: 10.1038/nrn3403 [PubMed: 23329161] Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LLB, Parvizi J, Hichwa RD. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience. 2000; 3(10):1049–1056. DOI: 10.1038/79871 [PubMed: 11017179] Darwin, C. The expression of the emotions in man and animals. London: John Murray; 1872. Dunn BD, Galton HC, Morgan R, Evans D, Oliver C, Meyer M, et al. Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science. 2010; 21(12):1835–44. DOI: 10.1177/0956797610389191 [PubMed: 21106893] Eid M, Diener E. Norms for experiencing emotions in different cultures: Inter- and intranational differences. Journal of Personality and Social Psychology. 2001; 81(5):869–885. DOI: 10.1037//0022-3514.81.5.869 [PubMed: 11708563] Ekman P. Universals and cultural differences in facial expressions of emotion. Nebraska Symposium on Motivation. 1971; 19:207–283. Immordino-Yang MH. Toward a microdevelopmental, interdisciplinary approach to social emotion. Emotion Review. 2010; 2(3):217–220. DOI: 10.1177/1754073910361985 Immordino-Yang MH, McColl A, Damasio H, Damasio AR. Neural correlates of admiration and compassion. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(19):8021–6. DOI: 10.1073/pnas.0810363106 [PubMed: 19414310]
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Immordino-Yang MH, Yang XF, Damasio H. Correlations between social-emotional feelings and anterior insula activity are independent from visceral states but influenced by culture. Frontiers in Human Neuroscience. 2014; 8:728.doi: 10.3389/fnhum.2014.00728 [PubMed: 25278862] James W. Discussion: The physical basis of emotion. Psychological Review. 1894; 1(5):516–529. DOI: 10.1037/h0065078 Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB. A link between the systems: Functional differentiation and integration within the human insula revealed by meta-analysis. Brain Structure & Function. 2010; 214(5–6):519–34. DOI: 10.1007/s00429-010-0255-z [PubMed: 20512376] Markus HR, Kitayama S. Culture and the self: Implications for cognition, emotion, and motivation. Psychological Review. 1991; 98(2):253–224. DOI: 10.1037/0033-295X.98.2.224 Matsumoto D. Cultural similarities and differences in display rules. Motivation and Emotion. 1990; 14(3):195–214. DOI: 10.1007/BF00995569 Matsumoto D, Yoo SH, Fontaine J, Anguas-Wong AM, Arriola M, Ataca B, et al. Mapping expressive differences around the world: The relationship between emotional display rules and individualism versus collectivism. Journal of Cross-Cultural Psychology. 2008; 39(1):55–74. DOI: 10.1177/0022022107311854 Mesquita B, Frijda NH. Cultural variations in emotions: A review. Psychological Bulletin. 1992; 112(2):179–204. DOI: 10.1037/0033-2909.112.2.179 [PubMed: 1454891] Mesulam MM, Mufson EJ. Insula of the old world monkey. III: Efferent cortical output and comments on function. The Journal of Comparative Neurology. 1982; 212(1):38–52. [PubMed: 7174907] Parkinson, B.; Fischer, A.; Manstead, ASR. Emotion in Social Relations: Cultural, Group, and Interpersonal Processes. New York: Psychology Press; 2005. Preacher KJ, Hayes AF. Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods. 2008; 40(3):879–891. DOI: 10.3758/BRM.40.3.879 [PubMed: 18697684] Saxbe DE, Yang XF, Borofsky LA, Immordino-Yang MH. The embodiment of emotion: Language use during the feeling of social emotions predicts cortical somatosensory activity. Social Cognitive and Affective Neuroscience. 2013; 8(7):806–812. DOI: 10.1093/scan/nss075 [PubMed: 22798396] Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, … Greicius MD. Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience. 2007; 27(9):2349–56. DOI: 10.1523/JNEUROSCI.5587-06.2007 [PubMed: 17329432] Seth AK. Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences. 2013; 17(11):565–73. DOI: 10.1016/j.tics.2013.09.007 [PubMed: 24126130] Tsai JL. Ideal affect: Cultural causes and behavioral consequences. Perspectives on Psychological Science. 2007; 2(3):242–259. DOI: 10.1111/j.1745-6916.2007.00043.x [PubMed: 26151968] Wallbott HG, Scherer KR. Emotion and economic development - Data and speculations concerning the relationship between economic factors and emotional experience. European Journal of Social Psychology. 1988; 18(3):267–273. DOI: 10.1002/ejsp.2420180305 Zaki J, Davis JI, Ochsner KN. Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage. 2012; 62(1):493–9. DOI: 10.1016/j.neuroimage.2012.05.012 [PubMed: 22587900]
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Views of the dorsal anterior insula (pink) and ventral anterior insula (turquoise) volumes of interest.
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In both Chinese and American groups, the more expressive a person, the more tightly fluctuations in feeling strength correlated with visceral somatosensory (dorsal anterior insula) neural activations. (A) Graphic depicting the relations among individuals’ expressiveness in the interview, and feelings and dAI BOLD response magnitudes during neuroimaging. r was calculated as the trial-by-trial correlation between feeling strength and dAI peak BOLD response magnitude. The relationship between expressiveness and r was calculated controlling for participants’ average feeling strength, average dAI peak BOLD response magnitude and age. (B) Scatterplot depicting the relationship between expressiveness and r (represented in bold in panel A). The center of data from each cultural Emotion. Author manuscript; available in PMC 2017 October 01.
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group is depicted with a solid-fill symbol, and illustrates the main effect of cultural group on expressiveness and r. Trend lines are plotted separately for each cultural group. NOTES: n = 27 for the Chinese group; n = 29 for the American group. We found no significant culture by expressiveness interaction on r: F[1,49] = .28, p = .59, ηp2 = .006.
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Fig. 3.
Expressiveness mediates the cultural group difference in how activations in visceral somatosensory cortex (dorsal anterior insula) correlate with feeling strength trial-by-trial, reported in Immordino-Yang et al., 2014. Mediation was tested controlling for average reported feeling strength, average dAI peak BOLD response magnitude and age. Estimated regression coefficients are depicted for each relationship, with standard errors in parentheses. The relationship of culture on r is depicted controlling for expressiveness. *indicates p
Emotion. Author manuscript; available in PMC 2017 October 01. Published in final edited form as: Emotion. 2016 October ; 16(7): 1033–1039. doi:10.1037/emo0000201.
Cultural Modes of Expressing Emotions Influence How Emotions Are Experienced Mary Helen Immordino-Yang1,2,3,*, Xiao-Fei Yang1,3, and Hanna Damasio1,3,4 1Brain
and Creativity Institute, University of Southern California, Los Angeles, CA 90089, USA
2Rossier
School of Education, University of Southern California, Los Angeles, CA 90089, USA
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3Neuroscience
Graduate Program, University of Southern California, Los Angeles, CA 90089,
USA 4Dornsife
Cognitive Neuroscience Imaging Center, University of Southern California, Los Angeles, CA 90089, USA
Abstract
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The brain’s mapping of bodily responses during emotion contributes to emotional experiences, or feelings. Culture influences emotional expressiveness, i.e. the magnitude of individuals’ bodily responses during emotion. So, are cultural influences on behavioral expressiveness associated with differences in how individuals experience emotion? Chinese and American young adults reported how strongly admiration and compassion-inducing stories made them feel, first in a private interview and then during fMRI. As expected, Americans were more expressive in the interview. While expressiveness did not predict stronger reported feelings or neural responses during fMRI, in both cultural groups more expressive people showed tighter trial-by-trial correlations between their experienced strength of emotion and activations in visceral-somatosensory cortex, even after controlling for individuals’ overall strength of reactions (neural and felt). Moreover, expressiveness mediated a previously described cultural effect in which activations in visceralsomatosensory cortex correlated with feeling strength among Americans but not among Chinese. Post-hoc supplementary analyses revealed that more expressive individuals reached peak activation of visceral-somatosensory cortex later in the emotion process and took longer to decide how strongly they felt. The results together suggest that differences in expressiveness correspond to differences in how somatosensory mechanisms contribute to constructing conscious feelings. By influencing expressiveness, culture may therefore influence how individuals know how strongly they feel, what conscious feelings are based on, or possibly what strong versus weak emotions “feel like.”
Correspondence to: Mary Helen Immordino-Yang, Brain and Creativity Institute & Rossier School of Education, University of Southern California, 3620A McClintock Ave, Room 267, Los Angeles, CA 90089-2921, [email protected]. Author Contributions MHI-Y and HD initiated a cross-cultural experiment. MHI-Y and X-FY designed the experiment, collected and analyzed the data. MHI-Y and X-FY wrote the paper, and HD provided critical feedback. All authors approved the final version of the manuscript for submission.
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Keywords East-West differences; subjective affect; insula; development; mental health
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In October, 2012, the world was swept by admiration for a Pakistani schoolgirl who resisted the Taliban. In December of that year, parents across the world were overwhelmed with compassion for the families of 20 American schoolchildren killed alongside their teachers. Upon learning of these events, some wept openly; others expressed their emotion more calmly, in a less behaviorally reactive manner. Cultural norms and values, such as individualism/collectivism (Markus & Kitayama, 1991), ideal affect (Tsai, 2007) and display rules, shape these styles of emotional expression (Ekman, 1971; Matsumoto et al., 2008; Mesquita & Frijda, 1992; Parkinson, Fischer, & Manstead, 2005). However, it is not clear whether these styles of expression correspond to differences in the way individuals experience their own emotions. Do calmer and more expressive individuals experience emotions in the same way?
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Emotions are, at their core, neural and somatic events whose evolutionary function is to prepare an organism to respond adaptively to a change in physical or social circumstances (Darwin, 1872; James, 1894). Once emotions are induced, people can become conscious of them (i.e., experience their emotions) by mentally constructing a feeling (Barrett, Mesquita, Ochsner, & Gross, 2007; Damasio, 1999). Neurobiologically, constructing feelings of emotions recruits brain systems that regulate and map body responses (Craig, 2002; Damasio & Carvalho, 2013). Psychologically, though, feelings are potentially as reliant on inferences and predictions about body states as on afferent interoceptive information (Seth, 2013). Feelings are socially and conceptually mediated, culturally variable, complex and dynamic, suggesting that they reflect context and development (Barrett et al., 2007; Barrett, 2012; Immordino-Yang, 2010).
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Given that feelings are supported by neural systems that map body states, and that feelings are conceptually mediated, could differences in how individuals habitually express emotions be associated with differences in the processes by which those individuals feel their emotions? Presumably, individuals whose emotions manifest in larger, more marked bodily/ behavioral responses would find those responses more salient and, potentially, informative. More expressive people could therefore learn to rely more heavily on the feeling of embodied reactions in deciding their current feeling strength. Over time, this difference could lead to a style of processing in which conscious feelings of emotion are more strongly associated with brain activity in somatosensory systems, whether this brain activity reflects real or simulated body states (Damasio, 1999; Seth, 2013). In essence, expressiveness could shift the sorts of embodied sensations, inferences and predictions that underlie conscious experiences of emotion (Immordino-Yang, 2010). We decided to investigate this possibility by testing whether behavioral expressiveness is associated with differences in how feeling strength correlates with fluctuations in neural activity in somatosensory cortices. Our region of interest was the dorsal Anterior Insula (dAI), a neural region important for interoception, emotion awareness, and social-emotional feelings (Craig, 2002; Critchley, Wiens, Rotshtein, Öhman, & Dolan, 2004; Damasio, 1999; Emotion. Author manuscript; available in PMC 2017 October 01.
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Immordino-Yang, McColl, Damasio, & Damasio, 2009; Zaki, Davis, & Ochsner, 2012). As the hub of the salience network, this region is heavily interconnected with frontal and limbic regions (Seeley et al., 2007). During emotion, the dAI can be thought of as providing a dynamic, integrative map of emotion-related body responses so that they have the possibility of informing conscious cognitive processing.
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Because emotional calmness is culturally valued in China while emotional expressiveness is valued in the United States (Bond, 1993; Markus & Kitayama, 1991; Tsai, 2007), we studied, as a first step, Chinese and American participants recruited from two similarly urban and academically competitive university communities, one in Beijing and one in Los Angeles. Additional investigations will be required to disentangle the multiple factors possibly contributing to differences in expressiveness, such as emotional ideals (e.g., those associated with individualism and collectivism), adaptation to cultural norms for emotion suppression and display, and individuals’ inherent biological reactivity and personal history. Here, we were interested to establish a link between natural emotional behavior and the neural correlates of emotional feelings in these two cultural contexts. We hypothesized that expressive people would feel their reactions differently—by a habitual psychological process that privileges embodiment—and that this difference would not be explained by expressive people reacting more strongly. We therefore tested the effect of behavioral expressiveness on the neural correlates of emotional feelings controlling for individuals’ average reported feeling strength and average neural activation magnitude during emotion processing.
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Overview of Procedures (1) During a videotaped two-hour private interview, participants reacted naturally to true stories inducing varieties of admiration and compassion. Participants’ behavioral reactions to a subset of stories involving painful physical injuries were used to index expressiveness (as these reactions are quick and relatively automatic). (2) During fMRI scanning, participants reacted again to the stories and reported their strength of feelings to each story in real time. For each participant, we calculated the strength of trial-by-trial correlation between neural activity fluctuations and reported feeling strength. Overview of Analytic Plan
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We tested whether: (a) the American group was more expressive than the Chinese group. We then tested whether individual differences in expressiveness predict: (b) the strength of feelings individuals experienced during scanning, and (c) the magnitude of the neural activation. Next, controlling for individuals’ average strength of feelings during scanning and average neural activation magnitude, we tested whether individuals’ expressiveness: (d) moderates the trial-by-trial correlation between dAI neural response and feeling strength. To test for the anatomical specificity of our effect, we: (e) analyzed the results from the ventral AI sector, involved in autonomic regulation and emotion induction (Kurth, Zilles, Fox, Laird, & Eickhoff, 2010; Mesulam & Mufson, 1982).
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The fMRI data were collected as part of a larger international project, briefly described below. An earlier study in this project examined the neural activity correlates of feeling strength at the group level (Immordino-Yang, Yang, & Damasio, 2014). Among other findings, it showed that activity in the dAI correlated with feeling strength in American groups (including in a group of East-Asian Americans), but not in Chinese groups. By contrast, activity in the vAI correlated with feelings in American and in Chinese groups. Because of that earlier finding, we expanded our originally planned analyses to: (f) test whether expressiveness would mediate the previously described cultural group difference in how dAI activity correlates with feelings. Finally, to strengthen our interpretation of the results, we conducted post hoc analyses of the effects of culture and expressiveness on time to emotion induction and awareness, presented in Supplemental Material.
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Statement on Sample, Measures, Manipulations and Data Exclusions The data for the current study were collected as part of a larger project investigating cultural influences on lifespan development of social emotion processing and its neurobiological correlates in multiple cultural contexts (n = 143). From the larger project sample we selected all Chinese and American young adults (aged 18–30) who had been born in the country where they currently live. (Participants who were not from a Chinese or an American background, who had immigrated, or who were outside this age range were excluded.) The sample partially overlaps with the sample used in Immordino-Yang et al., 2014. One qualified Chinese participant was excluded because she refused consent to be videotaped during the interview.
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Electrocardiograms (ECG) were collected simultaneously with neuroimaging in 44 of the participants (in all of the Americans and in 15 of the Chinese participants). All other manipulations, measures, and data exclusions in the study are reported. Participants Participants reported on a standard fMRI eligibility questionnaire that they were healthy, right-handed, neurologically normal, and with no history of psychiatric disorder, physical or emotional abuse. All reported normal hearing and normal or corrected-to-normal vision. All participants gave written informed consent in accordance with the requirements of the Institutional Review Boards of the University of Southern California (USC) or Beijing Normal University (BNU) and were compensated for their participation in accordance with their university’s norms.
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Chinese Group—28 Mandarin-speaking Chinese students from the BNU community (14 females; average age 22.9 years, SD = 3.1). All had been born and raised in mainland China. American Group—29 English-speaking American students from the USC community (16 females; average age 21.1 years, SD = 2.7; 12 participants identified as European-American, 13 as East-Asian, 2 as Latino and 2 as African-American). All had been born and raised in the U.S. Throughout the study, we tested our effects separately for the East-Asian Americans
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and for the Americans not of Asian descent. Since we found no differences in relations among expressiveness, feelings and neural activity, we collapsed the Americans into one group. For completeness, we also report the results from the East-Asian Americans for the major analyses. Stimuli
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All participants were presented with the same video stimuli, subtitled in the participants’ native language. (That is, participants saw half the videos in their native language and half in the other language, with all videos subtitled in their native language.) Subtitles were composed, translated and verified by native speakers. Narrative stimuli depicted compelling, true stories that unfolded like mini documentaries. Half of the stimuli featured Chinese protagonists and half featured Americans in equivalent situations (no American protagonists were of Asian descent). The corpus of 40 emotional narratives was balanced for positive and negative stories. (Stories had been piloted to induce varieties of admiration and of compassion/empathy.) 10 additional control narratives were piloted to be equivalently interesting but otherwise less emotion provoking, and were included to ensure that participants experienced a range of strengths of emotional reactions across the experiment. For example, one control stimulus featured the story of a professional man who decides to become a stay-at-home father. For additional details, see Immordino-Yang et al., 2014. Each video stimulus was prepared in two versions. A full length version (average length 43 seconds) was utilized in the pre-scan interview; a 5-second segment depicting the emotional crux of the narrative was shown in the scanner. Protocol
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Participants were told that they would be exposed to a series of true stories about real people’s lives, and that they should feel comfortable reporting their honest feelings in response to each. Participants were not told that we were studying emotional expressiveness.
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Adapting a previously developed protocol (see Immordino-Yang et al., 2009), participants were first introduced to the narrative stimuli in a private, videotaped interview in which an experimenter recounted each narrative verbally using a memorized script that began, “This is a story of a man/woman who…”, and included a brief description of the protagonist’s circumstances and accomplishments, followed by supplementary video images of the narrative protagonist shown on a laptop computer. Each narrative took between 60 and 90 seconds to present (including showing the full-length video) and finished with the experimenter asking, “How does this person’s story make you feel?” ”]. The experimenter then unobtrusively gazed downward into her [“ notebook and transcribed some words from the participants’ response as the participant described his/her reactions in an open-ended manner. Participants were told that the experimenter was taking notes in case the video camera failed. In actuality, this note-taking was also intended to standardize the experimenter’s behavior so that she would not inadvertently influence the behavior of the participant during the response phase. The interview took place in a quiet room on the university campus and was conducted by an experimenter of the same nationality as the participant (Immordino-Yang conducted the
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sessions in Los Angeles; Yang conducted those in Beijing). Narratives were presented in one of two counterbalanced orders. Prior to running the experiment, the experimenters extensively rehearsed the narrative scripts and reviewed together videotapes of practice preparation sessions with the aim of relaying the narratives consistently and equivalently. The interview lasted approximately 2 hours.
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Participants were then given a short break (~10 minutes). They then underwent BOLD fMRI as they viewed 5-second videos depicting the crux of each narrative with one sentence of verbal information from the preparation session delivered both auditorily (from a recording) and underneath the image in stationary Mandarin or English text, followed by 13 seconds of gray screen. A cross was shown for 2 seconds to separate trials. For each trial, participants reported via button press the real-time strength of their feeling once they became aware of it (one press per trial, at any point during the trial). Participants could report “no emotion,” “moderate emotion,” “strong emotion” or “overwhelmingly strong emotion.” Before the scanning session, experimenters stressed to participants that they should report their experienced strength of emotion at the current time. Participants confirmed their responses in a brief post-scan interview. Participants were shown each narrative twice over the course of the fMRI experiment for a total of 100 trials divided into four runs of approximately 9 minutes each. The two presentations of the same narrative were never shown during the same run. Analysis of Behavioral Expressiveness
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To gauge participants’ emotional expressiveness during the interview, participants’ reactions to narratives meant to elicit empathy/compassion for physical pain were coded. (These 10 narratives were a subset of the compassion stimuli, and depicted protagonists sustaining accidental painful injuries, e.g. a broken leg.) We chose to analyze only these interview trials for simplicity and reliability, as the phenotype of this emotion is relatively culturally universal and better known than the phenotypes of the other emotions induced. In addition, we had previously shown that behavioral responses to these videos were faster and that neural activity ramped up and dissipated more quickly (Immordino-Yang et al., 2009). We interpreted these findings as evidence that empathic reactions to physical pain are less nuanced and more automatic than reactions to admirable and socially painful stories. Coding the slower evolving admiration and compassion for social pain reactions could have made our results more susceptible to influence by display rules, suppression and other factors. For these reasons, we judged that the empathy for physical pain trials could capture participants’ natural behavior in a more direct way, and could provide a good, general, cross-culturally valid index of each participant’s natural behavioral reactiveness in this context. Each participant’s reactions were independently coded by at least one Chinese and one American expert rater blind to the study hypotheses. Coding was done with the sound off. Participants’ reactions to each stimulus were rated on a scale of 1–4 (the most expressive behavior evidenced determined the rating): 1.
Participant remained calm and showed no visible change in facial expression;
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2.
Participant tightened his/her facial muscles and noticeably blinked his/her eyes;
3.
Participant flinched, visibly lifted his/her shoulders, and/or covered his/her face with his/her hand(s);
4.
Participant displayed a strong facial expression and avoidant behavior, either pushing back his/her chair from the table or turning his/her upper body away from the stimulus.
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Inter-rater-reliability scores were all within the “excellent” range (Cohen’s Kappa > .84). Discrepancies between raters were resolved by discussion. As we were interested in a general index capturing the participants’ strongest reactions in this context, the three highest scores for each participant were averaged to produce an expressiveness score. (We did also test using the average of all trials, and the results remain significant, though variance explained decreased from approximately 18% to 10%.) fMRI data acquisition and processing Because the neuroimaging data for this study were collected as part of a larger project, the fMRI methods are only summarized here (for details see Immordino-Yang et al., 2014).
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The same scanner model and sequences were used to collect neuroimaging data at BNU Imaging Center for Brain Research and at USC Dana and David Dornsife Neuroimaging Center. Throughout the analyses, we implemented methods to account for brain size and shape differences. Data from one male Chinese participant were excluded due to excessive head movement (the participant coughed repeatedly). The remaining data underwent standard preprocessing and co-registration to the anatomical images in MNI space using SPM8 (Wellcome Department of Cognitive Neurology, London, UK). Calculating the effects of expressiveness on neural activity in the whole brain At the individual level, we modeled each participant’s task-related neural response using the method described in Immordino-Yang et al., 2014. For each participant, a contrast map of emotion versus implicit baseline was calculated. These contrast maps were entered into a group level whole-brain regression analysis, using expressiveness as the independent variable. Calculating the correlation between AI BOLD response and feeling strength for each participant
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The right and left dorsal and ventral AI volumes of interest were functionally defined using the contrast of emotion versus control for the conjunction of the groups, thresholded at p < . 005 uncorrected, then anatomically delimited and individually verified on each participant’s anatomy. See Figure 1 for views of the VOIs, and Immordino-Yang et al., 2014 for details. The time course of the BOLD signal for the average of the voxels within each volume of interest across each trial was extracted for each participant. To calculate each participant’s strength of trial-by-trial correlation between dAI BOLD response and reported feeling strength, we first averaged together the BOLD time courses
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corresponding to the two presentations of the same narrative stimulus (from different neuroimaging runs; this procedure served to improve the BOLD signal-to-noise ratio). Next, excluding the first two TRs (to accommodate the hemodynamic delay), we identified the peak value of the resulting time course (the local maximum of greatest magnitude). Finally, we averaged the button press values corresponding to the participant’s feeling strength during the two presentations of the same narrative. These procedures yielded 50 pairs of values for each participant from which to calculate the correlation coefficient. These procedures were then repeated for the vAI. (Parametric modulation analysis corroborated our findings; see Supplemental Material A). Testing the moderation hypothesis
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We tested whether expressiveness moderates the strength of correlation between dAI BOLD signal magnitude and feeling strength. To do this, the correlation coefficients calculated above were entered into a group-level linear regression model with behavioral expressiveness as the independent variable. Each participant’s average reported feeling strength, average peak BOLD magnitude in the dAI, and age were included in the model as covariates of no interest. (We controlled for age because the American group was slightly but significantly younger than the Chinese group.) Testing for the anatomical specificity of the moderation effect
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To test whether the moderation effect is specific to the dorsal sector of the AI, we tested whether expressiveness significantly moderates the strength of correlation between BOLD signal magnitude and feeling strength: first, in the vAI; second, in the vAI after partialling out variance in BOLD signal shared with the dAI; and third, in the dAI after partialling out variance in BOLD signal shared with the vAI. Testing the mediation hypothesis We have previously reported a cultural group difference in the strength of trial-by-trial correlation between dAI peak BOLD magnitude and participants’ feeling strength (Immordino-Yang et al., 2014). Here we wanted to establish whether participants’ expressiveness would mediate this group difference, controlling for participants’ average reported feeling strength, average peak BOLD magnitude in dAI and age. Using the biascorrected bootstrapping procedure described by Preacher & Hayes (2008) and implemented in SPSS 18, mediation effects were computed for each of 10,000 bootstrapped samples to determine the 99% confidence interval of the effect.
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Results Consistent with expectations, the American group was more expressive than the Chinese group (t[55] = 3.91, p < .001, Cohen’s d = 1.03, 99% CI [.16, .84]; we note that the EastAsian Americans were less expressive than the Americans not of Asian descent, t[27] = −2.13, p = .04, Cohen’s d = −.82, 95% CI [−.70, −0.01], and non-significantly more expressive than the Chinese group (t[39] = 1.94, p = .06, Cohen’s d = .68, 95% CI [−.01, .
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61]). Variance in expressiveness was equivalent between the American and Chinese groups (Levene’s test for equality of variances, F[1,55] = .80, p = .78). Neither cultural group nor gender experienced significantly stronger/weaker emotions. Men showed a greater effect of culture on expressiveness than women (interaction: F[1,56] = 12.58, p = .001, ηp2 = .183). See Table 1. Also consistent with expectations, more expressive participants did not report stronger feelings (r[54] = .02, p = .32, R2 = .00) and did not show greater neural responses in dAI, vAI or in any region of the brain involved in emotion or social processing, including in the amygdala, cingulate cortex, medial frontal cortex, precuneus, temporoparietal junction, or in other sectors of the insula (even using the lenient threshold of p < .01 uncorrected for multiple comparisons).
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However, as hypothesized, more expressive participants showed stronger trial-by-trial correlations between fluctuations in feeling strength and fluctuations in peak dAI BOLD magnitude (F[1,51] = 11.28, p=.001, ηp2 = .181). The relationship was positive for each variety of emotion induced when separately examined (ηp2admiration = .062; ηp2compassion = . 094). The effect was stronger for women (ηp2males = .123; ηp2females = .282; gender interaction: F[1,52] = 4.05, p = .049, ηp2 = .072). East-Asian Americans showed similar results to Americans not of Asian descent (i.e., no significant interaction: F[1,22] = .213, p = .649, ηp2 = .010). See also Figure 2.
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As evidence of the anatomical specificity of the effect, we found that expressiveness was related to the trial-by-trial correlation between feeling strength and BOLD magnitude in the ventral AI (the autonomic modulatory sector; F[1,51] = 5.34, p = .03, ηp2 = .095), but that this relationship became non-significant and small after controlling for variance shared with the dAI (F[1,51] = .88, p = .35, ηp2 = .017). By contrast, expressiveness significantly moderated the trial-by-trial correlation between feeling strength and BOLD magnitude in the dAI even after controlling for BOLD variance shared with the vAI (F[1,51] = 7.17, p = .01, ηp2 = .123). As illustrated in Figure 3, individual differences in participants’ expressiveness mediated the previously reported cultural group difference in the trial-by-trial correlation between dAI peak BOLD magnitude and feeling strength. The mean of the bootstrapped mediation effect was .09 with standard error .04; the 99% confidence interval ranged from .01 to .23 (statistically significant because it does not cross zero).
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Given our positive results, we undertook a series of post hoc analyses to strengthen the interpretation that our findings are due to effects of expressiveness on the feeling process and not to effects of expressiveness on emotion induction. Emotions must be induced before they can be felt (Damasio et al., 2000) and constructing feelings (including neurally mapping or simulating the body response) takes time. We therefore reasoned that expressiveness should be associated with delays in emotion awareness and its neural correlate, dorsal AI activation (Craig, 2002; Immordino-Yang et al., 2014; Zaki et al., 2012).
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But, there should be no delays in emotion induction, i.e. in the time required for the initial cognitive appraisal of the stimulus and the subsequent induction of the vAI activation and psychophysiological response. Given these hypotheses, we returned to the data from the participants for whom we had collected ECG (see Supplemental Material B). We found that expressiveness was not associated with delays in peak cardiac response or vAI activation (indices of emotion induction), but that expressiveness was associated with delays in dAI activation and participants’ reports of feelings (indices of emotion awareness).
Discussion
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Culture is known to affect ideals for emotional arousal (Tsai, 2007) and norms for emotional display (Matsumoto, 1990), as well as how often and how strongly individuals experience emotions in their daily lives (Bond, 1993; Eid & Diener, 2001; Wallbott & Scherer, 1988). Here we show that cultural influences on emotional behavior also relate to differences in the process by which individuals feel emotions, once they are induced. By combining subjective reports of feeling strength with neuroimaging in participants whose natural emotional behavior we had characterized, we demonstrated that: (1) for both Chinese and American cultural groups (and for the sub-group of Americans of East-Asian descent), the more expressive an individual, the more tightly fluctuations in experienced feeling strength correlated with fluctuations in neural response magnitude in visceral somatosensory cortex (dAI); (2) expressiveness also mediated a previously reported cultural group difference in which dAI activity correlated with feeling strength only in American participant groups. Notably, the effects were consistent across the range of emotions induced, and held after controlling for individuals’ average emotional reactivity (neural and felt). Interestingly, we found no evidence that more expressive individuals (or that Americans) had stronger feelings or stronger neural responses to the stimuli—only that their feelings correlated with neural activity differently. Our post hoc analyses suggest that expressiveness influenced the processing of feelings, rather than the induction of emotion.
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More work is needed to understand the developmental origins and underlying mechanisms of these effects, and to disentangle effects of emotion regulation, ideal affect and other factors. Cultural and individual differences in the embodied experiences of emotion have long been a focus of inquiry (Barrett et al., 2007; Cohen & Leung, 2009; Dunn et al., 2010; Eid & Diener, 2001; Saxbe, Yang, Borofsky, & Immordino-Yang, 2013). Our findings collectively suggest that by modulating bodily expression, culture also influences how somatosensory neural activity becomes associated with subjective affect (i.e., how individuals know how strongly they feel, or what emotional feelings are based on, or possibly what strong versus weak emotions “feel like”). Our study is limited in that we did not seek to disentangle culture and nationality, or to probe the origins of the differences in expressiveness we measured. We also measured only emotional intensity and not which specific emotions participants experienced to each narrative. However, by connecting observable emotional behaviors to private emotional experiences and their underlying neural substrate, we aim to enhance understanding and appreciation of cultural learning and the diversity of human experiences. The findings have important implications for social
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development and education, for mental health and psychiatry, and for theoretical models of emotional feelings.
Supplementary Material Refer to Web version on PubMed Central for supplementary material.
Acknowledgments MHIY was supported by NSF CAREER 11519520; the Brain and Creativity Institute Research Fund; the University of Southern California Provost; the Rossier School of Education; H. Damasio and MHIY were supported by National Institute of Health [P01 NS19632] to H. Damasio and A. Damasio; X-FY was funded by the USC Neuroscience Graduate Program Fellowship and the USC US-China Institute Summer Fieldwork Grant.
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R. Zhou secured access to BNU Imaging Center for Brain Research and Chinese participants; We thank A. Damasio, S. Kitayama, The Stanford Culture Collab., Y. Chentsova-Dutton, J. Parvizi, L. Young, E. Winner, H. Gardner, D. Daniel for discussions; J. Kaplan, S. Wong, L. Zhu for neuroimaging advice; M. Lay, B. Sanders, D. Yeung, A. Goldman, E. O’Day, T. Nanda, R. Atticus, J. Flores for help with data analysis.
References
Author Manuscript Author Manuscript
Barrett LF. Emotions are real. Emotion. 2012; 12(3):413–29. DOI: 10.1037/a0027555 [PubMed: 22642358] Barrett LF, Mesquita B, Ochsner KN, Gross JJ. The experience of emotion. Annual Review of Psychology. 2007; 58:373–403. DOI: 10.1146/annurev.psych.58.110405.085709 Bond MH. Emotions and their expression in Chinese culture. Journal of Nonverbal Behavior. 1993; 17(4):245–262. DOI: 10.1007/BF00987240 Cohen D, Leung AKY. The hard embodiment of culture. European Journal of Social Psychology. 2009; 39:1278–1289. DOI: 10.1002/ejsp Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience. 2002; 3(8):655–66. DOI: 10.1038/nrn894 [PubMed: 12154366] Critchley HD, Wiens S, Rotshtein P, Öhman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nature Neuroscience. 2004; 7:189– 195. DOI: 10.1038/nn1176 [PubMed: 14730305] Damasio, AR. The feeling of what happens: Body and emotion in the making of consciousness. New York: Harcourt; 1999. Damasio AR, Carvalho GB. The nature of feelings: Evolutionary and neurobiological origins. Nature Reviews Neuroscience. 2013; 14(2):143–152. DOI: 10.1038/nrn3403 [PubMed: 23329161] Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LLB, Parvizi J, Hichwa RD. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience. 2000; 3(10):1049–1056. DOI: 10.1038/79871 [PubMed: 11017179] Darwin, C. The expression of the emotions in man and animals. London: John Murray; 1872. Dunn BD, Galton HC, Morgan R, Evans D, Oliver C, Meyer M, et al. Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science. 2010; 21(12):1835–44. DOI: 10.1177/0956797610389191 [PubMed: 21106893] Eid M, Diener E. Norms for experiencing emotions in different cultures: Inter- and intranational differences. Journal of Personality and Social Psychology. 2001; 81(5):869–885. DOI: 10.1037//0022-3514.81.5.869 [PubMed: 11708563] Ekman P. Universals and cultural differences in facial expressions of emotion. Nebraska Symposium on Motivation. 1971; 19:207–283. Immordino-Yang MH. Toward a microdevelopmental, interdisciplinary approach to social emotion. Emotion Review. 2010; 2(3):217–220. DOI: 10.1177/1754073910361985 Immordino-Yang MH, McColl A, Damasio H, Damasio AR. Neural correlates of admiration and compassion. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(19):8021–6. DOI: 10.1073/pnas.0810363106 [PubMed: 19414310]
Emotion. Author manuscript; available in PMC 2017 October 01.
Immordino-Yang et al.
Page 12
Author Manuscript Author Manuscript Author Manuscript
Immordino-Yang MH, Yang XF, Damasio H. Correlations between social-emotional feelings and anterior insula activity are independent from visceral states but influenced by culture. Frontiers in Human Neuroscience. 2014; 8:728.doi: 10.3389/fnhum.2014.00728 [PubMed: 25278862] James W. Discussion: The physical basis of emotion. Psychological Review. 1894; 1(5):516–529. DOI: 10.1037/h0065078 Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB. A link between the systems: Functional differentiation and integration within the human insula revealed by meta-analysis. Brain Structure & Function. 2010; 214(5–6):519–34. DOI: 10.1007/s00429-010-0255-z [PubMed: 20512376] Markus HR, Kitayama S. Culture and the self: Implications for cognition, emotion, and motivation. Psychological Review. 1991; 98(2):253–224. DOI: 10.1037/0033-295X.98.2.224 Matsumoto D. Cultural similarities and differences in display rules. Motivation and Emotion. 1990; 14(3):195–214. DOI: 10.1007/BF00995569 Matsumoto D, Yoo SH, Fontaine J, Anguas-Wong AM, Arriola M, Ataca B, et al. Mapping expressive differences around the world: The relationship between emotional display rules and individualism versus collectivism. Journal of Cross-Cultural Psychology. 2008; 39(1):55–74. DOI: 10.1177/0022022107311854 Mesquita B, Frijda NH. Cultural variations in emotions: A review. Psychological Bulletin. 1992; 112(2):179–204. DOI: 10.1037/0033-2909.112.2.179 [PubMed: 1454891] Mesulam MM, Mufson EJ. Insula of the old world monkey. III: Efferent cortical output and comments on function. The Journal of Comparative Neurology. 1982; 212(1):38–52. [PubMed: 7174907] Parkinson, B.; Fischer, A.; Manstead, ASR. Emotion in Social Relations: Cultural, Group, and Interpersonal Processes. New York: Psychology Press; 2005. Preacher KJ, Hayes AF. Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods. 2008; 40(3):879–891. DOI: 10.3758/BRM.40.3.879 [PubMed: 18697684] Saxbe DE, Yang XF, Borofsky LA, Immordino-Yang MH. The embodiment of emotion: Language use during the feeling of social emotions predicts cortical somatosensory activity. Social Cognitive and Affective Neuroscience. 2013; 8(7):806–812. DOI: 10.1093/scan/nss075 [PubMed: 22798396] Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, … Greicius MD. Dissociable intrinsic connectivity networks for salience processing and executive control. The Journal of Neuroscience. 2007; 27(9):2349–56. DOI: 10.1523/JNEUROSCI.5587-06.2007 [PubMed: 17329432] Seth AK. Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences. 2013; 17(11):565–73. DOI: 10.1016/j.tics.2013.09.007 [PubMed: 24126130] Tsai JL. Ideal affect: Cultural causes and behavioral consequences. Perspectives on Psychological Science. 2007; 2(3):242–259. DOI: 10.1111/j.1745-6916.2007.00043.x [PubMed: 26151968] Wallbott HG, Scherer KR. Emotion and economic development - Data and speculations concerning the relationship between economic factors and emotional experience. European Journal of Social Psychology. 1988; 18(3):267–273. DOI: 10.1002/ejsp.2420180305 Zaki J, Davis JI, Ochsner KN. Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage. 2012; 62(1):493–9. DOI: 10.1016/j.neuroimage.2012.05.012 [PubMed: 22587900]
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Views of the dorsal anterior insula (pink) and ventral anterior insula (turquoise) volumes of interest.
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In both Chinese and American groups, the more expressive a person, the more tightly fluctuations in feeling strength correlated with visceral somatosensory (dorsal anterior insula) neural activations. (A) Graphic depicting the relations among individuals’ expressiveness in the interview, and feelings and dAI BOLD response magnitudes during neuroimaging. r was calculated as the trial-by-trial correlation between feeling strength and dAI peak BOLD response magnitude. The relationship between expressiveness and r was calculated controlling for participants’ average feeling strength, average dAI peak BOLD response magnitude and age. (B) Scatterplot depicting the relationship between expressiveness and r (represented in bold in panel A). The center of data from each cultural Emotion. Author manuscript; available in PMC 2017 October 01.
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group is depicted with a solid-fill symbol, and illustrates the main effect of cultural group on expressiveness and r. Trend lines are plotted separately for each cultural group. NOTES: n = 27 for the Chinese group; n = 29 for the American group. We found no significant culture by expressiveness interaction on r: F[1,49] = .28, p = .59, ηp2 = .006.
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Fig. 3.
Expressiveness mediates the cultural group difference in how activations in visceral somatosensory cortex (dorsal anterior insula) correlate with feeling strength trial-by-trial, reported in Immordino-Yang et al., 2014. Mediation was tested controlling for average reported feeling strength, average dAI peak BOLD response magnitude and age. Estimated regression coefficients are depicted for each relationship, with standard errors in parentheses. The relationship of culture on r is depicted controlling for expressiveness. *indicates p
