Culture but not gender modulates amygdala activation during explicit emotion recognition

BMC Neuroscience

Ewald Moser³  Ruben C Gur³  Ilse Kryspin-Exner²  Christian Windischberger¹  Simon Robinson¹  Ute Habel⁴  Birgit Derntl⁴ 

[1] Centre for Medical Physics and Biomedical Engineering, Medical University of Vienna, Vienna, Austria;Institute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria;Department of Psychiatry, University of Pennsylvania Medical School, and the Philadelphia Veterans Administration Medical Center, Philadelphia, USA;Department of Psychiatry, Psychotherapy, and Psychosomatics, RWTH Aachen University, Aachen, Germany

关键词: fMRI;    Amygdala;    Emotion;    Gender;    Culture;   

Others  :  1170708
DOI  :  10.1186/1471-2202-13-54

 received in 2011-10-03, accepted in 2012-05-29,  发布年份 2012

【 摘 要 】

Background

Mounting evidence indicates that humans have significant difficulties in understanding emotional expressions from individuals of different ethnic backgrounds, leading to reduced recognition accuracy and stronger amygdala activation. However, the impact of gender on the behavioral and neural reactions during the initial phase of cultural assimilation has not been addressed. Therefore, we investigated 24 Asians students (12 females) and 24 age-matched European students (12 females) during an explicit emotion recognition task, using Caucasian facial expressions only, on a high-field MRI scanner.

Results

Analysis of functional data revealed bilateral amygdala activation to emotional expressions in Asian and European subjects. However, in the Asian sample, a stronger response of the amygdala emerged and was paralleled by reduced recognition accuracy, particularly for angry male faces. Moreover, no significant gender difference emerged. We also observed a significant inverse correlation between duration of stay and amygdala activation.

Conclusion

In this study we investigated the “alien-effect” as an initial problem during cultural assimilation and examined this effect on a behavioral and neural level. This study has revealed bilateral amygdala activation to emotional expressions in Asian and European females and males. In the Asian sample, a stronger response of the amygdala bilaterally was observed and this was paralleled by reduced performance, especially for anger and disgust depicted by male expressions. However, no gender difference occurred. Taken together, while gender exerts only a subtle effect, culture and duration of stay as well as gender of poser are shown to be relevant factors for emotion processing, influencing not only behavioral but also neural responses in female and male immigrants.

【 授权许可】

   
2012 Derntl et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kitayama S, Park J: Cultural neuroscience of the self: understanding the social grounding of the brain. Soc Cogn Affect Neurosci 2010, 5:111-129.
• [2]Chiao JY, Ambady N: Cultural Neuroscience. Parsing Universality and Diversity across Levels of Analysis. In Handbook of Cultural Psychology. Edited by Kitayama S, Cohen D. Guilford Press, New York; 2007:237-254.
• [3]Gutchess AH, Welsh RC, Boduroglu A, Park DC: Cultural differences in neural function associated with object processing. Cogn Affect Behav Neurosci 2006, 6:102-109.
• [4]Rule NO, Freeman JB, Moran JM, Gabrieli JDE, Adams RB, Ambady N: Voting behavior is reflected in amygdala response across cultures. Soc Cogn Affect Neurosci 2010, 5:349-355.
• [5]Cheon BK, Im DM, Harada T, Kim JS, Mathur VA, Scimeca JM, Parrish TB, Park HW, Chiao JY: Cultural influences on neural basis of intergroup empathy. NeuroImage 2011, 57:642-650.
• [6]de Greck M, Shi Z, Wang G, Zuo X, Yang X, Wang X, Northoff G, Han S: Culture modulates brain activity during empathy with anger. NeuroImage 2012, 59:2871-2882.
• [7]Zhu Y, Zhang L, Fan J, Han S: Neural basis of cultural influence on self-representation. NeuroImage 2007, 34:1310-1316.
• [8]Chiao JY, Harada T, Komeda H, Li Z, Mano Y, Saito D, Parrish TB, Sadato N, Iidaka T: Dynamic cultural influences on neural representations of the self. J Cogn Neurosci 2010, 22:1-11.
• [9]Cunningham WA, Johnson MK, Raye CL, Gatenby JC, Gore JC, Banaji MR: Separable neural components in the processing of black and white faces. Psychol Sci 2004, 15:806-813.
• [10]Hart AJ, Whalen PJ, Shin LM, McInerney SC, Fischer H, Rauch SL: Differential response in the human amygdala to racial outgroup vs ingroup face stimuli. NeuroReport 2000, 11:2351-2355.
• [11]Lieberman MD, Hariri AH, Jarcho JM, Eisenberger NI, Bookheimer SY: An fMRI investigation of race-related amygdala activity in African-American and Caucasian-American individuals. Nat Neurosci 2005, 8:720-722.
• [12]Phelps EA, O’Connor KJ, Cunningham WA, Funayama ES, Gatenby JC, Gore JC, Banaji MR: Performance on indirect measures of race evaluation predicts amygdala activation. J Cogn Neurosci 2000, 12:729-738.
• [13]Cunningham WA, Zelazo PD: Attitudes and evaluations: a social cognitive neuroscience perspective. Trends Cogn Sci 2007, 11:97-104.
• [14]Ito TA, Bartholow BD: The neural correlates of race. Trends Cogn Sci 2009, 13:524-531.
• [15]Moriguchi Y, Ohnishi T, Kawachi T, Mori T, Hirakata M, Yamada M, Matsuda H, Komaki G: Specific brain activation in Japanese and Caucasian people to fearful faces. NeuroReport 2005, 16:133-136.
• [16]Chiao JY, Iidaka T, Gordon HL, Nogawa J, Bar M, Aminoff E, Sadato N, Ambady N: Cultural specificity in amygdala response to fear faces. J Cogn Neurosci 2008, 20:1-8.
• [17]Adams RB, Franklin RG, Rule NO, Freeman JB, Kveraga K, Hadjikhani N, Yoshikawa S, Ambady N: Culture, gaze and the neural processing of fear expressions. Soc Cogn. Affective Neurosci 2010, 5:340-348.
• [18]Derntl B, Habel U, Robinson S, Windischberger C, Kryspin-Exner I, Gur RC, Moser E: Amygdala activation during recognition of emotions in a foreign ethnic group is associated with duration of stay. Soc Neurosci 2009, 4:294-307.
• [19]Domes G, Schulze L, Bottger M, Grossman A, Hauenstein K, Wirtz PH, Heinrichs M, Herpertz SC: The neural correlates of sex differences in emotional reactivity and emotion regulation. Hum Brain Mapp 2010, 31:758-769.
• [20]McClure EB, Monk CS, Nelson EE, Zarahn E, Leibenluft E, Bilder RM, Charney DS, Ernst M, Pine DS: A developmental examination of gender differences in brain engagement during evaluation of threat. Biol Psychiatry 2004, 55:1047-1055.
• [21]Williams LM, Barton MJ, Kemp AH, Liddell BJ, Peduto A, Gordon E, Bryant RA: Distinct amygdala-autonomic arousal profiles in response to fear signals in healthy males and females. NeuroImage 2005, 28:618-626.
• [22]Hamann S, Herman RA, Nolan CL, Wallen K: Men and women differ in amygdala response to visual sexual stimuli. Nat Neurosci 2004, 7:411-416.
• [23]Schienle A, Schafer A, Stark R, Walter B, Vaitl D: Gender differences in the processing of disgust- and fear-inducing pictures: An fMRI study. NeuroReport 2005, 16:277-280.
• [24]Wrase J, Klein S, Gruesser SM, Hermann D, Flor H, Mann K, Braus DF, Heinz A: Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study. Neurosci Lett 2003, 348:41-45.
• [25]Aleman A, Swart M: Sex differences in neural activation to facial expressions denoting contempt and disgust. PLoS One 2008, 3:e3622.
• [26]Killgore WD, Yurgelun-Todd DA: Sex differences in amygdala activation during the perception of facial affect. NeuroReport 2001, 12:2543-2547.
• [27]Lee TMC, Liu HL, Hoosain R, Liao WT, Wu CT, Yuen KSL, Chan CC, Fox PT, Goa JH: Gender differences in neural correlates of recognition of happy and sad faces in humans assessed by functional magnetic resonance imaging. Neurosci Lett 2002, 333:13-16.
• [28]Nomura M, Ohira H, Haneda K, Iidaka T, Sadato N, Okada T, Yonekura Y: Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. NeuroImage 2004, 21:352-363.
• [29]Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P: Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 2009, 34:418-432.
• [30]Fitzgerald DA, Angstadt M, Jelsone LM, Nathan PJ, Phan KL: Beyond threat: Amygdala reactivity across multiple expressions of facial affect. NeuroImage 2006, 30:1441-1448.
• [31]Habel U, Windischberger C, Derntl B, Robinson S, Kryspin-Exner I, Gur RC, Moser E: Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. Neuropsychologia 2007, 45:2369-2377.
• [32]Derntl B, Habel U, Windischberger C, Robinson S, Kryspin-Exner I, Gur RC, Moser E: General and specific responsiveness of the amygdala during explicit emotion recognition. BMC Neurosci 2009, 10:91. BioMed Central Full Text
• [33]Huang Y, Tang S, Helmeste D, Shioiri T, Someya T: Differential judgements of static facial expressions of emotions in three cultures. Psychiatry Clin Neurosci 2001, 55:479-483.
• [34]Shioiri T, Someya T, Helmeste D, Tang SW: Misinterpretation of facial expression: a cross-cultural study. Psychiatry Clin Neurosci 1999, 53:45-50.
• [35]Shioiri T, Someya T, Helmeste D, Tang SW: Cultural difference in recognition of facial emotional expression: contrast between Japanese and American raters. Psychiatry Clin Neurosci 1999, 53:629-633.
• [36]Elfenbein HA, Ambady N: When familiarity breeds accuracy: cultural exposure and facial emotion recognition. J Pers Soc Psychol 2003, 85:276-290.
• [37]Sander G, Grafman J, Zalla T: The human amygdala: an evolved system for relevance detection. Rev Neurosci 2003, 14:303-316.
• [38]Goh JOS, Leshikar ED, Sutton BP, Tan JC, Sim SKY, Hebrank AC, Park DC: Culture differences in neural processing of faces and houses in the ventral visual cortex. Soc Cogn Affect Neurosci 2010, 5:227-235.
• [39]Hooker CI, Germine LT, Knight RT, D’Esposito M: Amygdala response to facial expressions reflects emotional learning. J Neurosci 2006, 26:8915-8922.
• [40]Elfenbein HA, Ambady N: On the universality and cultural specificity of emotion recognition: a meta-analysis. Psychol Bull 2002, 128:203-205.
• [41]Elfenbein HA, Beaupré M, Lévesque M, Hess U: Toward a dialect theory: cultural differences in the expression and recognition of posed facial expressions. Emotion 2007, 7:131-146.
• [42]Sato W, Kochiyama T, Uono S, Yoshikawa S: Amygdala integrates emotional expression and gaze direction in response to dynamic facial expressions. NeuroImage 2010, 50:1658-1665.
• [43]Straube T, Langohr B, Schmidt S, Mentzel H-J, Miltner WHR: Increased amygdala activation to averted versus direct gaze in humans is independent of valence of facial expression. NeuroImage 2010, 49:2680-2686.
• [44]Richeson JA, Todd AR, Trawalter S, Baird AA: Eye-gaze direction modulates race-related amygdala activity. Group Processes Intergroup Relations 2008, 11:233-246.
• [45]Macrae CN, Hood BM, Milne AB, Rowe AC, Mason MF: Are you looking at me? Eye gaze and person perception. Psychol Sci 2002, 13:460-464.
• [46]Argyle M, Cook M: Gaze and mutual gaze. Cambridge, England, Cambridge University Press; 1976.
• [47]Trawalter S, Todd AR, Baird AA, Richeson JA: Attending to threat: race-based patterns of selective attention. J Exp Soc Psychol 2008, 44:1322-1327.
• [48]Ito TA, Urland GR: Race and gender on the brain: electrocortical measures of attention to the race and gender of multiply categorizable individuals. J Pers Soc Psychol 2003, 85:616-626.
• [49]Ito TA, Urland GR: The influence of processing objectives on the perception of faces: an ERP study of race and gender perception. Cogn Affect Behav Neurosci 2005, 5:21-36.
• [50]Carretié L, Mercado F, Tapia M, Hinojosa JA: Emotion, attention, and the ‘negativity bias’, studied through event-related brain potentials. Internat J Psychophys 2001, 41:75-85.
• [51]Schupp HT, Junghöfer M, Weike AI, Hamm AO: Attention and emotion: an ERP analysis of facilitated emotional stimulus processing. NeuroReport 2003, 14:1107-1110.
• [52]Schupp HT, Ohman A, Junghöfer M, Weike AI, Stockburger J, Hamm AO: The facilitated processing of threatening faces: an ERP analysis. Emotion 2004, 4:189-200.
• [53]Wright CI, Martis B, Schwartz CE, Shin LM, Fischer HH, McMullin K, Rauch SL: Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex. NeuroImage 2003, 18:660-669.
• [54]Blackford JU, Buckholtz JW, Avery SN, Zald DH: A unique role for the human amygdala in novelty detection. NeuroImage 2010, 50:1188-1193.
• [55]Guimond S, Branscombe NR, Brunot S, Buunk AP, Chatard A, Désert M, Garcia DM, Haque S, Martinot D, Yzerbyt V: Culture, gender, and the self: variations and impact of social comparison processes. J Pers Soc Psychol 2007, 92:1118-1134.
• [56]Ohrmann P, Pedersen A, Braun M, Bauer J, Kugel H, Kersting A, Domschke K, Deckert J, Suslow T: Effect of gender on processing threat-related stimuli in patients with panic disorder: sex does matter. Depress Anxiety 2010, 27:1034-1043.
• [57]Kohn N, Kellermann T, Gur RC, Schneider F, Habel U: Gender differences in the neural correlates of humor processing: implications for different processing modes. Neuropsychologia 2011, 49:888-897.
• [58]Schulte-Rüther M, Markowitsch HJ, Shah NJ, Fink GR, Piefke M: Gender differences in brain networks supporting empathy. NeuroImage 2008, 42:393-403.
• [59]Derntl B, Finkelmeyer A, Eickhoff SB, Kellermann T, Falkenberg DI, Schneider F, Habel U: Multidimensional assessment of empathic abilities: Neural correlates and gender differences. Psychoneuroendocrinology 2010, 35:67-82.
• [60]Hugenberg K, Bodenhausen GV: Facing prejudice: implicit prejudice and the perception of facial threat. Psychol Sci 2003, 14:640-643.
• [61]Kang SK, Chasteen AL: Beyond the double-jeopardy hypothesis: assessing emotion on the faces of multiply-categorizable targets of prejudice. J Exp Soc Psychol 2009, 45:1281-1285.
• [62]Fischer H, Fransson P, Wright CI, Bäckman L: Enhanced occipital and anterior cingulate activation in men but not in woman during exposure to angry and fearful male faces. Cogn Affect Behav Neurosci 2004, 4:326-334.
• [63]Moser E, Stahlberg F, Ladd ME, Trattnig S: 7-T MR – from research to clinical application? NMR Biomed 2012, 25:695-716.
• [64]Kubota JT, Ito TA: Multiple cues in social perception: the time course of processing race and facial expression. J Exp Soc Psychol 2007, 43:738-752.
• [65]Chiao JY, Blizinsky KD: Culture-gene coevolution of individualism-collectivism and the serotonin transporter gene. Proc Biol Sci 2010, 277:529-537.
• [66]Wittchen HU, Zaudig M, Fydrich T: Strukturiertes Klinisches Interview für DSM-IV. Göttingen, Hogrefe; 1997.
• [67]Van der Ven AHGS, Ellis JL: A Rasch analysis of Raven´s standard progressive matrices. Person Individ Diff 2000, 29:45-64.
• [68]Gur RC, Sara R, Hagendoorn M, Marom O, Hughett P, Macy L, Turner T, Bajcsy R, Posner A, Gur RE: A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J Neurosci Methods 2002, 115:137-143.
• [69]Matsumoto D: Methodological requirements to test a possible in-group advantage in judging emotions across cultures: comments on Elfenbein and Ambady (2002) and evidence. Psychol Bull 2002, 128:236-242.
• [70]Robinson S, Windischberger C, Rauscher A, Moser E: Optimized 3 T EPI of the amygdalae. NeuroImage 2004, 22:203-210.
• [71]Robinson S, Hoheisel B, Windischberger C, Habel U, Lanzenberger R, Moser E: FMRI of the emotions: towards an improved understanding of amygdala function. Curr Med Imag Rev 2005, 1:115-129.
• [72]Robinson SD, Pripfl J, Bauer H, Moser E: The impact of EPI voxel size on SNR and BOLD sensitivity in the anterior medio-temporal lobe: a comparative group study of deactivation of the default mode. MAGMA 2008, 21:279-290.
• [73]Robinson SD, Moser E, Peper M: Functional magnetic resonance imaging of emotion. NeuroMethods 2009, 41:411-456.
• [74]Windischberger C, Langenberger H, Sycha T, Tschernko EM, Fuchsjager-Mayerl G, Schmetterer L, Moser E: On the origin of respiratory artifacts in BOLD-EPI of the human brain. Magn Reson Imag 2002, 20:575-582.
• [75]Windischberger C, Friedreich S, Hoheisel B, Moser E: The impact of physiological artifact correction on individual and group results of fMRI of the amygdala. NeuroImage 2006, 31:S28.
• [76]Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M: Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
• [77]Baron RM, Kenny DA: The moderator-mediator variable distinction in social psychological research: Conceptual, strategic, and statistical considerations. J Pers Soc Psychol 1986, 51:1173-1182.