Skip to main content
SpringerLink
Log in

Gender Role, But Not Sex, Shapes Humans’ Susceptibility to Emotion

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

It is unknown whether the famous sex-related difference in emotion processing is accounted for by biological sex, gender role, or their interaction. To clarify the issue, in Study 1 we recorded event-related potentials in response to negative and positive images of diverse intensities when 47 masculine (26 males) and 47 feminine (22 males) subjects performed a non-emotional task. The occipital P1 and N1 amplitudes were larger in women than in men, while feminine subjects showed larger N1 amplitudes than masculine subjects, regardless of sex. Moreover, feminine subjects showed enhanced frontocentral N2 (210–270 ms) amplitudes for highly and mildly negative than for neutral stimuli, while masculine subjects showed an emotion effect only for highly negative stimuli. The feminine-specific effect for mildly negative stimuli was positively correlated to the feminine score, and this correlation was located to the anterior cingulate and the superior and medial frontal gyri. Furthermore, feminine but not masculine subjects showed enhanced parietal P3 (330–560 ms) amplitudes for highly and mildly positive than for neutral stimuli, an effect positively related to the feminine score and localized to the precuneus, posterior cingulate, and superior temporal gyrus. Machine learning analyses verified that single-trial N2 and P3 amplitudes of feminine subjects reliably discriminated the intensity of negative and positive stimuli, respectively. For ecological considerations, in Study 2 we used an observational approach (n = 300) and confirmed that feminine gender role, rather than biological sex, predicted individual differences in daily experience of emotion-related psychopathological symptoms. These findings provide solid evidence for the critical impact of gender role rather than sex on emotional susceptibility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Campanella S, Rossignol M, Mejias S, Joassin F, Maurage P, Debatisse D, et al. Human gender differences in an emotional visual oddball task: An event-related potentials study. Neurosci Lett 2004, 367: 14–18.

    Article  CAS  PubMed  Google Scholar 

  2. Montagne B, Kessels RPC, Frigerio E, de Haan EHF, Perrett DI. Sex differences in the perception of affective facial expressions: do men really lack emotional sensitivity? Cogn Process 2005, 6: 136–141.

    Article  PubMed  Google Scholar 

  3. Scholten MRM, Aleman A, Montagne B, Kahn RS. Schizophrenia and processing of facial emotions: Sex matters. Schizophr Res 2005, 78: 61–67.

    Article  PubMed  Google Scholar 

  4. Stroud LR, Salovey P, Epel ES. Sex differences in stress responses: Social rejection versus achievement stress. Biol Psychiatry 2002, 52: 318–327.

    Article  PubMed  Google Scholar 

  5. Yuan J, Luo Y, Yan JH, Meng X, Yu F, Li H. Neural correlates of the females’ susceptibility to negative emotions: An insight into gender-related prevalence of affective disturbances. Hum Brain Mapp 2009, 30: 3676–3686.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hofer A, Siedentopf CM, Ischebeck A, Rettenbacher MA, Verius M, Felber S, et al. Gender differences in regional cerebral activity during the perception of emotion: A functional MRI study. Neuroimage 2006, 32: 854–862.

    Article  PubMed  Google Scholar 

  7. Cai A, Yang J, Shuang XU, Yuan J. The male advantage in regulating negative emotion by expressive suppression: An event-related potential study. Acta Psychol Sin 2016, 48: 482–494.

    Google Scholar 

  8. Mak AKY, Hu ZG, Zhang JXX, Xiao Z, Lee TMC. Sex-related differences in neural activity during emotion regulation. Neuropsychol 2009, 47: 2900–2908.

    Article  Google Scholar 

  9. Yuan J, Xu S, Li C, Yang J, Li H, Yuan Y, et al. The enhanced processing of visual novel events in females: ERP correlates from two modified three-stimulus oddball tasks. Brain Res 2012, 1437: 77–88.

    Article  CAS  PubMed  Google Scholar 

  10. Yuan J, Yang J, Chen J, Meng X, Li H. Enhanced sensitivity to rare, emotion-irrelevant stimuli in females: Neural correlates. Neuroscience 2010, 169: 1758–1767.

    Article  CAS  PubMed  Google Scholar 

  11. Crouter AC, Manke BA, McHale SM. The family context of gender intensification in early adolescence. Child Dev 1995, 66: 317–329.

    Article  CAS  PubMed  Google Scholar 

  12. Hyde JS, Mezulis AH, Abramson LY. The ABCs of depression: Integrating affective, biological, and cognitive models to explain the emergence of the gender difference in depression. Psychol Rev 2008, 115: 291–313.

    Article  PubMed  Google Scholar 

  13. Shanahan L, McHale SM, Crouter AC, Osgood DW. Warmth with mothers and fathers from middle childhood to late adolescence: Within- and between-families comparisons. Dev Psychol 2007, 43: 551–563.

    Article  PubMed  Google Scholar 

  14. Aube J, Fichman L, Saltaris C, Koestner R. Gender differences in adolescent depressive symptomatology: Towards an integrated social-developmental model. J Soc Clin Psychol 2000, 19: 297–313.

    Article  Google Scholar 

  15. Petersen AC, Sarigiani PA, Kennedy RE. Adolescent depression: Why more girls? J Youth Adolesc 1991, 20: 247–271.

    Article  CAS  PubMed  Google Scholar 

  16. Priess HA, Lindberg SM, Hyde JS. Adolescent gender-role identity and mental health: Gender intensification revisited. Child Dev 2009, 80: 1531–1544.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wichstrom L. The emergence of gender difference in depressed mood during adolescence: The role of intensified gender socialization. Dev Psychol 1999, 35: 232–245.

    Article  CAS  PubMed  Google Scholar 

  18. Bourne VJ, Maxwell AM. Examining the sex difference in lateralisation for processing facial emotion: Does biological sex or psychological gender identity matter? Neuropsychol 2010, 48: 1289–1294.

    Article  Google Scholar 

  19. Reidy DE, Sloan CA, Zeichner A. Gender role conformity and aggression: Influence of perpetrator and victim conformity on direct physical aggression in women. Pers Individ Dif 2009, 46: 231–235.

    Article  Google Scholar 

  20. Grubb A, Turner E. Attribution of blame in rape cases: A review of the impact of rape myth acceptance, gender role conformity and substance use on victim blaming. Aggress Violent Behav 2012, 17: 443–452.

    Article  Google Scholar 

  21. Baucom DH. Sex role identity and the decision to regain control among women - A learned helplessness investigation. J Pers Soc Psychol 1983, 44: 334–343.

    Article  CAS  PubMed  Google Scholar 

  22. Kopper BA, Epperson DL. The experience and expression of anger: Relationships with gender, gender role socialization, depression, and mental health functioning. J Couns Psychol 1996, 43: 158–165.

    Article  Google Scholar 

  23. Milovchevich D, Howells K, Drew N, Day A. Sex and gender role differences in anger: an Australian community study. Pers Individ Dif 2001, 31: 117–127.

    Article  Google Scholar 

  24. Delplanque S, Silvert L, Hot P, Sequeira H. Event-related P3a and P3b in response to unpredictable emotional stimuli. Biol Psychol 2005, 68: 107–120.

    Article  PubMed  Google Scholar 

  25. Yuan J, Zhang Q, Chen A, Li H, Wang Q, Zhuang Z, et al. Are we sensitive to valence differences in emotionally negative stimuli? Electrophysiological evidence from an ERP study. Neuropsychol 2007, 45: 2764–2771.

    Article  Google Scholar 

  26. Lou Y, Meng X, Yang J, Zhang S, Long Q, Yuan J. The impact of extraversion on attentional bias to pleasant stimuli: neuroticism matters. Exp Brain Res 2016, 234: 721–731.

    Article  PubMed  Google Scholar 

  27. Yuan J, Zhang J, Zhou X, Yang J, Meng X, Zhang Q, et al. Neural mechanisms underlying the higher levels of subjective well-being in extraverts: Pleasant bias and unpleasant resistance. Cogn Affect Behav Neurosci 2012, 12: 175–192.

    Article  PubMed  Google Scholar 

  28. Meng X, Yang J, cai A, Ding X, Liu W, Li H, et al. The neural mechanisms underlying the aging-related enhancement of positive affects: Electrophysiological evidences. Front Aging Neurosci 2015, 7: 1–15.

  29. Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 2007, 39: 175–191.

    Article  PubMed  Google Scholar 

  30. Bem SL. Gender schema theory: A cognitive account of sex typing. Psychol Rev 1981, 88: 354–364.

    Article  Google Scholar 

  31. Qian M, Zhang G, Luo S, Zhang S. Sex role inventory for college students (CSRI). Chin J Psychol 2000, 32: 99–104.

    Google Scholar 

  32. Else-Quest NM, Higgins A, Allison C, Morton LC. Gender differences in self-conscious emotional experience: A meta-analysis. Psychol Bull 2012, 138: 947–981.

    Article  PubMed  Google Scholar 

  33. Bai L, Ma H, Huang YX, Luo Y. The development of native Chinese affective picture system-A pretest in 46 college students. Chin Ment Health J 2005, 19: 719–722.

    Google Scholar 

  34. Long Q, Yang J, Lou Y, Cai A, Yuan J. Humans’ emotional habituation to pleasant stimuli: Behavioral and electrophysiological evidence. Chin Sci Bull 2015, 60: 3594–3605.

    Article  Google Scholar 

  35. Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find Exp Clin Pharmacol 2002, 24: 5–12.

    PubMed  Google Scholar 

  36. Fischer AG, Ullsperger M. Real and fictive outcomes are processed differently but converge on a common adaptive mechanism. Neuron 2013, 79: 1243–1255.

    Article  CAS  PubMed  Google Scholar 

  37. Gu R, Zhang D, Luo Y, Wang H, Broster LS. Predicting risk decisions in a modified Balloon Analogue Risk Task: Conventional and single-trial ERP analyses. Cogn Affect Behav Neurosci 2018, 18: 99–116.

    Article  PubMed  Google Scholar 

  38. van Gerven M, Hesse C, Jensen O, Heskes T. Interpreting single trial data using groupwise regularisation. Neuroimage 2009, 46: 665–676.

    Article  PubMed  Google Scholar 

  39. Blankertz B, Lemm S, Treder M, Haufe S, Mueller K-R. Single-trial analysis and classification of ERP components - A tutorial. Neuroimage 2011, 56: 814–825.

    Article  PubMed  Google Scholar 

  40. Steinhauser M, Yeung N. Decision processes in human performance monitoring. J Neurosci 2010, 30: 15643–15653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Martinez AM, Kak AC. PCA versus LDA. IEEE Transactions on Pattern Analysis and Machine Intelligence 2001, 23: 228–233.

    Article  Google Scholar 

  42. Kriegeskorte N, Simmons WK, Bellgowan PSF, Baker CI. Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci 2009, 12: 535–540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lang PJ, Bradley MM, Cuthbert BN. International affective picture system (IAPS): Technical manual and affective ratings. NIMH Center for the Study of Emotion and Attention. Gainesville, FL: University of Florida 1997.

  44. Beck AT, Steer RA, Ball R, Ranieri W. Comparison of beck depression inventories-IA and -II in psychiatric outpatients. J Pers Assess 1996, 67: 588–597.

    Article  CAS  PubMed  Google Scholar 

  45. Shek DTL. The Chinese version of the State-Trait Anxiety Inventory: Its relationship to different measures of psychological well-being. J Clin Psychol 1993, 49: 349–358.

    Article  CAS  PubMed  Google Scholar 

  46. Heinze HJ, Mangun GR, Burchert W, Hinrichs H, Scholz M, Munte TF, et al. Combined spatial and temporal imaging of brain activity during selective attention in humans. Nature 1994, 372: 543–546.

    Article  CAS  PubMed  Google Scholar 

  47. Luck SJ. An introduction to the event-related potential technique. London, UK: The MIT Press 2005.

    Google Scholar 

  48. Marzecová A, Schettino A, Widmann A, Sanmiguel I, Kotz SA, Schröger E. Attentional gain is modulated by probabilistic feature expectations in a spatial cueing task: ERP evidence. Sci Rep 2018, 8: 54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Nagy E, Potts GF, Loveland KA. Sex-related ERP differences in deviance detection. Int J Psychophysiol 2003, 48: 285–292.

    Article  PubMed  Google Scholar 

  50. Orozco S, Ehlers CL. Gender differences in electrophysiological responses to facial stimuli. Biol Psychiatry 1998, 44: 281–289.

    Article  CAS  PubMed  Google Scholar 

  51. Yang J, Zhang S, Lou Y, Long Q, Liang Y, Xie S, et al. The increased sex differences in susceptibility to emotional stimuli during adolescence: An event-related potential study. Front Hum Neurosci 2018, 11: 660.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bahm NIG, Simon-Thomas ER, Main M, Hesse E. Unresolved loss, a risk factor for offspring, predicts event-related potential responses to death-related imagery. Dev Psychol 2017, 53: 191–199.

    Article  PubMed  Google Scholar 

  53. Carretie L, Hinojosa JA, Martin-Loeches M, Mercado F, Tapia M. Automatic attention to emotional stimuli: Neural correlates. Hum Brain Mapp 2004, 22: 290–299.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Clayson PE, Clawson A, Larson MJ. The effects of induced state negative affect on performance monitoring processes. Soc Cogn Affect Neurosci 2012, 7: 677–688.

    Article  PubMed  Google Scholar 

  55. Albert J, Lopez-Martin S, Carretie L. Emotional context modulates response inhibition: Neural and behavioral data. Neuroimage 2010, 49: 914–921.

    Article  PubMed  Google Scholar 

  56. Wang Y, Yang J, Yuan J, Fu A, Meng X, Li H. The impact of emotion valence on brain processing of behavioral inhibitory control: Spatiotemporal dynamics. Neurosci Lett 2011, 502: 112–116.

    Article  CAS  PubMed  Google Scholar 

  57. Cacioppo JT, Gardner WL. Emotion. Ann Rev Psychol 1999, 50: 191–214.

    Article  CAS  Google Scholar 

  58. Huang YX, Luo Y. Temporal course of emotional negativity bias: An ERP study. Neurosci Lett 2006, 398: 91–96.

    Article  CAS  PubMed  Google Scholar 

  59. Posner MI, Rothbart MK, Voelker P. Developing brain networks of attention. Curr Opin Pediatr 2016, 28: 720–724.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Weible AP. Remembering to attend: The anterior cingulate cortex and remote memory. Behav Brain Res 2013, 245: 63–75.

    Article  PubMed  Google Scholar 

  61. Bocquillon P, Bourriez J-L, Palmero-Soler E, Defebvre L, Derambure P, Dujardin K. Impaired early attentional processes in Parkinson’s disease: A high-resolution event-related potentials study. PLoS One 2015, 10: e0131654.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Saletu M, Anderer P, Saletu-Zyhlarz GM, Mandl M, Zeitlhofer J, Saletu B. Event-related-potential low-resolution brain electromagnetic tomography (ERP-LORETA) suggests decreased energetic resources for cognitive processing in narcolepsy. Clin Neurophysiol 2008, 119: 1782–1794.

    Article  PubMed  Google Scholar 

  63. Schindler S, Kissler J. Selective visual attention to emotional words: Early parallel frontal and visual activations followed by interactive effects in visual cortex. Hum Brain Mapp 2016, 37: 3575–3587.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Vogt BA, Laureys S. Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog Brain Res 2005, 150: 205–217.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Kayser J, Tenke CE, Abraham KS, Alschuler DM, Alvarenga JE, Skipper J, et al. Neuronal generator patterns at scalp elicited by lateralized aversive pictures reveal consecutive stages of motivated attention. Neuroimage 2016, 142: 337–350.

    Article  PubMed  Google Scholar 

  66. Rohde KB, Caspar F, Koenig T, Pascual-Leone A, Stein M. Neurophysiological traces of interpersonal pain: How emotional autobiographical memories affect event-related potentials. Emotion 2018, 18: 290–303.

    Article  PubMed  Google Scholar 

  67. Baumeister S, Hohmann S, Wolf I, Plichta MM, Rechtsteiner S, Zangl M, et al. Sequential inhibitory control processes assessed through simultaneous EEG-fMRI. Neuroimage 2014, 94: 349–359.

    Article  PubMed  Google Scholar 

  68. Sun S, Zhen S, Fu Z, Wu D-A, Shimojo S, Adolphs R, et al. Decision ambiguity is mediated by a late positive potential originating from cingulate cortex. Neuroimage 2017, 157: 400–414.

    Article  PubMed  Google Scholar 

  69. Young JW, Bismark AW, Sun Y, Zhang W, McIlwain M, Grootendorst I, et al. Neurophysiological characterization of attentional performance dysfunction in schizophrenia patients in a reverse-translated task. Neuropsychopharmacol 2017, 42: 1338–1348.

    Article  Google Scholar 

  70. Li H, Yuan J, Lin C. The neural mechanism underlying the female advantage in identifying negative emotions: An event-related potential study. Neuroimage 2008, 40: 1921–1929.

    Article  PubMed  Google Scholar 

  71. Stevens JS, Hamann S. Sex differences in brain activation to emotional stimuli: A meta-analysis of neuroimaging studies. Neuropsychol 2012, 50: 1578–1593.

    Article  Google Scholar 

  72. Brebner J. Gender and emotions. Pers Individ Dif 2003, 34: 387–394.

    Article  Google Scholar 

  73. Beehr TA, Farmer SJ, Glazer S, Gudanowski DM, Nair VN. The enigma of social support and occupational stress: source congruence and gender role effects. J occup Health Psychol 2003, 8: 220–231.

    Article  PubMed  Google Scholar 

  74. Harris T. Recent developments in understanding the psychosocial aspects of depression. Brit Med Bull 2001, 57: 17–32.

    Article  CAS  PubMed  Google Scholar 

  75. Hankin BL, Abramson LY. Development of gender differences in depression: An elaborated cognitive vulnerability-transactional stress theory. Psychol Bull 2001, 127: 773–796.

    Article  CAS  PubMed  Google Scholar 

  76. Cox SJ, Mezulis AH, Hyde JS. The influence of child gender role and maternal feedback to child stress on the emergence of the gender difference in depressive rumination in adolescence. Dev Psychol 2010, 46: 842–852.

    Article  PubMed  Google Scholar 

  77. Li CE, DiGiuseppe R, Froh J. The roles of sex, gender, and coping in adolescent depression. Adolescence 2006, 41: 409–415.

    CAS  PubMed  Google Scholar 

  78. Wupperman P, Neumann CS. Depressive symptoms as a function of sex-role, rumination, and neuroticism. Pers Individ Dif 2006, 40: 189–201.

    Article  Google Scholar 

  79. Berenbaum SA, Beltz AM. How early hormones shape gender development. Curr Opin Behav Sci 2016, 7: 53–60.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Guapo VG, Graeff FG, Tagliati Zani AC, Labate CM, dos Reis RM, Del-Ben CM. Effects of sex hormonal levels and phases of the menstrual cycle in the processing of emotional faces. Psychoneuroendocrinol 2009, 34: 1087–1094.

    Article  CAS  Google Scholar 

  81. Maciukaite L, Jarutyte L, Ruksenas O. The effects of menstrual cycle phase on processing of emotional images. J Psychophysiol 2017, 31: 179–187.

    Article  Google Scholar 

  82. Duke SA, Balzer BWR, Steinbeck KS. Testosterone and its effects on human male adolescent mood and behavior: a systematic review. J Adolesc Health 2014, 55: 315–322.

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Natural Science Foundation of China (31671164, 31970980, and 31971018) and a Guangdong Key Basic Research Grant (2018B030332001), Shenzhen Basic Research Project (JCYJ20180305124305294), the Shenzhen–Hong Kong Institute of Brain Science (2019SHIBS0003), and the Shenzhen Education Science Program (ybzz19014).

Author information

Authors and Affiliations

  1. The Laboratory for Affect Cognition and Regulation, Institute of Brain and Psychological Sciences, Sichuan Normal University, Chengdu, 610068, China

    Jiajin Yuan & Jiemin Yang

  2. College of Psychology, Shenzhen University, Shenzhen, 518060, China

    Hong Li & Dandan Zhang

  3. Faculty of Psychology, Southwest University, Chongqing, 400715, China

    Quanshan Long

  4. Department of Psychology, The University of Hong Kong, Hong Kong, 999077, China

    Tatia M. C. Lee

  5. Shenzhen-Hong Kong Institute of Brain Science, Shenzhen, 518060, China

    Dandan Zhang

  6. Shenzhen Institute of Neuroscience, Shenzhen, 518060, China

    Dandan Zhang

Authors
  1. Jiajin Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Quanshan Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiemin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tatia M. C. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dandan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dandan Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 309 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, J., Li, H., Long, Q. et al. Gender Role, But Not Sex, Shapes Humans’ Susceptibility to Emotion. Neurosci. Bull. 37, 201–216 (2021). https://doi.org/10.1007/s12264-020-00588-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-020-00588-2

Keywords

Search

Navigation