Neural dynamics of pride and shame in social context: an approach with event-related brain electrical potentials

Sánchez-García, Jose; Rodríguez, Gema Esther; Hernández-Gutiérrez, David; Casado, Pilar; Fondevila, Sabela; Jiménez-Ortega, Laura; Muñoz, Francisco; Rubianes, Miguel; Martín-Loeches, Manuel

doi:10.1007/s00429-021-02296-7

Original Article
Published: 24 May 2021

Neural dynamics of pride and shame in social context: an approach with event-related brain electrical potentials

Jose Sánchez-García¹,
Gema Esther Rodríguez¹,
David Hernández-Gutiérrez¹,
Pilar Casado^1,2,
Sabela Fondevila^1,2,
Laura Jiménez-Ortega^1,2,
Francisco Muñoz^1,2,
Miguel Rubianes¹ &
Manuel Martín-Loeches^1,2

Brain Structure and Function volume 226, pages 1855–1869 (2021)Cite this article

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Abstract

The neural underpinnings of social emotions such as pride and shame are largely unknown. The present study aims to add evidence by exploiting the advantage of event-related brain electrical potentials (ERP) to examine the neural processes as they unfold over time. For this purpose, a dot-estimation task was adapted to explore these emotions as elicited in a simulated social context. Pride prompted an early negativity seemingly originated in medial parietal regions (precuneus) and possibly reflecting social comparison processes in successful trials. This was followed by a late positivity originated in medial frontal regions, probably reflecting the verification of singularly successful trials. Shame, in turn, elicited an early negativity apparently originated in the cuneus, probably related to mental imagery of the social situation. It was followed by a late positivity mainly originated in the same regions as the early negativity for pride, then conceivably reflecting social comparison processes, in this occasion in unsuccessful trials. None of these fluctuations correlated with self-reported feelings of either emotion, suggesting that they instead relate to social cognitive computations necessary to achieve them. The present results provide a dynamic depiction of neural mechanisms underlying these social emotions, probing the necessity to study them using an integrated approach with different techniques.

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References

Abe JAA, Izard CE (1999) The developmental functions of emotions: an analysis in terms of differential emotions theory. Cognit Emot 13(5):523–549. https://doi.org/10.1080/026999399379177
Article Google Scholar
Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7(4):268–277
CAS PubMed Article Google Scholar
Awan FG, Saleem O, Kiran A (2019) Recent trends and advances in solving the inverse problem for EEG source localization. Inverse Probl Sci Eng 27:1521–1536. https://doi.org/10.1080/17415977.2018.1490279
Article Google Scholar
Bastin C, Harrison BJ, Davey CG, Moll J, Whittle S (2016) Feelings of shame, embarrassment and guilt and their neural correlates: a systematic review. Neurosci Biobehav Rev 71:455–471. https://doi.org/10.1016/j.neubiorev.2016.09.019
PubMed Article Google Scholar
Beer JS, Keltner D (2004) What is unique about self-conscious emotions? Psychol Inq 15(2):126–129
Article Google Scholar
Bonini F, Burle B, Liégeois-Chauvel C, Régis J, Chauvel P, Vidal F (2014) Action monitoring and medial frontal cortex: leading role of supplementary motor area. Science 343(6173):888–891
CAS PubMed Article Google Scholar
Brusini P, Dehaene-Lambertz G, van Heugten M, de Carvalho A, Goffinet F, Fievet AC, Christophe A (2017) Ambiguous function words do not prevent 18-month-olds from building accurate syntactic category expectations: an ERP study. Neuropsychologia 98:4–12. https://doi.org/10.1016/j.neuropsychologia.2016.08.015
PubMed Article Google Scholar
Cohen J (1988) Statistical Power Analysis for the Behavioral sciences, 2nd edn. Lawrence erlbaum associates, New York
Google Scholar
Dancey CP, Reidy J (2007) Statistics without maths for psychology. Pearson Education
Davey CG, Pujol J, Harrison BJ (2016) Mapping the self in the brain’s default mode network. Neuroimage 132:390–397. https://doi.org/10.1016/j.neuroimage.2016.02.022
PubMed Article Google Scholar
Durkee PK, Lukaszewski AW, Buss DM (2019) Pride and shame: Key components of a culturally universal status management system. Evol Hum Behav 40(5):470–478
Article Google Scholar
Fields EC, Kuperberg GR (2019) Having your cake and eating it too: flexibility and power with mass univariate statistics for ERP data. Psychophysiology 57(2):e13468. https://doi.org/10.1111/psyp.13468
PubMed Article PubMed Central Google Scholar
Flinn MV, Geary DC, Ward CV (2005) Ecological dominance, social competition, and coalitionary arms races: Why humans evolved extraordinary intelligence. Evol Hum Behav 26(1):10–46. https://doi.org/10.1016/j.evolhumbehav.2004.08.005
Article Google Scholar
Gilbert P (2000) The relationship of shame, social anxiety and depression: the role of the evaluation of social rank. Clin Psychol Psychother 7(3):174–189. https://doi.org/10.1002/1099-0879(200007)7:3%3c174::AID-CPP236%3e3.0.CO;2-U
Article Google Scholar
Gilead M, Katzir M, Eyal T, Liberman N (2016) Neural correlates of processing “self-conscious” vs “basic” emotions. Neuropsychologia 81:207–218. https://doi.org/10.1016/j.neuropsychologia.2015.12.009
PubMed Article Google Scholar
Groppe DM, Urbach TP, Kutas M (2011a) Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. Psychophysiology 48(12):1711–1725. https://doi.org/10.1111/j.1469-8986.2011.01273.x
PubMed Article PubMed Central Google Scholar
Groppe DM, Urbach TP, Kutas M (2011b) Mass univariate analysis of event-related brain potentials/fields II: Simulation studies. Psychophysiology 48(12):1726–1737. https://doi.org/10.1111/j.1469-8986.2011.01272.x
PubMed Article PubMed Central Google Scholar
Haidt J (2003) The moral emotions. In: Davidson RJ, Scherer KR, Goldsmith HH (eds) Handbook of affective sciences. Oxford university press, UK, pp 852–870
Google Scholar
Hong YJ, Park S, Kyeong S, Kim JJ (2019) Neural basis of professional pride in the reaction to uniform wear. Front Hum Neurosci 13:253. https://doi.org/10.3389/fnhum.2019.00253
PubMed Article PubMed Central Google Scholar
Jiménez-Ortega L, Ramos-Badaya E, Hernández-Gutiérrez D, Silvera M, Espuny J, Garcia JS, Martín-Loeches M (2020) Effects of reader’s facial expression on syntactic processing: A brain potential study. Brain Res 1736:146745
PubMed Article Google Scholar
Keuken MC, Hardie A, Dorn BT, Dev S, Paulus MP, Jonas KJ, Pineda JA (2011) The role of the left inferior frontal gyrus in social perception: an rTMS study. Brain Res 1383:196–205. https://doi.org/10.1016/j.brainres.2011.01.073
CAS PubMed Article Google Scholar
Lakens D (2013) Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 4:863. https://doi.org/10.3389/fpsyg.2013.00863
PubMed Article PubMed Central Google Scholar
Leng B, Wang X, Cao B, Li F (2016) Frontal negativity: an electrophysiological index of interpersonal guilt. Soc Neurosci 12(6):649–660. https://doi.org/10.1080/17470919.2016.1223749
PubMed Article Google Scholar
Lewis M, Haviland-Jones JM (2000) Handbook of emotions, 2nd edn. Guilford press, New York
Google Scholar
Lopes da Silva F, Niedermeyer E (2005) Electroencephalography: basic principles, clinical applications, and related fields. Lippincott Williams & Wilkins, Philadelphia
Google Scholar
Lou HC, Luber B, Crupain M, Keenan JP, Nowak M, Kjaer TW, Sackeim HA, Lisanby SH (2004) Parietal cortex and representation of the mental Self. Proc Natl Acad Sci USA 101(17):6827–6832. https://doi.org/10.1073/pnas.0400049101
CAS PubMed Article PubMed Central Google Scholar
Luck SJ (2014) An introduction to the event-related potential technique. MIT Press
Google Scholar
Luck SJ, Hillyard SA (1984) Electrophysiological correlates of feature analysis during visual search. Psychophysiology 31(3):291–308. https://doi.org/10.1111/j.1469-8986.1994.tb02218.x
Article Google Scholar
Makeig, S., Enghoff, S., Jung, T. P., & Sejnowski, T. J. (2000, June 19–22). Moving-window ICA decomposition of EEG data reveals event-related changes in oscillatory brain activity [Conference paper]. Second International Workshop on Independent Component Analysis and Signal Separation, Helsinki, Finland. https://sccn.ucsd.edu/~scott/pdf/ICA00a.pdf
Menesini E, Camodeca M (2008) Shame and guilt as behaviour regulators: Relationships with bullying, victimization and prosocial behaviour. B J Develop Psychol 26(2):183–196. https://doi.org/10.1348/026151007X205281
Article Google Scholar
Michl P, Meindl T, Meister F, Born C, Engel RR, Reiser M, Hennig-Fast K (2014) Neurobiological underpinnings of shame and guilt: a pilot fMRI study. Soc Cogn Affect Neurosci 9(2):150–157. https://doi.org/10.1093/scan/nss114
PubMed Article Google Scholar
Mochizuki AA, Sudo MM, Kirino E, Itoh K (2014) Brain activation associated with motor imagery of coordination exercises and social abilities. Eur J Sport Sci 14(7):671–677. https://doi.org/10.1080/17461391.2014.893019
PubMed Article Google Scholar
Moll J, Zahn R, de Oliveira-Souza R, Krueger F, Grafman J (2005) The neural basis of human moral cognition. Nat Rev Neurosci 6(10):799–809
CAS PubMed Article Google Scholar
Northoff G, Heinzel A, De Greck M, Bermpohl F, Dobrowolny H, Panksepp J (2006) Self-referential processing in our brain––a meta-analysis of imaging studies on the self. Neuroimage 31(1):440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002
PubMed Article Google Scholar
Oldfield RC (1971) The assessment and analysis of handiness: the Edinburgh inventory. Neuropsychologia 9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4
CAS PubMed Article Google Scholar
Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D (2002) Functional imaging with low resolution brain electromagnetic tomography (LORETA): a review. Methods Find Exp Clinic Pharmacol 24 Suppl C:91–95
CAS Google Scholar
Qin P, Northoff G (2011) How is our self related to midline regions and the default-mode network? Neuroimage 57(3):1221–1233. https://doi.org/10.1016/j.neuroimage.2011.05.028
PubMed Article Google Scholar
Robertson TE, Sznycer D, Delton AW, Tooby J, Cosmides L (2018) The true trigger of shame: Social devaluation is sufficient, wrongdoing is unnecessary. Evol Hum Behav 39(5):566–573. https://doi.org/10.1016/j.evolhumbehav.2018.05.010
Article Google Scholar
Roth L, Kaffenberger T, Herwig U, Brühl AB (2014) Brain activation associated with pride and shame. Neuropsychobiology 69(2):95–106. https://doi.org/10.1159/000358090
PubMed Article Google Scholar
Sánchez-García J, Espuny J, Hernández-Gutiérrez D, Casado P, Muñoz F, Jiménez-Ortega L, Martín-Loeches M (2019) Neurofunctional characterization of early prefrontal processes contributing to interpersonal guilt. Cogn Affect Behav Neurosci 19(5):1192–1202. https://doi.org/10.3758/s13415-019-00748-6
PubMed Article Google Scholar
Schurz M, Radua J, Aichhorn M, Richlan F, Perner J (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev 42:9–34. https://doi.org/10.1016/j.neubiorev.2014.01.009
PubMed Article Google Scholar
Simon-Thomas ER, Godzik J, Castle E, Antonenko O, Ponz A, Kogan A, Keltner DJ (2012) An fMRI study of caring vs self-focus during induced compassion and pride. Soc Cognit Affect Neurosci 7(6):635–648. https://doi.org/10.1093/scan/nsr045
Article Google Scholar
Sznycer D, Al-Shawaf L, Bereby-Meyer Y, Curry OS, De Smet D, Ermer E, McClung J (2017a) Cross-cultural regularities in the cognitive architecture of pride. Proc Natl Acad Sci 114:1874–1879
CAS PubMed Article PubMed Central Google Scholar
Sznycer D, Cosmides L, Tooby J (2017b) Adaptationism carves emotions at their functional joints. Psychol Inq 28:56–62
Article Google Scholar
Sznycer D, Xygalatas D, Agey E, Alami S, An XF, Ananyeva KI, Fukushima S (2018a) Cross-cultural invariances in the architecture of shame. Proc Natl Acad Sci 115:9702–9707
CAS PubMed Article PubMed Central Google Scholar
Sznycer D, Xygalatas D, Alami S, An XF, Ananyeva KI, Fukushima S, Onyishi IE (2018b) Invariances in the architecture of pride across small-scale societies. Proc Natl Acad Sci 115:8322–8327
CAS PubMed Article PubMed Central Google Scholar
Takahashi H, Matsuura M, Koeda M, Yahata N, Suhara T, Kato M, Okubo Y (2008) Brain activations during judgments of positive self-conscious emotion and positive basic emotion: pride and joy. Cereb Cortex 18(4):898–903. https://doi.org/10.1093/cercor/bhm120
PubMed Article Google Scholar
Tangney JP, Dearing RL (2003) Shame and guilt. Guilford press
Google Scholar
Tangney JP, Wagner PE, Fletcher C, Gramzow R (1992) Shamed into anger? The relation of shame and guilt to anger and self-reported aggression. J Pers Soc Psychol 62(4):669–675. https://doi.org/10.1037//0022-3514.62.4.669
CAS PubMed Article Google Scholar
Tangney JP, Miller R, Flicker L, Barlow DH (1996) Are shame, guilt, and embarrassment distinct emotions? J Pers Soc Psychol 70(6):1256–1269. https://doi.org/10.1037//0022-3514.70.6.1256
CAS PubMed Article Google Scholar
Tangney JP, Stuewig J, Mashek DJ (2007) Moral emotions and moral behavior. Annu Rev Psychol 58:345–372. https://doi.org/10.1146/annurev.psych.56.091103.070145
PubMed Article PubMed Central Google Scholar
Tracy JL, Randles D (2011) Four models of basic emotions: a review of Ekman and Cordaro, Izard, Levenson, and Panksepp and Watt. Emot Rev 3(4):397–405. https://doi.org/10.1177/1754073911410747
Article Google Scholar
Tracy JL, Robins RW (2007) The psychological structure of pride: a tale of two facets. J Pers Soc Psychol 92(3):506–525. https://doi.org/10.1037/0022-3514.92.3.506
PubMed Article Google Scholar
Whittle S, Liu K, Bastin C, Harrison BJ, Davey CG (2016) Neurodevelopmental correlates of proneness to guilt and shame in adolescence and early adulthood. Dev Cogn Neurosci 19:51–57
PubMed Article PubMed Central Google Scholar
Zahn R, Moll J, Paiva M, Garrido G, Krueger F, Huey ED, Grafman J (2009) The neural basis of human social values: evidence from functional MRI. Cereb Cortex 19(2):276–283. https://doi.org/10.1093/cercor/bhn080
PubMed Article Google Scholar
Zahn R, Garrido G, Moll J, Grafman J (2014) Individual differences in posterior cortical volume correlate with proneness to pride and gratitude. Soc Cognit Affect Neurosci 9(11):1676–1683. https://doi.org/10.1093/scan/nst158
Article Google Scholar
Zhu R, Wu H, Xu Z, Tang H, Shen X, Mai X, Liu C (2017) Early distinction between shame and guilt processing in an interpersonal context. Soc Neurosci 14(1):1–14. https://doi.org/10.1080/17470919.2017.1391119
Article Google Scholar
Zhu R, Feng C, Zhang S, Mai X, Liu C (2019) Differentiating guilt and shame in an interpersonal context with univariate activation and multivariate pattern analyses. Neuroimage 186:476–486. https://doi.org/10.1016/j.neuroimage.2018.11.012
PubMed Article Google Scholar

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Authors and Affiliations

Center for Human Evolution and Behavior, UCM-ISCIII. Avda Monforte de Lemos, 5, Pabellón 14, 28029, Madrid, Spain
Jose Sánchez-García, Gema Esther Rodríguez, David Hernández-Gutiérrez, Pilar Casado, Sabela Fondevila, Laura Jiménez-Ortega, Francisco Muñoz, Miguel Rubianes & Manuel Martín-Loeches
Psychobiology and Methods in Behavioral Sciences Department, Complutense University of Madrid, Madrid, Spain
Pilar Casado, Sabela Fondevila, Laura Jiménez-Ortega, Francisco Muñoz & Manuel Martín-Loeches

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Jose Sánchez-García
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Gema Esther Rodríguez
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David Hernández-Gutiérrez
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Pilar Casado
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Sabela Fondevila
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Laura Jiménez-Ortega
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Francisco Muñoz
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Miguel Rubianes
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Manuel Martín-Loeches
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Sánchez-García, J., Rodríguez, G.E., Hernández-Gutiérrez, D. et al. Neural dynamics of pride and shame in social context: an approach with event-related brain electrical potentials. Brain Struct Funct 226, 1855–1869 (2021). https://doi.org/10.1007/s00429-021-02296-7

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Received: 20 September 2020
Accepted: 08 May 2021
Published: 24 May 2021
Issue Date: July 2021
DOI: https://doi.org/10.1007/s00429-021-02296-7

Keywords

ERP
Pride
Shame
Social emotions
Medial frontal areas
Cuneus
Precuneus