Brain Structure and Function

, Volume 224, Issue 9, pp 3201–3212 | Cite as

A dimensional approach to jealousy reveals enhanced fronto-striatal, insula and limbic responses to angry faces

  • Xiaoxiao Zheng
  • Lizhu Luo
  • Jialin Li
  • Lei Xu
  • Feng Zhou
  • Zhao Gao
  • Benjamin BeckerEmail author
  • Keith M. KendrickEmail author
Original Article


Jealousy is a complex social emotion combining the different primary emotions of anger, fear and sadness. Previous evidence has suggested the involvement of fronto-striatal dopaminergic circuitry in pathological jealousy, although little is known about overlaps with the neural representation of primary emotions involved in non-morbid jealousy and the utility of a dimensional neuroimaging approach. In the current study, 85 healthy subjects underwent fMRI during an emotional face recognition paradigm and resting state. A total of 150 faces (happy, angry, fearful, sad, neutral) were presented and subjects required to identify the expression and rate its intensity. Trait jealousy was assessed using the Multidimensional Jealousy Scale. Behavioral results showed that only intensity ratings of angry faces were positively associated with subjects’ jealousy scores. During processing of angry versus neutral expression faces, subjects with elevated jealousy exhibited increased activation in the right thalamus, insula, fusiform gyrus and hippocampus, left dorsal striatum, superior parietal lobule and bilateral cerebellum and inferior frontal gyrus after controlling for trait aggression and sex. Functional connectivity between the inferior frontal gyrus and dorsal striatum was also increased. No associations with resting-state functional connectivity were found. Overall, the present study demonstrates an association between exaggerated jealousy and increased intensity ratings of angry faces as well as activity and functional connectivity of the dorsal striatal–inferior frontal circuitry. Thus, increased emotional responsivity to social threat and enhanced activity in limbic regions and dopaminergic fronto-striatal circuitry may be features of both non-morbid and pathological jealousy confirming the utility of a dimensional approach.


Anger Jealousy Dimensional approach Face emotion Fronto-striatal circuits Limbic system 



This work was supported by the National Natural Science Foundation of China (NSFC) grant numbers 31530032 (KMK) and 91632117 (BB).

Author contributions statement

X.Z., B.B, and K.K designed the study and wrote the paper. X.Z. and L.L. prepared all the materials and programed the procedures. X.Z., L.L., J.L., L.X., and Z.G. acquired the data. X.Z., L.L, F.Z., B.B., and K.K. analyzed the data. X.Z., B.B and K.K interpreted the data and drafted the paper. All authors contributed to and have approved the final version of the manuscript.

Compliance with ethical standards

Conflict of interest

We have nothing to disclose in terms of disclosure of potential conflicts of interest.

Research involving human and/or animal participants

The study had full ethical approval by the local ethics committee at the University of Electronic Science and Technology of China and experiments were carried out in accordance with the latest revision of the Declaration of Helsinki.

Informed consent

Informed consent was obtained in writing from all individual participants included in the study.

Supplementary material

429_2019_1958_MOESM1_ESM.docx (713 kb)
Supplementary material 1 (DOCX 713 kb)


  1. Adolphs R, Damásio H, Tranel D, Damásio AR (1996) Cortical systems for the recognition of emotion in facial expressions. J Neurosci 16:7678–7687. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anders S, Lotze M, Erb M, Grodd W, Birbaumer N (2004) Brain activity underlying emotional valence and arousal: a response-related fMRI study. Hum Brain Mapp 23:200–209. CrossRefPubMedGoogle Scholar
  3. Andrade A, Paradis AL, Rouquette S, Poline JB (1999) Ambiguous results in functional neuroimaging data analysis due to covariate correlation. Neuroimage 10:483–486. CrossRefPubMedGoogle Scholar
  4. Angelides NH, Gupta J, Vickery TJ (2017) Associating resting-state connectivity with trait impulsivity. Soc Cog Affect Neurosci 12:1001–1008. CrossRefGoogle Scholar
  5. Aronson E, Pines A (1980). Exploring sexual jealousy. In annual meetings of the Western Psychological Association’s Convention, Honolulu, Hawaii, 5–9 May 1980Google Scholar
  6. Bauminger N (2004) The expression and understanding of jealousy in children with autism. Dev Psychopathol 16:157–175. CrossRefPubMedGoogle Scholar
  7. Baur V, Hänggi J, Langer N, Jäncke L (2013) Resting-state functional and structural connectivity within an insula-amygdala route specifically index state and trait anxiety. Biol Psychiatry 73:85–92. CrossRefPubMedGoogle Scholar
  8. Beck AT, Steer RA, Ball R, Ranieri WF (1996) Comparison of beck depression inventories-ia and-ii in psychiatric outpatients. J Pers Assess 67:588–597. CrossRefPubMedGoogle Scholar
  9. Björklund A, Dunnett SB (2007) Dopamine neuron systems in the brain: an update. Trends Neurosci 30:194–202. CrossRefPubMedGoogle Scholar
  10. Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using an SPM toolbox. NeuroImage. CrossRefGoogle Scholar
  11. Buss DM, Haselton M (2005) The evolution of jealousy. Trends Cogn Sci 9:506–507. CrossRefPubMedGoogle Scholar
  12. Buss AH, Perry M (1992) The aggression questionnaire. J Pers Soc Psych 63:452–459. CrossRefGoogle Scholar
  13. Camicioli R (2011) Neuropsychiatric disorders: othello syndrome - At the interface of neurology and psychiatry. Nat Rev Neurol 7:477–478. CrossRefPubMedGoogle Scholar
  14. Carr L, Iacoboni M, Dubeau M, Mazziotta JC, Lenzi GL (2003) Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci 100:5497–5502. CrossRefPubMedGoogle Scholar
  15. Carretié L, Ríos M, de la Gándara BS, Tapia M, Albert J, López-Martín S, Álvarez-Linera J (2009) The striatum beyond reward: caudate responds intensely to unpleasant pictures. Neurosci 164:1615–1622. CrossRefGoogle Scholar
  16. Chau SA, Herrmann N, Sherman C, Chung J, Eizenman M, Kiss A, Lanctot KL (2017) Visual selective attention toward novel stimuli predicts cognitive decline in Alzheimer’s disease patients. J Alzheimer’s disease 55:1339–1349. CrossRefGoogle Scholar
  17. Chen LF, Yen YS (2007) Taiwanese facial expression image database. Brain Mapping Laboratory, Institute of Brain Science, National Yang-Ming University, Taipei, TaiwanGoogle Scholar
  18. Colibazzi T, Posner J, Wang Z, Gorman D, Gerber A, Yu S, Zhu H, Kangarlu A, Duan Y, Russell J, Peterson BS (2010) Neural systems subserving valence and arousal during the experience of induced emotions. Emotion 10:377–389. CrossRefPubMedGoogle Scholar
  19. Cunningham WA, Raye CL, Johnson MK (2004) Implicit and explicit evaluation: fMRI correlates of valence, emotional intensity, and control in the processing of attitudes. J Cogn Neurosci 16:1717–1729. CrossRefPubMedGoogle Scholar
  20. Cuthbert BN (2014) The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry 13:28–35. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Delgado MR (2007) Reward-related responses in the human striatum. Ann NY Acad Sci 1104:70–88. CrossRefPubMedGoogle Scholar
  22. Ekman P (1999) Basic Emotions. In: Dalglish T, Power MJ (eds) Handbook of Cognition and Emotion. John Wiley and Sons, New York, pp 45–60. CrossRefGoogle Scholar
  23. Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 15:85–93. CrossRefPubMedGoogle Scholar
  24. Fisher HE, Brown LL, Aron A, Strong G, Mashek D (2010) Reward, addiction, and emotion regulation systems associated with rejection in love. J Neurophysiol 104:51–60. CrossRefPubMedGoogle Scholar
  25. Frank MJ, Seeberger LC, O’Reilly RC (2004) By carrot or by stick: cognitive reinforcement learning in Parkinsonism. Science 306:1940–1943. CrossRefPubMedGoogle Scholar
  26. 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 (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 44:418–432Google Scholar
  27. Gable PA, Poole BD (2014) Influence of trait behavioral inhibition and behavioral approach motivation systems on the LPP and frontal asymmetry to anger pictures. Soc Cogn Affect Neurosci 9:182–190. CrossRefPubMedGoogle Scholar
  28. Gong X, Huang Y, Wang Y, Luo Y (2011) Revision of the Chinese facial affective picture system. Chinese Ment Health J 25:40–46Google Scholar
  29. Graff-Radford J, Whitwell JL, Geda YE, Josephs KA (2012) Clinical and imaging features of Othello’s syndrome. Eur J Neurol 19:38–46. CrossRefPubMedGoogle Scholar
  30. Guadagno RE, Sagarin BJ (2010) Sex differences in jealousy: an evolutionary perspective on online infidelity. J Appl Soc Psychol 40:2636–2655. CrossRefGoogle Scholar
  31. Hägele C, Schlagenhauf F, Rapp M, Sterzer P, Beck A, Bermpohl F, Stoy M, Ströhle A, Wittchen H, Dolan RJ, Heinz A (2015) Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacol 232:331–341. CrossRefGoogle Scholar
  32. Hägele C, Friedel E, Schlagenhauf F, Sterzer P, Beck A, Bermpohl F, Stoy M, Held-Poschardt D, Wittmann A, Ströhle A, Heinz A (2016) Affective responses across psychiatric disorders—A dimensional approach. Neurosci Lett 623:71–78. CrossRefPubMedGoogle Scholar
  33. Hahn A, Stein P, Windischberger C, Weissenbacher A, Spindelegger C, Moser E, Kasper S, Lanzenberger R (2011) Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. NeuroImage 56:881–889. CrossRefPubMedGoogle Scholar
  34. Harmon-Jones E, Peterson CK, Harris CR (2009) Jealousy: novel methods and neural correlates. Emotion 9:113–117. CrossRefPubMedGoogle Scholar
  35. Harris CR (2004) The evolution of jealousy: did men and women, facing different selective pressures, evolve different“brands” of jealousy? Recent evidence suggests not. Am Sci 92:62–71CrossRefGoogle Scholar
  36. Huguenard JR, McCormick DA (2007) Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci 30:350–356. CrossRefPubMedGoogle Scholar
  37. Hupka RB (1984) Jealousy: compound emotion or label for a particular situation? Motiv Emotion 8:141–155CrossRefGoogle Scholar
  38. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine D, Quinn K, Sanislow C, Wang P (2010) Research Domain Criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry 167:748–751. CrossRefPubMedGoogle Scholar
  39. Kawashima R, Sugiura M, Kato T, Nakamura A, Hatano K, Ito K, Fukuda H, Kojima S, Nakamura K (1999) The human amygdala plays an important role in gaze monitoring: a PET study. Brain 122:779–783. CrossRefPubMedGoogle Scholar
  40. Lazarus RS (1992) Emotion and Adaptation. Contemp Sociol 21:522. CrossRefGoogle Scholar
  41. Li W, Qian M (1995) Revision of the State-Trait anxiety inventory with sample of Chinese college students. Chinese Sci Abs Series B 3:50Google Scholar
  42. Li X, Phillips MR, Zhang Y, Niu Y, Tong Y, Yang S (2011) Development, reliability and validity of the Chinese version of Buss and Perry aggression questionnaire. Chinese J Nervous Ment Dis 37:607–613Google Scholar
  43. Li J, Xu L, Zheng X, Fu M, Zhou F, Xu X, Ma X, Li K, Kendrick KM, Becker B (2019) Common and dissociable contributions of alexithymia and autism to domain-specific interoceptive dysregulations-a dimensional neuroimaging approach. Psychother Psychosom 88:187–189. CrossRefPubMedGoogle Scholar
  44. Luauté JP, Saladini O, Luauté MD (2008) Neuroimaging correlates of chronic delusional jealousy after right cerebral infarction. J Neuropsychiatry Clin Neurosci 20:245–247. CrossRefPubMedGoogle Scholar
  45. Luo L, Becker B, Zheng X, Zhao Z, Xu X, Zhou F, Wang J, Kou J, Dai J, Kendrick KM (2018) A dimensional approach to determine common and specific neurofunctional markers for depression and social anxiety during emotional face processing. Hum Brain Mapp 39:758–771. CrossRefPubMedGoogle Scholar
  46. Lupo M, Troisi E, Chiricozzi FR, Clausi S, Molinari M, Leggio M (2015) Inability to process negative emotions in cerebellar damage: a functional transcranial doppler sonographic study. Cerebellum 14:663–669. CrossRefPubMedGoogle Scholar
  47. Marazziti D, Poletti M, Dell’Osso L, Baroni S, Bonuccelli U (2013) Prefrontal cortex, dopamine, and jealousy endophenotype. CNS Spectr 18:6–14. CrossRefPubMedGoogle Scholar
  48. McCormick DA, Bal T (1994) Sensory gating mechanisms of the thalamus. Curr Op Neurobiol 4:550–556. CrossRefPubMedGoogle Scholar
  49. McLaren DG, Ries ML, Xu G, Johnson SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 61:1277–1286. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mitsuhata Y, Tsukagoshi H (1992) Cerebellar infarction presenting erotic delusion and delusion of jealousy in the acute phase. Rinsho Shinkeigaku Clin Neurol 32:1256–1260Google Scholar
  52. Mumford JA, Poline JB, Poldrack RA (2015) Orthogonalization of regressors in fMRI models. PLoS One 10:e0126255. CrossRefPubMedPubMedCentralGoogle Scholar
  53. N’Diaye K, Sander D, Vuilleumier P (2009) Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity. Emotion 9:798–806. CrossRefPubMedGoogle Scholar
  54. Nakamura K, Kawashima R, Ito K, Sugiura M, Kato T, Nakamura A, Hatano K, Nagumo S, Kubota K, Fukuda H, Kojima S (1999) Activation of the right inferior frontal cortex during assessment of facial emotion. J Neurophysiol 82:1610–1614. CrossRefPubMedGoogle Scholar
  55. Narumoto J, Nakamura K, Kitabayashi Y, Fukui K (2006) Othello syndrome secondary to right orbitofrontal lobe excision. J Neuropsychiatry Clin Neurosci 18:560–561. CrossRefPubMedGoogle Scholar
  56. O’Brien RM (2007) A caution regarding rules of thumb for variance inflation factors. Quality Quantity 41:673–690. CrossRefGoogle Scholar
  57. Ohashi K, Anderson CM, Bolger EA, Khan A, McGreenery CE, Teicher MH (2017) Childhood maltreatment is associated with alteration in global network fiber-tract architecture independent of history of depression and anxiety. NeuroImage 150:50–59. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Orosz G, Szekeres Á, Kiss ZG, Farkas P, Roland-Lévy C (2015) Elevated romantic love and jealousy if relationship status is declared on Facebook. Front Psychol 6:214. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Parrott WG, Smith RH (1993) Distinguishing the experiences of envy and jealousy. J Pers Soc Psychol 64:906–920. CrossRefPubMedGoogle Scholar
  60. Pauls DL, Abramovitch A, Rauch SL, Geller DA (2014) Obsessive-compulsive disorder: an integrative genetic and neurobiological perspective. Nat Rev Neurosci 15:410–424. CrossRefPubMedGoogle Scholar
  61. Pfeiffer SM, Wong PTP (1989) Multidimensional jealousy. J Soc Pers Rel 6:181–196CrossRefGoogle Scholar
  62. Phillips ML, Williams LM, Heining M, Herba CM, Russell T, Andrew C, Bullmore ET, Brammer MJ, Williams SC, Morgan M, Young AW, Gray JA (2004) Differential neural responses to overt and covert presentations of facial expressions of fear and disgust. NeuroImage 21:1484–1496. CrossRefPubMedGoogle Scholar
  63. Poletti M, Perugi G, Logi C, Romano A, Del Dotto P, Ceravolo R, Rossi G, Pepe P, Dell’Osso L, Bonuccelli U (2012) Dopamine agonists and delusional jealousy in Parkinson’s disease: a cross-sectional prevalence study. Move Dis 27:1679–1682. CrossRefGoogle Scholar
  64. Rilling JK, Winslow JT, Kilts CD (2004) The neural correlates of mate competition in dominant male rhesus macaques. Biol Psychiatry 56:364–375. CrossRefPubMedGoogle Scholar
  65. Ruzich E, Allison C, Smith P, Watson P, Auyeung B, Ring H, Baron-Cohen S (2015) Measuring autistic traits in the general population: a systematic review of the Autism-Spectrum Quotient (AQ) in a nonclinical population sample of 6,900 typical adult males and females. Mol Autism 6:2. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sevy S, Hassoun Y, Bechara A, Yechiam E, Napolitano B, Burdick K, Delman H, Malhotra A (2006) Emotion-based decision-making in healthy subjects: short-term effects of reducing dopamine levels. Psychopharmacol 188:228–235. CrossRefGoogle Scholar
  67. Shamay-Tsoory SG, Tibi-Elhanany Y, Aharon-Peretz J (2007) The green-eyed monster and malicious joy: the neuroanatomical bases of envy and gloating (schadenfreude). Brain 130:1663–1678. CrossRefPubMedGoogle Scholar
  68. Slotnick SD (2017) Cluster success: fMRI inferences for spatial extent have acceptable false-positive rates. Cogn Neurosci 8:150–155. CrossRefPubMedGoogle Scholar
  69. Spielberger CD (1983) Manual for the State-Trait Anxiety Inventory STAI (form Y)(“self-evaluation questionnaire”)Google Scholar
  70. Sprengelmeyer R, Jentzsch I (2006) Event related potentials and the perception of intensity in facial expressions. Neuropsychologia 44:2899–2906. CrossRefPubMedGoogle Scholar
  71. Strata P (2015) The Emotional Cerebellum. Cerebellum 14:570–577. CrossRefPubMedGoogle Scholar
  72. Sun Y, Yu H, Chen J, Liang J, Lu L, Zhou X, Shi J (2016) Neural substrates and behavioral profiles of romantic jealousy and its temporal dynamics. Sci Rep 6:27469. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Takahashi H, Matsuura M, Yahata N, Koeda M, Suhara T, Okubo Y (2006) Men and women show distinct brain activations during imagery of sexual and emotional infidelity. NeuroImage 32:1299–1307. CrossRefPubMedGoogle Scholar
  74. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289. CrossRefPubMedGoogle Scholar
  75. Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C (2007) Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull 71:601–609. CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang Z, Yuan C, Huang J, Li Z, Chen J, Zhang H, Fang D, Xiao Z (2011) Reliability and validity of the Chinese version of Beck Depression Inventory-II among depression patients. Chinese Ment Health J 25:476–480Google Scholar
  77. Wicker B, Keysers C, Plailly J, Royet J-P, Gallese V, Rizzolotti G (2003) Both of us disgusted in my insula:the common neural basis of seeing and feeling disgust. Neuron 40:655–664CrossRefGoogle Scholar
  78. Xiang Y, Kong F, Wen X, Wu Q, Mo L (2016) Neural correlates of envy: regional homogeneity of resting-state brain activity predicts dispositional envy. NeuroImage 142:225–230. CrossRefPubMedGoogle Scholar
  79. Yan C, Zang Y (2010) DPARSF: a MATLAB toolbox for” pipeline” data analysis of resting-state fMRI. Front Sys Neurosci 4:13. CrossRefGoogle Scholar
  80. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7:464–476. CrossRefPubMedGoogle Scholar
  81. Zang Y, He Y, Zhu C, Cao Q, Sui M, Liang M, Tian L, Jiang T, Feng W (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29:83–91. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformationUniversity of Electronic Science and Technology of ChinaChengduChina

Personalised recommendations