Skip to main content
SpringerLink
Log in

Altered empathy-related resting-state functional connectivity in patients with bipolar disorder

  • Original Paper
  • Published:
European Archives of Psychiatry and Clinical Neuroscience Aims and scope Submit manuscript

Abstract

Empathy is the ability to generate emotional responses (i.e., cognitive empathy) and to make cognitive inferences (i.e., affective empathy) to other people’s emotions. Empirical evidence suggests that patients with bipolar disorder (BD) exhibit impairment in cognitive empathy, but findings on affective empathy are inconsistent. Few studies have examined the neural mechanisms of cognitive and affective empathy in patients with BD. In this study, we examined the empathy-related resting-state functional connectivity (rsFC) in BD patients. Thirty-seven patients with BD and 42 healthy controls completed the self-report Questionnaires of Cognitive and Affective Empathy (QCAE), the Yoni behavioural task, and resting-sate fMRI brain scans. Group comparison of empathic ability was conducted. The interactions between group and empathic ability on seed-based whole brain rsFC were examined. BD patients scored lower on the Online Simulation subscale of the QCAE and showed positive correlations between cognitive empathy and the rsFC of the dorsal Medial Prefrontal Cortex (dmPFC) with the lingual gyrus. The correlations between cognitive empathy and the rsFC of the temporal–parietal junction (TPJ) with the fusiform gyrus, the cerebellum and the parahippocampus were weaker in BD patients than that in healthy controls. These findings highlight the underlying neural mechanisms of empathy impairments in BD patients.

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.

Fig.1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. World-Health-Organization (1993) The ICD-10 classification of mental and behavioural disorders: diagnostic criteria for research. World Health Organization

  2. Vazquez GH, Holtzman JN, Lolich M et al (2015) Recurrence rates in bipolar disorder: systematic comparison of long-term prospective, naturalistic studies versus randomized controlled trials. Eur Neuropsychopharmacol 25:1501–1512

    Article  CAS  PubMed  Google Scholar 

  3. Vlad M, Raucher-Chene D, Henry A, Kaladjian A (2018) Functional outcome and social cognition in bipolar disorder: is there a connection? Eur Psychiatry 52:116–125

    Article  PubMed  Google Scholar 

  4. Bio DS, Soeiro-de-Souza MG, Otaduy MCG et al (2013) The impact of limbic system morphology on facial emotion recognition in bipolar I disorder and healthy controls. Neuropsychiatr Dis Treat 9:743

    PubMed  PubMed Central  Google Scholar 

  5. Moreno-Manso JM, García-Baamonde ME, Blázquez-Alonso M et al (2018) Empathy and coping strategies in youths subject to protection measures. Child Youth Serv Rev 93:100–107

    Article  Google Scholar 

  6. Reniers RLEP, Corcoran R, Drake R et al (2011) The QCAE: a questionnaire of cognitive and affective empathy. J Pers Assess 93:84–95

    Article  PubMed  Google Scholar 

  7. Shamay-Tsoory SG, Harari H, Aharon-Peretz J, Levkovitz Y (2010) The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies. Cortex 46:668–677

    Article  PubMed  Google Scholar 

  8. Inoue Y, KkS Y (2006) Deficit in theory of mind is a risk for relapse of major depression. J Affect Disord 95:125–127

    Article  CAS  PubMed  Google Scholar 

  9. Haroa JM, Gonzalez-Pinto A, Novick D et al (2011) 2-year course of bipolar disorder type I patients in outpatient care: factors associated with remission and functional recovery. Eur Neuropsychopharmacol 21:287–293

    Article  CAS  Google Scholar 

  10. Bora E, Bartholomeusz C, Pantelis C (2016) Meta-analysis of Theory of mind (ToM) impairment in bipolar disorder. Psychol Med 46:253–264

    Article  CAS  PubMed  Google Scholar 

  11. Lysaker PH, Irarrázaval L, Gagen EC et al (2018) Metacognition in schizophrenia disorders: comparisons with community controls and bipolar disorder: replication with a Spanish language Chilean sample. Psychiatry Res 267:528–534

    Article  PubMed  Google Scholar 

  12. Shamay-Tsoory SG, Harari OH, Levkovitz Y (2009) Neuropsychological evidence of impaired cognitive empathy in euthymic bipolar disorder. J Neuropsychiatry Clin Neurosci 21:59–67

    Article  PubMed  Google Scholar 

  13. Derntl B, Seidel E-M, Schneider F, Habel U (2012) How specific are emotional deficits? A comparison of empathic abilities in schizophrenia, bipolar and depressed patients. Schizophr Res 142:58–64

    Article  PubMed  PubMed Central  Google Scholar 

  14. Fan Y, Duncan NW, De GM, Northoff G (2011) Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev 35:903–911

    Article  PubMed  Google Scholar 

  15. Danilo B, Leonhard S, Kai V et al (2012) Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy. Brain Struct Funct 217:783–796

    Article  Google Scholar 

  16. Baron-Cohen S, Ring HA, Wheelwright S et al (2010) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11:1891–1898

    Article  Google Scholar 

  17. Schurz M, Radua J, Aichhorn M et al (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev 42:9–34

    Article  PubMed  Google Scholar 

  18. Kim S, Kim S, Kim H et al (2017) Altered functional connectivity of the default mode network in low-empathy subjects. Yonsei Med J 58:1061–1065

    Article  PubMed  PubMed Central  Google Scholar 

  19. Takeuchi H, Taki Y, Rui N et al (2014) Association between resting-state functional connectivity and empathizing/systemizing. Neuroimage 99:312–322

    Article  PubMed  Google Scholar 

  20. Cox CL, Uddin LQ, Di MA et al (2012) The balance between feeling and knowing: affective and cognitive empathy are reflected in the brain’s intrinsic functional dynamics. Soc Cogn Affect Neurosci 7:727

    Article  PubMed  Google Scholar 

  21. Kim E, Jung Y, Ku J et al (2009) Reduced activation in the mirror neuron system during a virtual social cognition task in euthymic bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 33:1409–1416

    Article  PubMed  Google Scholar 

  22. Willert A, Mohnke S, Erk S et al (2016) Alterations in neural theory of mind processing in euthymic patients with bipolar disorder and unaffected relatives. Bipolar Disord 17:880–891

    Article  Google Scholar 

  23. Lahera G, Herrera S, Reinares M et al (2015) Hostile attributions in bipolar disorder and schizophrenia contribute to poor social functioning. Acta Psychiatr Scand 131:472–482

    Article  CAS  PubMed  Google Scholar 

  24. Si T, Liang S, Dang W et al (2009) Evaluation of the reliability and validity of Chinese version of the mini-international neuropsychiatric interview in patients with mental disorders. Chinese Ment Heal J 23:397–493

    Google Scholar 

  25. Liang Y, Yang H, Ma Y et al (2019) Validation and extension of the questionnaire of cognitive and affective empathy in the Chinese setting. PsyCh J 8:439–448

    Article  PubMed  Google Scholar 

  26. Shamay-Tsoory SG, Shur S, Barcai-Goodman L et al (2007) Dissociation of cognitive from affective components of theory of mind in schizophrenia. Psychiatry Res 149:11–23

    Article  PubMed  Google Scholar 

  27. Zhang Q, Li X, Parker GJ et al (2016) Theory of mind correlates with clinical insight but not cognitive insight in patients with schizophrenia. Psychiatry Res Neuroimaging 237:188–195

    Article  Google Scholar 

  28. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Young RC, Biggs JT, Ziegler VE, Meyer DA (1978) A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry 133:429–435

    Article  CAS  PubMed  Google Scholar 

  30. Gong YX (1992) Manual of Wechsler Adult Intelligence Scale-Chinese Version. Chinese Map, Changsha

  31. Yan CG, Di WX, Zuo XN, Zang YF (2016) DPABI: data processing and analysis for (Resting-State) brain imaging. Neuroinformatics 14:339–351

    Article  PubMed  Google Scholar 

  32. Power JD, Barnes KA, Snyder AZ et al (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154

    Article  PubMed  Google Scholar 

  33. Friston KJ, Williams S, Howard R et al (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346–355

    Article  CAS  PubMed  Google Scholar 

  34. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113

    Article  PubMed  Google Scholar 

  35. Andrewshanna JR, Reidler JS, Sepulcre J et al (2010) Functional-anatomic fractionation of the brain’s default network. Neuron 65:550–562

    Article  CAS  Google Scholar 

  36. Fusar-Poli P, Placentino A, Carletti F et al (2009) Laterality effect on emotional faces processing: ALE meta-analysis of evidence. Neurosci Lett 452:262–267

    Article  CAS  PubMed  Google Scholar 

  37. Kim S, Kim J, Kim J et al (2007) The neural mechanism of imagining facial affective expression. Brain Res 1145:128–137

    Article  CAS  PubMed  Google Scholar 

  38. Lee J, Choi S, Kang J et al (2017) Structural characteristics of the brain reward circuit regions in patients with bipolar I disorder: a voxel-based morphometric study. Psychiatry Res Neuroimaging 269:82–89

    Article  PubMed  Google Scholar 

  39. Usnich T, Spengler S, Sajonz B et al (2015) Perception of social stimuli in mania: an fMRI study. Psychiatry Res Neuroimaging 231:71–76

    Article  Google Scholar 

  40. Müller VI, Höhner Y, Eickhoff SB (2018) Influence of task instructions and stimuli on the neural network of face processing: an ALE meta-analysis. Cortex 103:240–255

    Article  PubMed  PubMed Central  Google Scholar 

  41. Van OF, Baetens K, Mariën P, Vandekerckhove M (2014) Social cognition and the cerebellum: a meta-analysis of over 350 fMRI studies. Neuroimage 86:554–572

    Article  Google Scholar 

  42. Van OF, Mariën P (2016) Functional connectivity between the cerebrum and cerebellum in social cognition: a multi-study analysis. Neuroimage 124:248–255

    Article  Google Scholar 

  43. Van OF, Van de Steen F, van Dun K, Heleven E (2020) Connectivity between the cerebrum and cerebellum during social and non-social sequencing using dynamic causal modelling. Neuroimage 206:116326

    Article  Google Scholar 

  44. Kim H (2016) Default network activation during episodic and semantic memory retrieval: a selective meta-analytic comparison. Neuropsychologia 80:35–46

    Article  PubMed  Google Scholar 

  45. Shamay-Tsoory SG, Judith AP, Daniella P (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain A J Neurol 132:617

    Article  Google Scholar 

  46. Arnone D, Cavanagh J, Gerber D et al (2009) Magnetic resonance imaging studies in bipolar disorder and schizophrenia: meta-analysis. Br J Psychiatry 195:194–201

    Article  PubMed  Google Scholar 

  47. Yucel K, McKinnon MC, Taylor VH et al (2007) Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology 195:357–367

    Article  CAS  PubMed  Google Scholar 

  48. Bodnar A, Rybakowski JK (2017) Increased affective empathy in bipolar patients during a manic episode. Rev Bras Psiquiatr 39:342–345

    Article  PubMed  PubMed Central  Google Scholar 

  49. Liang Y, Yang H, Zhang Y et al (2020) Validation of the questionnaire of cognitive and affective empathy in patients with schizophrenia, major depressive disorder and bipolar disorder. Cogn Neuropsychiatry 25:466–479

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from Beijing Municipal Science & Technology Commission Grant (Z161100000216138), Beijing Training Project for the Leading Talents in Science and Technology (Z151100000315020), Beijing Municipal Science and Technology Commission (Z171100001017086), National Natural Science Foundation of China (31871114; 31400884), and the CAS Key Laboratory of Mental Health, Institute of Psychology. These funding agents had no further role in the study design; in the collection, analysis and interpretation of the data; in the writing of the manuscript; and in the decision to submit the paper for publication.

Author information

Author notes

  1. Yun-si Liang and Shu-zhe Zhou equally contributed to this article.

Authors and Affiliations

  1. Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Chaoyang District, Beijing, 100101, China

    Yun-si Liang, Yi-jing Zhang, Xin-lu Cai, Yi Wang & Raymond C. K. Chan

  2. Sino-Danish College, University of Chinese Academy of Sciences, Beijing, China

    Yun-si Liang, Xin-lu Cai & Raymond C. K. Chan

  3. Sino-Danish Center for Education and Research, Beijing, China

    Yun-si Liang, Xin-lu Cai, Kristoffer H. Madsen & Raymond C. K. Chan

  4. Department of Psychology, University of Chinese Academy of Sciences, Beijing, China

    Yun-si Liang, Yi-jing Zhang, Xin-lu Cai, Yi Wang & Raymond C. K. Chan

  5. Peking University Sixth Hospital, 51 Huayuan Road, Haidian District, Beijing, 100191, China

    Shu-zhe Zhou, Xin Yu & Yan-tao Ma

  6. Peking University Institute of Mental Health, Beijing, China

    Shu-zhe Zhou, Xin Yu & Yan-tao Ma

  7. Key Laboratory of Mental Health, Ministry of Health, Peking University, Beijing, China

    Shu-zhe Zhou, Xin Yu & Yan-tao Ma

  8. National Clinical Research Center for Mental Disorders, Peking University Sixth Hospital, Beijing, China

    Shu-zhe Zhou, Xin Yu & Yan-tao Ma

  9. Castle Peak Hospital, Hong Kong Special Administrative Region, Hong Kong, China

    Eric F. C. Cheung & Simon S. Y. Lui

  10. Department of Psychiatry, The University of Hong Kong, Hong Kong Special Administrative Region, Hong Kong, China

    Simon S. Y. Lui

  11. Danish Research Centre for Magnetic Resonance, Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital, Amager and Hvidovre, Hvidovre, Denmark

    Kristoffer H. Madsen

  12. Department of Applied Mathematics and Computer Science, Technical University of Denmark, Kongens Lyngby, Denmark

    Kristoffer H. Madsen

Authors
  1. Yun-si Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shu-zhe Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi-jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin-lu Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eric F. C. Cheung
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Simon S. Y. Lui
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xin Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kristoffer H. Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yan-tao Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Raymond C. K. Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YL collected and analyzed the data, and wrote up the draft of the manuscript. SZ was responsible for imaging data protocol, collection and quality control, helped analyzed the data and interpreted the findings and commented the draft critically. YZ and XC collected data and implanted test, and commented on the manuscript critically. YW designed the study, contributed to imaging data analysis, quality control, interpreted the findings and commented critically on the manuscript. YM contributed to the funding sources, monitoring the clinical data quality, interpreted the findings and commented on the manuscript critically. EC, SL, KM and XY interpreted the findings and commented on the manuscript critically. RC generated the idea and designed the study, interpreted the findings and commented on the manuscript critically. All authors commented on the manuscript and agreed to the final submission.

Corresponding authors

Correspondence to Yan-tao Ma or Raymond C. K. Chan.

Ethics declarations

Conflict of interest

The authors declared that there are no conflicts of interest in relation to the subject of this study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 445 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liang, Ys., Zhou, Sz., Zhang, Yj. et al. Altered empathy-related resting-state functional connectivity in patients with bipolar disorder. Eur Arch Psychiatry Clin Neurosci 272, 839–848 (2022). https://doi.org/10.1007/s00406-021-01305-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00406-021-01305-4

Keywords

Search

Navigation