Skip to main content
SpringerLink
Log in

Female Cerebellum Seems Sociable; An iTBS Investigation

  • RESEARCH
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

The cerebellum has been shown to be engaged in tasks other than motor control, including cognitive and affective functions. Prior neuroimaging studies have documented the role of this area in social cognition and despite these findings, no studies have yet examined the causal relationship between the cerebellum and social cognition. This study aimed to investigate the role of the cerebellum in empathy and theory of mind (ToM) in a randomized, placebo-controlled, double-blind, parallel study. 32 healthy participants were assigned to either a sham or active group. For the active group, an intermittent theta-burst stimulation (iTBS) protocol at 100% of the motor threshold was applied to the cerebellum, while the control group received sham stimulation. An eyes-closed EEG session, the Empathy Quotient (EQ) test, and the Reading the Mind in the Eyes Test (RMET) were administered before and after the iTBS session. The results demonstrated differences in cognitive empathy, ToM, and a decrease in the activity of the default mode network (DMN) between the active and sham groups in females. Females also showed a decrease in the activity of the affective empathy network and connectivity in the DMN. We conclude that cognitive empathy and ToM are associated with cerebellar activity, and due to sex-related differences in the cortical organization of this area which is modulated by sex hormones, the stimulation of the cerebellum in males and females yields different results.

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

Similar content being viewed by others

Data Availability

All data are included in the manuscript. However, the datasets used and/ or analyzed in the current study are available from the corresponding author on reasonable request.

References

  1. Adamaszek M, D’Agata F, Ferrucci R, Habas C, Keulen S, Kirkby K, … Moulton E. Consensus paper: cerebellum and emotion. Cerebellum. 2017;16:552–576.

  2. Schmahmann JD. The cerebellum and cognition. Neurosci Lett. 2019;688:62–75.

    Article  CAS  PubMed  Google Scholar 

  3. Mannarelli D, Pauletti C, Currà A, Marinelli L, Corrado A, DelleChiaie R, Fattapposta F. The cerebellum modulates attention network functioning: evidence from a cerebellar transcranial direct current stimulation and attention network test study. The Cerebellum. 2019;18:457–68.

    Article  PubMed  Google Scholar 

  4. Stein H. Why does the neocortex need the cerebellum for working memory? J Neurosci. 2021;41(30):6368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Blackwood N, Ffytche D, Simmons A, Bentall R, Murray R, Howard R. The cerebellum and decision making under uncertainty. Cogn Brain Res. 2004;20(1):46–53. https://doi.org/10.1016/j.cogbrainres.2003.12.009.

    Article  Google Scholar 

  6. Sokolov AA. The cerebellum in social cognition. Front Cell Neurosci. 2018;12:145.

    Article  Google Scholar 

  7. Calarge C, Andreasen NC, O’Leary DS. Visualizing how one brain understands another: a PET study of theory of mind. Am J Psychiatry. 2003;160(11):1954–64.

    Article  PubMed  Google Scholar 

  8. Picerni E, Laricchiuta D, Piras F, Vecchio D, Petrosini L, Cutuli D, Spalletta G. Macro-and micro-structural cerebellar and cortical characteristics of cognitive empathy towards fictional characters in healthy individuals. Sci Rep. 2021;11(1):8804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Beuriat P-A, Cohen-Zimerman S, Smith GN, Krueger F, Gordon B, Grafman J. Evidence of the role of the cerebellum in cognitive theory of mind using voxel-based lesion mapping. Sci Rep. 2022;12(1):4999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Clausi S, Olivito G, Siciliano L, Lupo M, Laghi F, Baiocco R, Leggio M. The cerebellum is linked to theory of mind alterations in autism. A direct clinical and MRI comparison between individuals with autism and cerebellar neurodegenerative pathologies. Autism Res. 2021;14(11):2300–13.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Marsh AA. The neuroscience of empathy. Curr Opin Behav Sci. 2018;19:110–5.

    Article  Google Scholar 

  12. Balconi M, Bortolotti A. Detection of the facial expression of emotion and self-report measures in empathic situations are influenced by sensorimotor circuit inhibition by low-frequency rTMS. Brain Stimul. 2012;5(3):330–6.

    Article  PubMed  Google Scholar 

  13. Balconi M, Bortolotti A, Gonzaga L. Emotional face recognition, EMG response, and medial prefrontal activity in empathic behaviour. Neurosci Res. 2011;71(3):251–9.

    Article  PubMed  Google Scholar 

  14. Balconi M, Canavesio Y. Empathy, approach attitude, and rTMs on left DLPFC affect emotional face recognition and facial feedback (EMG). J Psychophysiol. 2015.

  15. Costa A, Torriero S, Oliveri M, Caltagirone C. Prefrontal and temporo-parietal involvement in taking others’ perspective: TMS evidence. Behav Neurol. 2008;19(1–2):71–4.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Giardina A, Caltagirone C, Oliveri M. Temporo-parietal junction is involved in attribution of hostile intentionality in social interactions: an rTMS study. Neurosci Lett. 2011;495(2):150–4.

    Article  CAS  PubMed  Google Scholar 

  17. Krall SC, Volz LJ, Oberwelland E, Grefkes C, Fink GR, Konrad K. The right temporoparietal junction in attention and social interaction: A transcranial magnetic stimulation study. Hum Brain Mapp. 2016;37(2):796–807.

    Article  PubMed  Google Scholar 

  18. Balconi M, Crivelli D, Bortolotti A. Detection of facial expression of emotion and self-report measures in empathic situations are influenced by ACC inhibition. rTMS evidences. Neuropsychol Trends.2010;(8):18–18.

  19. Hoekert M, Vingerhoets G, Aleman A. Results of a pilot study on the involvement of bilateral inferior frontal gyri in emotional prosody perception: an rTMS study. BMC Neurosci. 2010;11(1):1–8.

    Article  Google Scholar 

  20. Keuken MC, Hardie A, Dorn B, Dev S, Paulus M, Jonas K, … Pineda J. The role of the left inferior frontal gyrus in social perception: an rTMS study. Brain Res. 2011;1383:196–205.

  21. Pobric G, Hamilton AFdC. Action understanding requires the left inferior frontal cortex. Curr Biol. 2006;16(5):524–9.

    Article  CAS  PubMed  Google Scholar 

  22. Silani G, Lamm C, Ruff CC, Singer T. Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments. J Neurosci. 2013;33(39):15466–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ferrucci R, Giannicola G, Rosa M, Fumagalli M, Boggio PS, Hallett M, … Priori A. Cerebellum and processing of negative facial emotions: cerebellar transcranial DC stimulation specifically enhances the emotional recognition of facial anger and sadness. Cogn Emot. 2012; 26(5):786–799.

  24. Schutter DJ, Enter D, Hoppenbrouwers SS. High-frequency repetitive transcranial magnetic stimulation to the cerebellum and implicit processing of happy facial expressions. J Psychiatry Neurosci. 2009;34(1):60–5.

    PubMed  PubMed Central  Google Scholar 

  25. Schutter DJ, van Honk J. The cerebellum in emotion regulation: a repetitive transcranial magnetic stimulation study. The Cerebellum. 2009;8:28–34.

    Article  PubMed  Google Scholar 

  26. Van Overwalle F, Van de Steen F, Mariën P. Dynamic causal modeling of the effective connectivity between the cerebrum and cerebellum in social mentalizing across five studies. Cogn Affect Behav Neurosci. 2019;19:211–23.

    Article  PubMed  Google Scholar 

  27. Guo W, Liu F, Liu J, Yu M, Zhang Z, Liu G, Xiao C, Zhao J. Increased cerebellar-default-mode-network connectivity in drug-naive major depressive disorder at rest. Medicine (Baltimore). 2015;94(9):e560.

  28. Guo W, Liu F, Zhang Z, Liu G, Liu J, Yu L, … Zhao J. Increased cerebellar functional connectivity with the default-mode network in unaffected siblings of schizophrenia patients at rest. Schizophrenia Bull. 2015;41(6):1317–1325.

  29. Lv D, Ou Y, Chen Y, Yang R, Zhong Z, Jia C, … Sun Z. Increased cerebellar–default-mode network connectivity at rest in obsessive–compulsive disorder. Eur Arch Psychiatry Clin Neurosci. 2020;270:1015–1024.

  30. Chen G, Zhao L, Jia Y, Zhong S, Chen F, Luo X, … Huang L. Abnormal cerebellum-DMN regions connectivity in unmedicated bipolar II disorder. J Affect Disord. 2019;243:441–447.

  31. Grami F, De Marco G, Bodranghien F, Manto M, Habas C. Cerebellar transcranial direct current stimulation reconfigurates static and dynamic functional connectivity of the resting-state networks. Cerebellum Ataxias. 2021;8(1):1–12.

    Article  Google Scholar 

  32. Christov-Moore L, Simpson EA, Coudé G, Grigaityte K, Iacoboni M, Ferrari PF. Empathy: gender effects in brain and behavior. Neurosci Biobehav Rev. 2014;46:604–27.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Han S, Fan Y, Mao L. Gender difference in empathy for pain: an electrophysiological investigation. Brain Res. 2008;1196:85–93.

    Article  CAS  PubMed  Google Scholar 

  34. Jie J, Luo P, Zhuang M, Fan M, Wang Y, Yang Y, Zheng X. Gender differences in empathic responses to others’ economic payoffs: an event-related potentials study. Exp Brain Res. 2019;237:1347–59.

    Article  PubMed  Google Scholar 

  35. Pang C, Li W, Zhou Y, Gao T, Han S. Are women more empathetic than men? Questionnaire and EEG estimations of sex/gender differences in empathic ability. Soc Cogn Affect Neurosci. 2023;18(1):008.

    Article  Google Scholar 

  36. Proverbio AM, Zani A, Adorni R. Neural markers of a greater female responsiveness to social stimuli. BMC Neurosci. 2008;9(1):1–10.

    Article  Google Scholar 

  37. Rueckert L, Naybar N. Gender differences in empathy: The role of the right hemisphere. Brain Cogn. 2008;67(2):162–7.

    Article  PubMed  Google Scholar 

  38. Yang C-Y, Decety J, Lee S, Chen C, Cheng Y. Gender differences in the mu rhythm during empathy for pain: an electroencephalographic study. Brain Res. 2009;1251:176–84.

    Article  CAS  PubMed  Google Scholar 

  39. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatr Allied Discip. 2001;42(2):241–51.

    Article  CAS  Google Scholar 

  40. Baron-Cohen S, Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord. 2004;34:163–75.

    Article  PubMed  Google Scholar 

  41. Rojas GM, Alvarez C, Montoya CE, De la Iglesia-Vaya M, Cisternas JE, Gálvez M. Study of resting-state functional connectivity networks using EEG electrodes position as seed. Front Neurosci. 2018;12:235.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Zandbagleh A, Mirzakuchaki S, Daliri MR, Premkumar P, Sanei S. Classification of low and high schizotypy levels via evaluation of brain connectivity. Int J Neural Syst. 2022;32(04):2250013.

    Article  PubMed  Google Scholar 

  43. Aydore S, Pantazis D, Leahy RM. A note on the phase locking value and its properties. Neuroimage. 2013;74:231–44.

    Article  PubMed  Google Scholar 

  44. Varastegan S, Kazemi R, Rostami R, Khomami S, Zandbagleh A, Hadipour AL. Remember NIBS? tACS improves memory performance in elders with subjective memory complaints. GeroScience. 2023;45(2):851–69.

    Article  PubMed  Google Scholar 

  45. Theiler J, Eubank S, Longtin A, Galdrikian B, Farmer JD. Testing for nonlinearity in time series: the method of surrogate data. Physica D. 1992;58(1–4):77–94.

    Article  Google Scholar 

  46. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 2010;52(3):1059–69.

    Article  PubMed  Google Scholar 

  47. Mulert C, Jäger L, Schmitt R, Bussfeld P, Pogarell O, Möller H-J, … Hegerl U. Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage. 2004; 22(1):83–94.

  48. Vitacco D, Brandeis D, Pascual-Marqui R, Martin E. Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Hum Brain Mapp. 2002;17(1):4–12.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Worrell GA, Lagerlund TD, Sharbrough FW, Brinkmann BH, Busacker NE, Cicora KM, O’Brien TJ. Localization of the epileptic focus by low-resolution electromagnetic tomography in patients with a lesion demonstrated by MRI. Brain Topogr. 2000;12:273–82.

    Article  CAS  PubMed  Google Scholar 

  50. Dierks T, Jelic V, Pascual-Marqui RD, Wahlund L-O, Julin P, Linden DE, … Nordberg A. Spatial pattern of cerebral glucose metabolism (PET) correlates with localization of intracerebral EEG-generators in Alzheimer's disease. Clin Neurophysiol. 2000; 111(10):1817–1824.

  51. Fan Y, Duncan NW, De Greck M, Northoff G. Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev. 2011;35(3):903–11.

    Article  PubMed  Google Scholar 

  52. Kogler L, Müller VI, Werminghausen E, Eickhoff SB, Derntl B. Do I feel or do I know? Neuroimaging meta-analyses on the multiple facets of empathy. Cortex. 2020;129:341–55.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kazemi R, Rostami R, Dehghan S, Nasiri Z, Lotfollahzadeh S, Hadipour AL, … Ikeda S. Alpha frequency rTMS modulates theta lagged nonlinear connectivity in dorsal attention network. Brain Res Bull. 2020;162:271–281.

  54. Kazemi R, Rostami R, Nasiri Z, Hadipour AL, Kiaee N, Coetzee JP, … Adamson MM. Electrophysiological and behavioral effects of unilateral and bilateral rTMS; A randomized clinical trial on rumination and depression. Journal of affective disorders. 2022;317:360–372.

  55. Pascual-Marqui RD, Lehmann D, Koukkou M, Kochi K, Anderer P, Saletu B, … Prichep L. Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos Trans Royal Soc A: Math, Phys Eng Sci. 2011;369(1952):3768–3784.

  56. Canuet L, Ishii R, Pascual-Marqui RD, Iwase M, Kurimoto R, Aoki Y, … Takeda M. Resting-state EEG source localization and functional connectivity in schizophrenia-like psychosis of epilepsy. PloS one. 2011; 6(11):e27863.

  57. Zhang X, Liang M, Qin W, Wan B, Yu C, Ming D. Gender differences are encoded differently in the structure and function of the human brain revealed by multimodal MRI. Front Hum Neurosci. 2020;14:244.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Steele CJ, Chakravarty MM. Gray-matter structural variability in the human cerebellum: lobule-specific differences across sex and hemisphere. Neuroimage. 2018;170:164–73.

    Article  PubMed  Google Scholar 

  59. Fitzgerald M, Pritschet L, Santander T, Grafton ST, Jacobs EG. Cerebellar network organization across the human menstrual cycle. Sci Rep. 2020;10(1):20732.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Hedges VL, Ebner TJ, Meisel RL, Mermelstein PG. The cerebellum as a target for estrogen action. Front Neuroendocrinol. 2012;33(4):403–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. İrem A, Semra İ. Analysis of gender differences with functional connectivity and default mode network and fronto-parietal network. Avrupa Bilim ve Teknoloji Dergisi, pp 298–303.

  62. Rochat MJ. Sex and gender differences in the development of empathy. J Neurosci Res. 2023;101(5):718–29.

    Article  CAS  PubMed  Google Scholar 

  63. Groen Y, Wijers A, Tucha O, Althaus M. Are there sex differences in ERPs related to processing empathy-evoking pictures? Neuropsychologia. 2013;51(1):142–55.

    Article  CAS  PubMed  Google Scholar 

  64. Zupan B, Neumann D, Babbage D, Willer B. Sex-based differences in affective and cognitive empathy following severe traumatic brain injury. Neuropsychology. 2018;32(5):554–63. https://doi.org/10.1037/neu0000462.

    Article  PubMed  Google Scholar 

  65. Bluhm RL, Osuch EA, Lanius RA, Boksman K, Neufeld RW, Théberge J, Williamson P. Default mode network connectivity: effects of age, sex, and analytic approach. NeuroReport. 2008;19(8):887–91.

    Article  PubMed  Google Scholar 

  66. Dong H-h, Guo, M-x, Zhang Y-t, Fu Y, Shi H-l. Sex differences in brain gray and white matter in healthy young adults: correlations with resting state ALFF. Paper presented at the 2010 3rd International Conference on Biomedical Engineering and Informatics. 2010.

  67. Ficek-Tani B, Horien C, Ju S, Xu W, Li N, Lacadie C, … Fredericks C. Sex differences in default mode network connectivity in healthy aging adults. Cerebral Cortex. 2023;33(10):6139–6151

  68. Shanmugan S, Seidlitz J, Cui Z, Adebimpe A, Bassett DS, Bertolero MA, … Gur RC. Sex differences in the functional topography of association networks in youth. Proc Natl Acad Sci. 2022;119(33):e2110416119.

  69. Xu C, Li C, Wu H, Wu Y, Hu S, Zhu Y, … Liu J. Gender differences in cerebral regional homogeneity of adult healthy volunteers: a resting-state FMRI study. BioMed Res Int. 2015;2015.

Download references

Acknowledgements

None.

Author information

Authors and Affiliations

  1. Department of Psychology, University of South Carolina, Columbia, SC, USA

    Fereshteh Kavandi Ghezeljeh

  2. Faculty of Entrepreneurship, University of Tehran, Farshi Moghadam (16 St.), North Kargar Ave., Tehran, Iran

    Reza Kazemi

  3. Department of Psychology, University of Tehran, Tehran, Iran

    Reza Rostami & Fatemeh Rostam Vandi

  4. School of Electrical Engineering, Iran University of Science and Technology, Tehran, Iran

    Ahmad Zandbagleh

  5. Department of Psychology, West Tehran Branch, Islamic Azad University, Tehran, Iran

    Sanaz Khomami

  6. Department of Cognitive Sciences, University of Messina, Messina, Italy

    Abed L. Hadipour

Authors
  1. Fereshteh Kavandi Ghezeljeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reza Kazemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Reza Rostami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ahmad Zandbagleh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sanaz Khomami
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fatemeh Rostam Vandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abed L. Hadipour
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RK, RR and FK: designed the study; FK and RR: carried out the study; ALH, SKH, and AZ: analyzed the behavioral and EEG data; RK, RR, ALH, AZ and FK: interpreted the results and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Reza Kazemi.

Ethics declarations

Ethical Approval and Consent to Participate

The protocol of research was approved by the Ethical committee of the University of Tehran. All participants gave their written informed consent to participate in the research.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghezeljeh, F.K., Kazemi, R., Rostami, R. et al. Female Cerebellum Seems Sociable; An iTBS Investigation. Cerebellum (2024). https://doi.org/10.1007/s12311-024-01686-x

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12311-024-01686-x

Keywords

Search

Navigation