nach oben

26.03.2024 | RESEARCH

Female Cerebellum Seems Sociable; An iTBS Investigation

verfasst von: Fereshteh Kavandi Ghezeljeh, Reza Kazemi, Reza Rostami, Ahmad Zandbagleh, Sanaz Khomami, Fatemeh Rostam Vandi, Abed L. Hadipour

Erschienen in: The Cerebellum

Einloggen, um Zugang zu erhalten

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.

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.

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

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.PubMedCrossRef

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

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.CrossRef

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

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

11.

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

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentral

25.

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

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.PubMedCrossRef

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.CrossRef

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.PubMedPubMedCentralCrossRef

33.

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

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.PubMedCrossRef

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.CrossRef

36.

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

37.

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

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

43.

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

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.PubMedCrossRef

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.CrossRef

46.

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

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedPubMedCentralCrossRef

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.PubMedCrossRef

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.PubMedPubMedCentralCrossRef

60.

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

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRefPubMed

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.PubMedCrossRef

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.

Titel: Female Cerebellum Seems Sociable; An iTBS Investigation
verfasst von: Fereshteh Kavandi Ghezeljeh
Reza Kazemi
Reza Rostami
Ahmad Zandbagleh
Sanaz Khomami
Fatemeh Rostam Vandi
Abed L. Hadipour
Publikationsdatum: 26.03.2024
Verlag: Springer US
Erschienen in: The Cerebellum
Print ISSN: 1473-4222
Elektronische ISSN: 1473-4230
DOI: https://doi.org/10.1007/s12311-024-01686-x

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Vierten reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Bluttest erkennt Parkinson schon zehn Jahre vor der Diagnose

10.05.2024 Parkinson-Krankheit Nachrichten

Ein Bluttest kann abnorm aggregiertes Alpha-Synuclein bei einigen Menschen schon zehn Jahre vor Beginn der motorischen Parkinsonsymptome nachweisen. Mit einem solchen Test lassen sich möglicherweise Prodromalstadien erfassen und die Betroffenen früher behandeln.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen