Intrinsic Shapes of Empathy: Functional Brain Network Topology Encodes Intersubjective Experience and Awareness Traits.

brain networks empathy functional magnetic resonance imaging fMRI individual differences intersubjectivity

Journal

Brain sciences
ISSN: 2076-3425
Titre abrégé: Brain Sci
Pays: Switzerland
ID NLM: 101598646

Informations de publication

Date de publication:
05 Apr 2022
Historique:
received: 08 03 2022
revised: 31 03 2022
accepted: 02 04 2022
entrez: 21 4 2022
pubmed: 22 4 2022
medline: 22 4 2022
Statut: epublish

Résumé

Trait empathy is an essential personality feature in the intricacy of typical social inclinations of individuals. Empathy is likely supported by multilevel neuronal network functioning, whereas local topological properties determine network integrity. In the present functional MRI study (N = 116), we aimed to trace empathic traits to the intrinsic brain network architecture. Empathy was conceived as composed of two dimensions within the concept of pre-reflective, intersubjective understanding. Vicarious experience consists of the tendency to resonate with the feelings of other individuals, whereas intuitive understanding refers to a natural awareness of others' emotional states. Analyses of graph theoretical measures of centrality showed a relationship between the fronto-parietal network and psychometric measures of vicarious experience, whereas intuitive understanding was associated with sensorimotor and subcortical networks. Salience network regions could constitute hubs for information processing underlying both dimensions. The network properties related to empathy dimensions mainly concern inter-network information flow. Moreover, interaction effects implied several sex differences in the relationship between functional network organization and trait empathy. These results reveal that distinct intrinsic topological network features explain individual differences in separate dimensions of intersubjective understanding. The findings could help understand the impact of brain damage or stimulation through alterations of empathy-related network integrity.

Identifiants

pubmed: 35448008
pii: brainsci12040477
doi: 10.3390/brainsci12040477
pmc: PMC9024660
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Ministry of Education, Universities and Research
ID : Departments of Excellence 2018-2022 initiative

Références

Neurosci Biobehav Rev. 2017 Dec;83:132-139
pubmed: 29032087
Nat Neurosci. 2005 Jul;8(7):955-60
pubmed: 15937484
Trends Cogn Sci. 2011 Nov;15(11):512-9
pubmed: 21983148
J Hist Behav Sci. 2005 Spring;41(2):151-63
pubmed: 15812816
Nat Rev Neurosci. 2015 Jan;16(1):55-61
pubmed: 25406711
Cereb Cortex. 2019 Dec 17;29(11):4628-4645
pubmed: 30668664
Trends Cogn Sci. 2013 Dec;17(12):602-3
pubmed: 24129332
Neuroimage. 2017 Oct 15;160:73-83
pubmed: 27845257
Neuroimage. 2009 Oct 1;47(4):1408-16
pubmed: 19442749
Neurosci Biobehav Rev. 2016 Dec;71:313-322
pubmed: 27590830
Neurosci Biobehav Rev. 2012 Jan;36(1):341-9
pubmed: 21782846
Nat Rev Neurosci. 2001 Sep;2(9):661-70
pubmed: 11533734
Trends Neurosci. 2010 Jun;33(6):277-84
pubmed: 20226543
Neuron. 2002 Jul 18;35(2):395-405
pubmed: 12160756
Front Aging Neurosci. 2014 Oct 10;6:262
pubmed: 25346685
Dialogues Clin Neurosci. 2010;12(4):546-52
pubmed: 21319498
Nature. 2005 Feb 24;433(7028):895-900
pubmed: 15729348
Phys Rev E Stat Nonlin Soft Matter Phys. 2008 Mar;77(3 Pt 2):036114
pubmed: 18517468
Proc Natl Acad Sci U S A. 2011 May 3;108(18):7641-6
pubmed: 21502525
Science. 2013 Nov 1;342(6158):1238411
pubmed: 24179229
Neuroimage. 2015 Aug 15;117:305-10
pubmed: 26008886
Neuroimage. 2017 Feb 15;147:952-959
pubmed: 27729277
Dev Cogn Neurosci. 2019 Apr;36:100607
pubmed: 30579789
Brain. 2009 Mar;132(Pt 3):617-27
pubmed: 18971202
Front Integr Neurosci. 2020 Feb 14;14:3
pubmed: 32116582
Trends Cogn Sci. 2011 Oct;15(10):483-506
pubmed: 21908230
Nat Neurosci. 2004 Feb;7(2):189-95
pubmed: 14730305
J Cogn Neurosci. 2011 Jul;23(7):1808-22
pubmed: 20666597
Brain. 2010 May;133(Pt 5):1515-25
pubmed: 20371509
Nonlinear Biomed Phys. 2007 Jul 05;1(1):3
pubmed: 17908336
Sci Rep. 2017 Aug 30;7(1):9986
pubmed: 28855682
PLoS Comput Biol. 2009 Jun;5(6):e1000408
pubmed: 19521503
Proc Natl Acad Sci U S A. 2008 Aug 26;105(34):12569-74
pubmed: 18723676
Brain Res. 2010 Jan 13;1308:100-13
pubmed: 19836364
Brain Connect. 2012;2(1):25-32
pubmed: 22432927
J Neuropsychiatry Clin Neurosci. 2011 Winter;23(1):74-82
pubmed: 21304142
Cortex. 2020 Jul;128:143-161
pubmed: 32335328
Front Hum Neurosci. 2013 Sep 11;7:571
pubmed: 24062671
Nat Rev Neurosci. 2010 Jun;11(6):417-28
pubmed: 20445542
Neuropsychologia. 2006;44(6):950-8
pubmed: 16198378
Curr Opin Neurobiol. 2021 Jun;68:107-115
pubmed: 33756399
Neuroimage. 2017 Jul 1;154:128-149
pubmed: 27956209
Hum Brain Mapp. 2018 Dec;39(12):4689-4706
pubmed: 30076763
Prog Neurobiol. 2012 Jul;98(1):38-48
pubmed: 22580447
PLoS One. 2019 Apr 29;14(4):e0216164
pubmed: 31034510
Brain Stimul. 2012 Apr;5(2):95-102
pubmed: 22503509
Neuropsychologia. 2003;41(8):919-31
pubmed: 12667528
Nat Protoc. 2018 Dec;13(12):2801-2826
pubmed: 30446748
Nat Rev Neurosci. 2009 Mar;10(3):186-98
pubmed: 19190637
Trends Cogn Sci. 2007 Apr;11(4):153-7
pubmed: 17300981
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5497-502
pubmed: 12682281
Neuroimage. 2017 May 15;152:437-449
pubmed: 28167349
PLoS One. 2013 Jul 04;8(7):e68910
pubmed: 23861951
Cortex. 2013 May;49(5):1420-34
pubmed: 23036522
Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Feb;69(2 Pt 2):026113
pubmed: 14995526
Brain. 2016 Dec;139(Pt 12):3063-3083
pubmed: 27497487
J Psychopharmacol. 1997;11(2):107-14
pubmed: 9208374
Philos Trans R Soc Lond B Biol Sci. 2007 Apr 29;362(1480):659-69
pubmed: 17301027
Ann N Y Acad Sci. 2007 Dec;1121:528-45
pubmed: 17846163
Trends Cogn Sci. 2008 Jul;12(7):259-64
pubmed: 18555737
J Gerontol B Psychol Sci Soc Sci. 2013 Mar;68(2):168-75
pubmed: 22865821
Neuroimage. 2009 May 15;46(1):39-46
pubmed: 19457380
Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):36-41
pubmed: 17190818
Neuropsychologia. 2015 May;71:165-72
pubmed: 25846668
Neuroimage. 2008 Nov 15;43(3):528-39
pubmed: 18786642
Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Jul;80(1 Pt 2):016118
pubmed: 19658785
Behav Brain Sci. 2002 Feb;25(1):1-20; discussion 20-71
pubmed: 12625087
Assessment. 2016 Dec;23(6):769-777
pubmed: 26253573
Brain Cogn. 1994 Jul;25(2):161-93
pubmed: 7917240
Proc Natl Acad Sci U S A. 2018 Feb 13;115(7):E1598-E1607
pubmed: 29382744
Front Neurosci. 2017 Sep 07;11:492
pubmed: 28936159
Comput Biomed Res. 1996 Jun;29(3):162-73
pubmed: 8812068
Trends Cogn Sci. 2004 Sep;8(9):396-403
pubmed: 15350240
Neuroimage. 2014 Jan 1;84:320-41
pubmed: 23994314
Neuroimage. 2013 Apr 1;69:51-61
pubmed: 23220493
J Cogn Neurosci. 2012 Jun;24(6):1275-85
pubmed: 22401285
Neuropsychologia. 2021 Jun 18;156:107832
pubmed: 33753085
Neuroimage. 2010 Sep;52(3):1059-69
pubmed: 19819337
Dialogues Clin Neurosci. 2018 Jun;20(2):133-140
pubmed: 30250390
Neurosci Biobehav Rev. 2014 Oct;46 Pt 4:604-27
pubmed: 25236781
Neuroscientist. 2011 Feb;17(1):18-24
pubmed: 21071616
Philos Trans R Soc Lond B Biol Sci. 2014 Apr 28;369(1644):20130177
pubmed: 24778374
Neuroimage. 2011 Aug 1;57(3):1221-33
pubmed: 21609772
J Cogn Neurosci. 2012 Jan;24(1):106-18
pubmed: 21812568
Neuropsychopharmacology. 2011 Oct;36(11):2200-10
pubmed: 21734650
Brain. 2017 Apr 1;140(4):1086-1099
pubmed: 28334943
Psychopathology. 2003 Jul-Aug;36(4):171-80
pubmed: 14504450
Behav Cogn Neurosci Rev. 2004 Jun;3(2):71-100
pubmed: 15537986
Brain. 2014 Apr;137(Pt 4):981-97
pubmed: 24293265
Soc Cogn Affect Neurosci. 2020 May 11;15(2):225-233
pubmed: 32128580
Ann N Y Acad Sci. 2009 Mar;1156:81-96
pubmed: 19338504
J Neurosci Methods. 2015 Oct 30;254:46-59
pubmed: 26213217
Curr Top Behav Neurosci. 2017;30:193-206
pubmed: 26602249
Neuroimage. 2018 Oct 15;180(Pt B):370-382
pubmed: 28974453
Neuropsychologia. 2018 Aug;117:428-439
pubmed: 30033396
J Cogn Neurosci. 2020 Sep;32(9):1764-1779
pubmed: 32530380
Neuropsychologia. 2016 Feb;82:142-148
pubmed: 26801227
Neuroimage. 2011 Feb 1;54(3):2492-502
pubmed: 20946964
PLoS Comput Biol. 2007 Feb 2;3(2):e17
pubmed: 17274684
Brain Struct Funct. 2010 Jun;214(5-6):655-67
pubmed: 20512370
Soc Cogn Affect Neurosci. 2012 Aug;7(6):727-37
pubmed: 21896497
Sci Rep. 2019 Feb 22;9(1):2603
pubmed: 30796260
Soc Cogn Affect Neurosci. 2022 May 5;17(5):437-446
pubmed: 34746947
Neuroimage. 2008 Aug 1;42(1):393-403
pubmed: 18514546
Hum Brain Mapp. 2021 Oct 1;42(14):4777-4804
pubmed: 34322943
Neuropsychologia. 2021 Oct 15;161:107991
pubmed: 34391808
Neurosci Biobehav Rev. 2011 Jan;35(3):903-11
pubmed: 20974173
Nat Neurosci. 2012 Apr 15;15(5):675-80
pubmed: 22504346
Annu Rev Neurosci. 2012;35:1-23
pubmed: 22715878
Neuroimage. 2016 Apr 15;130:230-240
pubmed: 26899786
Neuroimage. 2012 Sep;62(3):2034-9
pubmed: 22683384
Trends Cogn Sci. 2013 Dec;17(12):683-96
pubmed: 24231140
Curr Opin Neurobiol. 2009 Dec;19(6):666-71
pubmed: 19880311
Neurosci Biobehav Rev. 2020 Aug;115:77-95
pubmed: 32492474
Mol Psychiatry. 2014 Sep;19(9):966-977
pubmed: 25048001
Dev Cogn Neurosci. 2013 Jan;3:22-32
pubmed: 23245217
Sci Rep. 2012;2:336
pubmed: 22468223
Brain Sci. 2021 Oct 02;11(10):
pubmed: 34679377
Eur J Neurosci. 2022 Mar;55(6):1519-1531
pubmed: 35266192
PLoS One. 2011;6(7):e21570
pubmed: 21829437
Nat Rev Neurosci. 2002 Aug;3(8):655-66
pubmed: 12154366
Child Dev. 1987 Aug;58(4):992-1000
pubmed: 3608668
J Cogn Neurosci. 2003 Apr 1;15(3):324-37
pubmed: 12729486
J Neurosci. 2007 Aug 1;27(31):8161-5
pubmed: 17670959
Phys Rev E Stat Nonlin Soft Matter Phys. 2009 Mar;79(3 Pt 2):036116
pubmed: 19392027
Nat Rev Neurosci. 2010 Apr;11(4):264-74
pubmed: 20216547

Auteurs

Sjoerd J H Ebisch (SJH)

Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.
Institute of Advanced Biomedical Technologies (ITAB), G. d'Annunzio University of Chieti-Pescara, Via Luigi Polacchi 11, 66100 Chieti, Italy.

Andrea Scalabrini (A)

Department of Psychological, Health and Territorial Sciences (DiSPuTer), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Georg Northoff (G)

The Royal's Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1N 6N5, Canada.
Brain and Mind Research Institute, Centre for Neural Dynamics, Faculty of Medicine, University of Ottawa, Ottawa, ON K1N 6N5, Canada.
Mental Health Centre, Zhejiang University School of Medicine, Hangzhou 310030, China.
Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310030, China.
TMU Research Centre for Brain and Consciousness, Shuang Hospital, Taipei Medical University, Taipei 110, Taiwan.
Graduate Institute of Humanities in Medicine, Taipei Medical University, Taipei 110, Taiwan.

Clara Mucci (C)

Department of Human and Social Sciences, University of Bergamo, 24129 Bergamo, Italy.

Maria Rita Sergi (MR)

Department of Medicine and Aging Sciences, G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Aristide Saggino (A)

Department of Medicine and Aging Sciences, G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Antonio Aquino (A)

Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Francesca R Alparone (FR)

Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Mauro Gianni Perrucci (MG)

Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.
Institute of Advanced Biomedical Technologies (ITAB), G. d'Annunzio University of Chieti-Pescara, Via Luigi Polacchi 11, 66100 Chieti, Italy.

Vittorio Gallese (V)

Unit of Neuroscience, Department of Medicine and Surgery, University of Parma, 43121 Parma, Italy.

Simone Di Plinio (S)

Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d'Annunzio University of Chieti-Pescara, 66100 Chieti, Italy.

Classifications MeSH