Brain-to-brain mechanisms underlying pain empathy and social modulation of pain in the patient-clinician interaction.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
27 06 2023
Historique:
pmc-release: 20 12 2023
medline: 22 6 2023
pubmed: 20 6 2023
entrez: 20 6 2023
Statut: ppublish

Résumé

Social interactions such as the patient-clinician encounter can influence pain, but the underlying dynamic interbrain processes are unclear. Here, we investigated the dynamic brain processes supporting social modulation of pain by assessing simultaneous brain activity (fMRI hyperscanning) from chronic pain patients and clinicians during video-based live interaction. Patients received painful and nonpainful pressure stimuli either with a supportive clinician present (Dyadic) or in isolation (Solo). In half of the dyads, clinicians performed a clinical consultation and intake with the patient prior to hyperscanning (Clinical Interaction), which increased self-reported therapeutic alliance. For the other half, patient-clinician hyperscanning was completed without prior clinical interaction (No Interaction). Patients reported lower pain intensity in the Dyadic, relative to the Solo, condition. In Clinical Interaction dyads relative to No Interaction, patients evaluated their clinicians as better able to understand their pain, and clinicians were more accurate when estimating patients' pain levels. In Clinical Interaction dyads, compared to No Interaction, patients showed stronger activation of the dorsolateral and ventrolateral prefrontal cortex (dlPFC and vlPFC) and primary (S1) and secondary (S2) somatosensory areas (Dyadic-Solo contrast), and clinicians showed increased dynamic dlPFC concordance with patients' S2 activity during pain. Furthermore, the strength of S2-dlPFC concordance was positively correlated with self-reported therapeutic alliance. These findings support that empathy and supportive care can reduce pain intensity and shed light on the brain processes underpinning social modulation of pain in patient-clinician interactions. Our findings further suggest that clinicians' dlPFC concordance with patients' somatosensory processing during pain can be boosted by increasing therapeutic alliance.

Identifiants

pubmed: 37339198
doi: 10.1073/pnas.2212910120
pmc: PMC10293846
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2212910120

Subventions

Organisme : NCCIH NIH HHS
ID : R61 AT009306
Pays : United States
Organisme : NCRR NIH HHS
ID : P41 RR014075
Pays : United States
Organisme : NCRR NIH HHS
ID : UL1 RR025758
Pays : United States
Organisme : NCCIH NIH HHS
ID : R33 AT009306
Pays : United States
Organisme : NIDA NIH HHS
ID : R90 DA023427
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR019254
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR023043
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR023401
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR019307
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR019254
Pays : United States

Références

Front Psychiatry. 2019 Jul 04;10:475
pubmed: 31333518
Otolaryngol Head Neck Surg. 2011 Jan;144(1):120-2
pubmed: 21493400
Soc Neurosci. 2019 Feb;14(1):1-9
pubmed: 29091537
Psychosom Med. 2003 Mar-Apr;65(2):276-83
pubmed: 12651995
Phys Ther. 2014 Apr;94(4):477-89
pubmed: 24309616
Phys Med Rehabil Clin N Am. 2006 May;17(2):287-302
pubmed: 16616268
Proc Natl Acad Sci U S A. 2018 Mar 13;115(11):E2528-E2537
pubmed: 29483250
Neuroimage. 2011 Sep 15;58(2):665-74
pubmed: 21718792
Cereb Cortex. 2007 Sep;17(9):2214-22
pubmed: 17124286
Nat Neurosci. 2020 Jun;23(6):754-760
pubmed: 32341541
Pain. 2010 Mar;148(3):368-374
pubmed: 19875233
Cortex. 2010 Jun;46(6):769-80
pubmed: 19709653
Nat Rev Neurosci. 2019 Aug;20(8):495-505
pubmed: 31138910
Proc Natl Acad Sci U S A. 2018 Aug 21;115(34):8569-8574
pubmed: 30082406
Ann Behav Med. 2015 Aug;49(4):557-69
pubmed: 25623896
J Pain. 2017 Jul;18(7):787-799
pubmed: 28479279
Front Psychiatry. 2019 Mar 14;10:126
pubmed: 30930803
Cogn Behav Neurol. 2005 Mar;18(1):55-67
pubmed: 15761277
J Pain. 2020 Nov - Dec;21(11-12):1160-1174
pubmed: 32544602
Health Psychol. 1989;8(2):221-38
pubmed: 2786808
Psychosom Med. 1995 Jan-Feb;57(1):23-31
pubmed: 7732155
Proc Natl Acad Sci U S A. 2023 Jun 27;120(26):e2212910120
pubmed: 37339198
Arthritis Rheum. 2004 Dec;50(12):4035-44
pubmed: 15593181
Nat Commun. 2018 Sep 12;9(1):3397
pubmed: 30209286
JAMA. 2014 Apr 16;311(15):1547-55
pubmed: 24737367
Sci Rep. 2019 Jun 10;9(1):8398
pubmed: 31182760
Cereb Cortex. 2019 Jul 22;29(8):3457-3470
pubmed: 30192902
Ann N Y Acad Sci. 2016 Apr;1369(1):218-39
pubmed: 27206250
Neuroimage. 2012 Jan 16;59(2):1369-81
pubmed: 21875671
Neuroimage. 2012 Jul 16;61(4):1277-86
pubmed: 22484411
Sci Adv. 2020 Oct 21;6(43):
pubmed: 33087365
Somatosens Mot Res. 1992;9(4):265-77
pubmed: 1492527
eNeuro. 2022 Apr 13;9(2):
pubmed: 35365502
Cochrane Database Syst Rev. 2013 May 31;(5):CD007070
pubmed: 23728665
J Neurosci. 2017 Oct 4;37(40):9715-9723
pubmed: 28883019
PLoS One. 2014 Apr 09;9(4):e94207
pubmed: 24718585
Med Image Anal. 2001 Jun;5(2):143-56
pubmed: 11516708
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
Psychosom Med. 2009 Sep;71(7):789-97
pubmed: 19661195
Neuroimage. 2004 Apr;21(4):1732-47
pubmed: 15050594
Health Psychol. 1994 Sep;13(5):384-92
pubmed: 7805632
Neuroimage. 2003 Oct;20(2):870-88
pubmed: 14568458
Neuropsychologia. 2007 Oct 1;45(13):3054-67
pubmed: 17640690
Psychol Sci. 2006 Dec;17(12):1032-9
pubmed: 17201784
Neuroimage. 2012 Feb 1;59(3):2430-7
pubmed: 21933717
J R Soc Med. 2018 Jul;111(7):240-252
pubmed: 29672201
Scand J Pain. 2019 Dec 18;20(1):205-209
pubmed: 31433786
J Pain Symptom Manage. 2002 Nov;24(5):526-42
pubmed: 12547052
Cereb Cortex. 2019 Apr 1;29(4):1572-1583
pubmed: 29931116
Sci Adv. 2021 Mar 31;7(14):
pubmed: 33789899
Women Health. 2008;48(2):123-44
pubmed: 19042213
J Pain. 2005 Apr;6(4):228-36
pubmed: 15820910
Arthritis Rheumatol. 2014 Jan;66(1):203-12
pubmed: 24449585
Mol Psychiatry. 2014 Mar;19(3):392-8
pubmed: 23358155
Behav Brain Sci. 2013 Aug;36(4):393-414
pubmed: 23883742
Eur Neurol. 1998;39(4):193-9
pubmed: 9635468
Psychon Bull Rev. 2018 Dec;25(6):2119-2140
pubmed: 29619648
Cortex. 2013 Sep;49(8):2201-9
pubmed: 23290634
Neuroimage. 2001 Dec;14(6):1370-86
pubmed: 11707093
Soc Cogn Affect Neurosci. 2017 Oct 1;12(10):1574-1583
pubmed: 28985422
BMJ. 2008 May 3;336(7651):999-1003
pubmed: 18390493
PLoS One. 2019 Feb 27;14(2):e0211890
pubmed: 30811457
Patient Educ Couns. 2013 Feb;90(2):220-5
pubmed: 23177399
Neuroimage. 2004;23 Suppl 1:S208-19
pubmed: 15501092
J Behav Med. 1999 Feb;22(1):75-91
pubmed: 10196730
Transl Psychiatry. 2022 Jan 28;12(1):44
pubmed: 35091536
Neuroimage. 2002 Oct;17(2):825-41
pubmed: 12377157
Clin J Pain. 2008 Oct;24(8):669-77
pubmed: 18806531
Cereb Cortex. 2012 Jul;22(7):1593-603
pubmed: 21893681
Pain. 2019 Sep;160(9):2072-2085
pubmed: 31241496
Behav Neurol. 2008;19(1-2):71-4
pubmed: 18413921
Soc Cogn Affect Neurosci. 2009 Jun;4(2):208-13
pubmed: 19470529
Annu Rev Neurosci. 2001;24:167-202
pubmed: 11283309
Soc Cogn Affect Neurosci. 2020 Sep 24;15(7):709-723
pubmed: 32608498
Neuroimage. 2009 Oct 15;48(1):63-72
pubmed: 19573611
Neuropsychologia. 2020 Aug;145:106427
pubmed: 28712948
J Pain Symptom Manage. 2016 Jan;51(1):1-8
pubmed: 26297851
Neurosci Biobehav Rev. 2018 Sep;92:437-452
pubmed: 30006033
Behav Brain Sci. 2013 Aug;36(4):435
pubmed: 23883764
N Engl J Med. 2013 Apr 11;368(15):1388-97
pubmed: 23574118
Ann Med. 2011 Nov;43(7):495-502
pubmed: 21770697
Fam Pract. 2004 Dec;21(6):699-705
pubmed: 15528286
Am J Chin Med. 2018 Oct 9;:1-33
pubmed: 30298749
Neuropsychologia. 2019 Feb 18;124:19-30
pubmed: 30633875
Neuroimage. 2011 Feb 1;54(3):2492-502
pubmed: 20946964
Philos Trans R Soc Lond B Biol Sci. 2016 May 5;371(1693):
pubmed: 27069044
Neuroimage. 2008 Apr 1;40(2):955-962
pubmed: 18234518
Arthritis Rheumatol. 2015 May;67(5):1395-1405
pubmed: 25622796
BMJ. 2020 Jul 20;370:m1668
pubmed: 32690477
J Neurosci Res. 2017 Jan 2;95(1-2):604-616
pubmed: 27870423
Soc Cogn Affect Neurosci. 2019 Mar 5;14(3):253-261
pubmed: 30753646
Soc Cogn Affect Neurosci. 2015 Aug;10(8):1030-7
pubmed: 25556212
Nat Rev Neurosci. 2015 Jul;16(7):403-18
pubmed: 26087681
Soc Cogn Affect Neurosci. 2018 Sep 5;13(8):841-849
pubmed: 30060130
Trends Neurosci. 2017 Jan;40(1):15-27
pubmed: 27986294
Proc Natl Acad Sci U S A. 2013 Oct 29;110(44):17993-8
pubmed: 24127578
Soc Sci Med. 2018 Jan;196:47-55
pubmed: 29127852

Auteurs

Dan-Mikael Ellingsen (DM)

Department of Physics and Computational Radiology, Division of Radiology and Nuclear Medicine, Oslo University Hospital, Oslo 0372, Norway.
Department of Psychology, Pedagogy and Law, School of Health Sciences, Kristiania University College, Oslo 0107, Norway.
Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.

Kylie Isenburg (K)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.

Changjin Jung (C)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
KM Research Science Division, Korea Institute of Oriental Medicine, Daejeon 461-24, Republic of Korea.

Jeungchan Lee (J)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, MA 02129.

Jessica Gerber (J)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.

Ishtiaq Mawla (I)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.

Roberta Sclocco (R)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Radiology, Logan University, Chesterfield, MO 63017.

Arvina Grahl (A)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, MA 02129.

Alessandra Anzolin (A)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, MA 02129.

Robert R Edwards (RR)

Department of Anesthesiology, Brigham and Women's Hospital, Boston, MA 02115.

John M Kelley (JM)

School of Social Sciences, Communication, and Humanities, Endicott College, Beverley, MA 02115.
Program in Placebo Studies & Therapeutic Encounter, Harvard Medical School, Boston, MA 02215.

Irving Kirsch (I)

Program in Placebo Studies & Therapeutic Encounter, Harvard Medical School, Boston, MA 02215.

Ted J Kaptchuk (TJ)

Program in Placebo Studies & Therapeutic Encounter, Harvard Medical School, Boston, MA 02215.

Vitaly Napadow (V)

Athinoula A. Martinos Center for Biomedical Imaging, Massa, chusetts General Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, Charlestown, MA 02129.
Department of Radiology, Logan University, Chesterfield, MO 63017.

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