Pathological claustrum activity drives aberrant cognitive network processing in human chronic pain.

Chronic pain Claustrum Cognition Cognitive control Migraine Networks Pain

Journal

bioRxiv : the preprint server for biology
Titre abrégé: bioRxiv
Pays: United States
ID NLM: 101680187

Informations de publication

Date de publication:
02 Nov 2023
Historique:
pubmed: 14 11 2023
medline: 14 11 2023
entrez: 14 11 2023
Statut: epublish

Résumé

Aberrant cognitive network activity and cognitive deficits are established features of chronic pain. However, the nature of cognitive network alterations associated with chronic pain and their underlying mechanisms require elucidation. Here, we report that the claustrum, a subcortical nucleus implicated in cognitive network modulation, is activated by acute painful stimulation and pain-predictive cues in healthy participants. Moreover, we discover pathological activity of the claustrum and a lateral aspect of the right dorsolateral prefrontal cortex (latDLPFC) in migraine patients. Dynamic causal modeling suggests a directional influence of the claustrum on activity in this latDLPFC region, and diffusion weighted imaging (DWI) verifies their structural connectivity. These findings advance understanding of claustrum function during acute pain and provide evidence of a possible circuit mechanism driving cognitive impairments in chronic pain.

Identifiants

pubmed: 37961503
doi: 10.1101/2023.11.01.564054
pmc: PMC10635040
pii:
doi:

Types de publication

Preprint

Langues

eng

Subventions

Organisme : NCCIH NIH HHS
ID : R01 AT007176
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS112356
Pays : United States

Déclaration de conflit d'intérêts

Declaration of Interests: The authors declare no competing interests.

Références

J Cereb Blood Flow Metab. 1997 Mar;17(3):301-8
pubmed: 9119903
Curr Biol. 2018 Sep 10;28(17):2752-2762.e7
pubmed: 30122531
Cell Rep. 2018 Jan 2;22(1):84-95
pubmed: 29298436
Neuropsychopharmacology. 2011 Jan;36(1):316-38
pubmed: 20844478
Brain. 2004 Apr;127(Pt 4):835-43
pubmed: 14960499
J Neurosci. 2022 Apr 13;42(15):3241-3252
pubmed: 35232759
Pain. 2010 Mar;148(3):368-374
pubmed: 19875233
Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):11073-8
pubmed: 17576922
Brain. 2022 Apr 18;145(2):441-456
pubmed: 34897383
Cortex. 2013 May;49(5):1195-205
pubmed: 22789779
J Neurosci. 2011 May 18;31(20):7540-50
pubmed: 21593339
Hum Brain Mapp. 2015 Mar;36(3):827-38
pubmed: 25339630
Pain. 2020 Aug;161(8):1837-1846
pubmed: 32701843
Pain. 2011 May;152(5):1104-1113
pubmed: 21377797
Neuroimage. 2006 Apr 1;30(2):436-43
pubmed: 16300968
J Neurosci. 2015 Aug 19;35(33):11595-605
pubmed: 26290236
J Neurosci Methods. 2008 Jul 15;172(1):137-41
pubmed: 18501969
Neuroimage. 2015 Nov 15;122:166-76
pubmed: 26236030
Psychol Bull. 1999 May;125(3):356-66
pubmed: 10349356
Neuroimage. 2019 Oct 15;200:12-25
pubmed: 31226492
Sci Rep. 2021 Nov 25;11(1):22929
pubmed: 34824311
Neuroimage. 2010 Feb 15;49(4):3057-64
pubmed: 19944173
J Neurosci. 2007 Feb 28;27(9):2349-56
pubmed: 17329432
Proc Natl Acad Sci U S A. 2021 Jul 6;118(27):
pubmed: 34193521
Cereb Cortex. 2023 Aug 23;33(17):9787-9801
pubmed: 37429832
Cereb Cortex. 2014 Nov;24(11):2981-90
pubmed: 23765157
Front Syst Neurosci. 2014 Jul 03;8:123
pubmed: 25071475
NMR Biomed. 2019 Apr;32(4):e3785
pubmed: 28945294
Neuroimage. 2007 Aug 1;37(1):90-101
pubmed: 17560126
Neuroimage. 1996 Jun;3(3 Pt 1):143-57
pubmed: 9345485
Neuroimage. 2019 Oct 15;200:174-190
pubmed: 31226497
Pharmacol Rev. 2019 Jul;71(3):316-344
pubmed: 31221820
eNeuro. 2014 Dec 30;1(1):e20.14
pubmed: 25893216
Neuroimage. 2013 Nov 15;82:208-25
pubmed: 23747457
J Neurosci. 2012 Oct 31;32(44):15601-10
pubmed: 23115195
J Neurosci. 2008 Sep 10;28(37):9239-48
pubmed: 18784304
Neuroimage. 2019 Aug 1;196:59-67
pubmed: 30954711
Trends Cogn Sci. 2008 Mar;12(3):99-105
pubmed: 18262825
Hum Brain Mapp. 2005 Dec;26(4):231-9
pubmed: 15954139
Cell Rep. 2023 Feb 28;42(2):112118
pubmed: 36774552
Neuroimage. 2003 Aug;19(4):1273-302
pubmed: 12948688
Neuroscience. 1984 Jun;12(2):409-25
pubmed: 6462456
Pain. 2006 Feb;120(3):297-306
pubmed: 16427738
Sci Data. 2015 Jan 20;2:140054
pubmed: 25977805
Neuroimage. 2013 Oct 15;80:105-24
pubmed: 23668970
Neuroimage. 2005 Aug 1;27(1):59-69
pubmed: 15978845
Neuroimage. 2013 Oct 15;80:62-79
pubmed: 23684880
Neuroimage. 2015 Feb 15;107:207-218
pubmed: 25497686
Neuroimage. 2003 Oct;20(2):870-88
pubmed: 14568458
Brain. 2003 May;126(Pt 5):1079-91
pubmed: 12690048
J Comp Neurol. 2017 Apr 15;525(6):1347-1362
pubmed: 26801010
Neurol Res. 2023 Aug;45(8):717-724
pubmed: 37019685
Neuroimage. 2012 Aug 15;62(2):782-90
pubmed: 21979382
Biol Psychiatry. 2020 Nov 1;88(9):719-726
pubmed: 32456782
Magn Reson Med. 2003 Nov;50(5):1077-88
pubmed: 14587019
Neuroimage. 2017 Jul 1;154:169-173
pubmed: 27888059
Ann Card Anaesth. 2019 Jan-Mar;22(1):67-72
pubmed: 30648682
Trends Cogn Sci. 2022 Dec;26(12):1133-1152
pubmed: 36192309
J Neurosci. 2010 Sep 29;30(39):12964-77
pubmed: 20881115
Brain Res Cogn Brain Res. 2005 Sep;25(1):153-60
pubmed: 15935625
Neuron. 2007 Oct 25;56(2):209-25
pubmed: 17964241
Neuroimage. 2006 Jul 1;31(3):968-80
pubmed: 16530430
Neuroimage. 2007 Jan 1;34(1):144-55
pubmed: 17070705
Hum Brain Mapp. 2009 Sep;30(9):2731-45
pubmed: 19072897
Proc Natl Acad Sci U S A. 2016 May 24;113(21):6059-64
pubmed: 27162349
J Comp Neurol. 2002 Dec 9;454(2):140-57
pubmed: 12412139
Rev Neurosci. 2014;25(1):1-24
pubmed: 24361772
Brain Dev. 2007 Mar;29(2):83-91
pubmed: 16919409
Elife. 2016 Mar 21;5:
pubmed: 26999822
Cell Rep. 2022 Dec 20;41(12):111860
pubmed: 36543121
J Neurophysiol. 2007 May;97(5):3651-9
pubmed: 17314240
Philos Trans R Soc Lond B Biol Sci. 2005 Apr 29;360(1456):781-95
pubmed: 15937012
Biol Psychiatry. 2007 Apr 15;61(8):935-45
pubmed: 17046727
Neuroimage. 2002 Oct;17(2):825-41
pubmed: 12377157
Brain. 2013 Sep;136(Pt 9):2751-68
pubmed: 23983029
Neuroimage. 2013 Oct 15;80:144-68
pubmed: 23702415
Neuroimage. 2010 Jan 15;49(2):1432-45
pubmed: 19782143
J Neurosci. 2006 Nov 1;26(44):11501-9
pubmed: 17079679
N Engl J Med. 2013 Apr 11;368(15):1388-97
pubmed: 23574118
Schizophr Res. 2006 Apr;83(2-3):155-71
pubmed: 16448806
Pain. 2013 Jul;154(7):972-7
pubmed: 23473784
Neuroimage. 2012 Oct 1;62(4):2222-31
pubmed: 22366334
Science. 2003 Nov 14;302(5648):1181-5
pubmed: 14615530
Brain Struct Funct. 2018 Dec;223(9):3945-3958
pubmed: 30109490
Neuroimage. 2014 Aug 1;96:22-35
pubmed: 24657780
Hum Brain Mapp. 1996;4(1):58-73
pubmed: 20408186
PLoS Comput Biol. 2010 Nov 18;6(11):e1001006
pubmed: 21124954
Neuroimage. 2020 Sep;218:116980
pubmed: 32454209
Reg Anesth Pain Med. 2020 Jul;45(7):486-494
pubmed: 32371500
Cell Rep. 2023 May 30;42(5):112506
pubmed: 37182208
Neuroimage. 2014 Jul 15;95:287-304
pubmed: 24657353
Brain Res Bull. 2001 Nov 15;56(5):495-507
pubmed: 11750795
Neuroimage Clin. 2015 Jan 10;7:347-58
pubmed: 25610798
Proc Natl Acad Sci U S A. 2003 Jan 7;100(1):253-8
pubmed: 12506194
Brain Struct Funct. 2018 Jul;223(6):2999-3006
pubmed: 29623428
Elife. 2022 Sep 28;11:
pubmed: 36169404
J Neurosci. 2023 Apr 5;43(14):2527-2536
pubmed: 36868855
Mol Psychiatry. 2003 Jan;8(1):60-70
pubmed: 12556909
Am J Psychiatry. 2005 Jul;162(7):1256-65
pubmed: 15994707
J Neurosci. 2008 Feb 6;28(6):1398-403
pubmed: 18256259
Magn Reson Med. 1996 Jan;35(1):107-13
pubmed: 8771028
Neuropsychopharmacology. 2022 Jan;47(1):90-103
pubmed: 34408276
Front Neuroanat. 2018 Nov 26;12:100
pubmed: 30534060
Clin J Pain. 2016 Aug;32(8):673-80
pubmed: 26626294
Neurosci Lett. 2008 Jul 4;439(1):7-12
pubmed: 18502045
Pain. 2010 Apr;149(1):19-26
pubmed: 20129735
Neurotherapeutics. 2021 Jan;18(1):534-543
pubmed: 33184743
Nat Rev Neurosci. 2011 Mar;12(3):154-67
pubmed: 21331082
J Neurosci. 2022 Oct 26;42(43):8154-8168
pubmed: 36100399
Clin Psychol Rev. 2014 Nov;34(7):563-79
pubmed: 25265056
Cereb Cortex. 2015 Nov;25(11):4126-34
pubmed: 24925773

Auteurs

Brent W Stewart (BW)

Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.

Michael L Keaser (ML)

Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.

Hwiyoung Lee (H)

Department of Epidemiology & Public Health, Maryland Psychiatric Research Center, Catonsville, MD, USA.

Sarah M Margerison (SM)

Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.
Physical Therapy and Rehabilitation Science, University of Maryland School of Medicine, Baltimore, MD, USA.

Matthew A Cormie (MA)

Centre for Multimodal Sensorimotor and Pain Research, Faculty of Dentistry, University of Toronto, ON, Canada.

Massieh Moayedi (M)

Centre for Multimodal Sensorimotor and Pain Research, Faculty of Dentistry, University of Toronto, ON, Canada.
Department of Dentistry, Mount Sinai Hospital, Toronto, ON, Canada.
Division of Clinical & Computational Neuroscience, Krembil Brain Institute, University Health Network.

Martin A Lindquist (MA)

Department of Biostatistics, Johns Hopkins University, Baltimore, MD, USA.

Shuo Chen (S)

Department of Epidemiology & Public Health, Maryland Psychiatric Research Center, Catonsville, MD, USA.

Brian N Mathur (BN)

Department of Pharmacology, University of Maryland School of Medicine, Baltimore, MD, USA.

David A Seminowicz (DA)

Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.
Department of Medical Biophysics, Schulich School of Medicine & Dentistry, University of Western Ontario, London, Ontario, Canada.

Classifications MeSH