The bed nucleus of the stria terminalis and functionally linked neurocircuitry modulate emotion processing and HPA axis dysfunction in posttraumatic stress disorder.

Bed nucleus of the stria terminalis Functional connectivity Hypothalamic pituitary adrenal (HPA) axis PTSD Subcortical brain networks fMRI

Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2020
Historique:
received: 08 04 2020
revised: 14 09 2020
accepted: 15 09 2020
pubmed: 19 10 2020
medline: 29 6 2021
entrez: 18 10 2020
Statut: ppublish

Résumé

The bed nucleus of the stria terminalis (BNST) plays an important role in rodent posttraumatic stress disorder (PTSD), but evidence to support its relevance to human PTSD is limited. We sought to understand the role of the BNST in human PTSD via fMRI, behavioral, and physiological measurements. 29 patients with PTSD (childhood sexual abuse) and 23 healthy controls (HC) underwent BOLD imaging with an emotional word paradigm. Symptom severity was assessed using the Clinician-Administered PTSD Scale and HPA-axis dysfunction was assessed by measuring the diurnal cortisol amplitude index (DCAI). A data-driven multivariate analysis was used to determine BNST task-based functional co-occurrence (tbFC) across individuals. In the trauma-versus-neutral word contrast, patients showed increased activation compared to HC in the BNST, medial prefrontal cortex (mPFC), posterior cingulate gyrus (PCG), caudate heads, and midbrain, and decreased activation in dorsolateral prefrontal cortex (DLPFC). Symptom severity positively correlated with activity in the BNST, caudate head, amygdala, hippocampus, dorsal anterior cingulate gyrus (dACG), and PCG, and negatively with activity in the medial orbiotofrontal cortex (mOFC) and DLPFC. Patients and HC showed marked differences in the relationship between the DCAI and BOLD activity in the BNST, septal nuclei, dACG, and PCG. Patients showed stronger tbFC between the BNST and closely linked limbic and subcortical regions, and a loss of negative tbFC between the BNST and DLPFC. Based upon novel data, we present a new model of dysexecutive emotion processing and HPA-axis dysfunction in human PTSD that incorporates the role of the BNST and functionally linked neurocircuitry.

Sections du résumé

BACKGROUND
The bed nucleus of the stria terminalis (BNST) plays an important role in rodent posttraumatic stress disorder (PTSD), but evidence to support its relevance to human PTSD is limited. We sought to understand the role of the BNST in human PTSD via fMRI, behavioral, and physiological measurements.
METHODS
29 patients with PTSD (childhood sexual abuse) and 23 healthy controls (HC) underwent BOLD imaging with an emotional word paradigm. Symptom severity was assessed using the Clinician-Administered PTSD Scale and HPA-axis dysfunction was assessed by measuring the diurnal cortisol amplitude index (DCAI). A data-driven multivariate analysis was used to determine BNST task-based functional co-occurrence (tbFC) across individuals.
RESULTS
In the trauma-versus-neutral word contrast, patients showed increased activation compared to HC in the BNST, medial prefrontal cortex (mPFC), posterior cingulate gyrus (PCG), caudate heads, and midbrain, and decreased activation in dorsolateral prefrontal cortex (DLPFC). Symptom severity positively correlated with activity in the BNST, caudate head, amygdala, hippocampus, dorsal anterior cingulate gyrus (dACG), and PCG, and negatively with activity in the medial orbiotofrontal cortex (mOFC) and DLPFC. Patients and HC showed marked differences in the relationship between the DCAI and BOLD activity in the BNST, septal nuclei, dACG, and PCG. Patients showed stronger tbFC between the BNST and closely linked limbic and subcortical regions, and a loss of negative tbFC between the BNST and DLPFC.
CONCLUSIONS
Based upon novel data, we present a new model of dysexecutive emotion processing and HPA-axis dysfunction in human PTSD that incorporates the role of the BNST and functionally linked neurocircuitry.

Identifiants

pubmed: 33070099
pii: S2213-1582(20)30279-5
doi: 10.1016/j.nicl.2020.102442
pmc: PMC7569227
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

102442

Subventions

Organisme : NIMH NIH HHS
ID : P50 MH058911
Pays : United States

Informations de copyright

Copyright © 2020. Published by Elsevier Inc.

Références

Hum Brain Mapp. 2015 Oct;36(10):4076-88
pubmed: 26178381
J Comp Neurol. 1990 Dec 22;302(4):697-706
pubmed: 1707064
Psychoneuroendocrinology. 2018 Mar;89:239-249
pubmed: 29395488
Cortex. 2015 Mar;64:281-8
pubmed: 25569763
Hum Brain Mapp. 2017 Apr;38(4):2190-2205
pubmed: 28070973
Nat Rev Neurosci. 2012 Nov;13(11):769-87
pubmed: 23047775
J Neurosci. 2018 Jun 13;38(24):5567-5583
pubmed: 29844022
Nat Neurosci. 2015 Oct;18(10):1353-63
pubmed: 26404710
Psychoneuroendocrinology. 2017 Sep;83:25-41
pubmed: 28578301
Soc Cogn Affect Neurosci. 2017 Apr 1;12(4):555-568
pubmed: 27998993
Arch Gen Psychiatry. 1961 Jun;4:561-71
pubmed: 13688369
Cortex. 2015 May;66:60-8
pubmed: 25800506
Hum Brain Mapp. 2018 Mar;39(3):1367-1379
pubmed: 29266586
Am J Psychiatry. 1992 Jan;149(1):143-4
pubmed: 1728172
J Psychiatr Res. 2011 May;45(5):630-7
pubmed: 21109253
Biol Psychiatry. 2005 Mar 1;57(5):464-73
pubmed: 15737660
Neurosci Biobehav Rev. 2010 Sep;35(1):91-6
pubmed: 20109491
JAMA Psychiatry. 2017 Apr 1;74(4):407-415
pubmed: 28273291
Front Behav Neurosci. 2014 Apr 01;8:112
pubmed: 24744710
Neuroimage. 2002 Nov;17(3):1358-64
pubmed: 12414275
Neuroimage. 1998 Nov;8(4):360-9
pubmed: 9811554
Nat Rev Neurosci. 2010 Jul;11(7):503-13
pubmed: 20559337
J Neurosci. 2012 May 16;32(20):6906-16
pubmed: 22593059
Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10456-9
pubmed: 10468630
Mol Psychiatry. 2018 Apr;23(4):914-922
pubmed: 28439099
Neuroimage. 2002 Jan;15(1):1-15
pubmed: 11771969
Mol Psychiatry. 2016 Apr;21(4):450-63
pubmed: 26878891
J Pers Soc Psychol. 1989 Feb;56(2):267-83
pubmed: 2926629
Mol Psychiatry. 2018 Oct;23(10):1990-1997
pubmed: 28761080
Neurobiol Stress. 2019 Jun 04;11:100180
pubmed: 31236437
Neurosci Biobehav Rev. 2016 Oct;69:124-35
pubmed: 27443960
Nature. 2013 Apr 11;496(7444):224-8
pubmed: 23515155
Neuroimage. 2000 Jun;11(6 Pt 1):708-34
pubmed: 10860798
Neuroimage. 2014 May 1;91:311-23
pubmed: 24444996
Transl Psychiatry. 2018 Jan 31;8(1):33
pubmed: 29382815
Depress Anxiety. 2017 Jan;34(1):25-36
pubmed: 27110997
N Engl J Med. 2017 Jun 22;376(25):2459-2469
pubmed: 28636846
Soc Cogn Affect Neurosci. 2015 May;10(5):645-53
pubmed: 25062841
Trends Cogn Sci. 2011 Feb;15(2):85-93
pubmed: 21167765
Neurosci Biobehav Rev. 2014 May;42:1-8
pubmed: 24525267
Neuropsychopharmacology. 2010 Jan;35(1):105-35
pubmed: 19693004
Hum Brain Mapp. 2016 Mar;37(3):1091-102
pubmed: 26678871
Neuropsychopharmacology. 2016 Jan;41(1):103-25
pubmed: 26096838
Annu Rev Neurosci. 2015 Jul 8;38:433-47
pubmed: 25938726
Biol Psychiatry. 2018 Apr 15;83(8):638-647
pubmed: 29275839
Transl Psychiatry. 2016 Jul 19;6:e857
pubmed: 27434491
Biol Psychiatry. 2013 Dec 1;74(11):827-36
pubmed: 23871471
Neuroimage. 2017 Feb 15;147:872-879
pubmed: 27780778
Brain Lang. 2015 Dec;151:12-22
pubmed: 26575986
Hum Brain Mapp. 2012 Aug;33(8):1914-28
pubmed: 21769991
Magn Reson Med. 2001 Apr;45(4):635-44
pubmed: 11283992
Brain Res Rev. 2011 Jun 24;67(1-2):226-51
pubmed: 21354205
Biol Psychiatry. 2010 Sep 1;68(5):416-24
pubmed: 20497902
Nat Neurosci. 2018 Feb;21(2):283-289
pubmed: 29292378
Neuroimage. 2017 Feb 1;146:288-292
pubmed: 27876653
Nat Rev Neurosci. 2013 Jul;14(7):488-501
pubmed: 23783199
Nature. 2013 Apr 11;496(7444):219-23
pubmed: 23515158
Mol Psychiatry. 2017 Dec;22(12):1691-1700
pubmed: 27550842
J Neurosci. 2017 Oct 4;37(40):9645-9656
pubmed: 28893930
Learn Mem. 2017 Aug 16;24(9):480-491
pubmed: 28814474
J Mol Neurosci. 2010 Nov;42(3):327-40
pubmed: 20405238
Psychoneuroendocrinology. 2010 Jan;35(1):15-20
pubmed: 19836143
J Trauma Stress. 1995 Jan;8(1):75-90
pubmed: 7712061
Behav Res Ther. 1986;24(1):1-8
pubmed: 3947307
Am J Psychiatry. 2016 Nov 1;173(11):1083-1093
pubmed: 27609244
Eur J Neurosci. 2018 Oct;48(8):2783-2794
pubmed: 29044802
J Neurosci. 2009 Jun 3;29(22):7330-40
pubmed: 19494154

Auteurs

Samir Awasthi (S)

Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Hong Pan (H)

Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Joseph E LeDoux (JE)

Center for Neural Science, New York University, New York, NY, USA.

Marylene Cloitre (M)

National Center for PTSD, Veteran Affairs Palo Alto Health Care System, USA; Department of Psychiatry and Behavioral Sciences, Stanford University, Palo Alto, CA, USA.

Margaret Altemus (M)

Department of Psychiatry, Yale School of Medicine, New Haven, CT, USA.

Bruce McEwen (B)

Rockefeller University, New York, NY, USA.

David Silbersweig (D)

Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA. Electronic address: dsilbersweig@bwh.harvard.edu.

Emily Stern (E)

Department of Psychiatry, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA; Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH