Unstable wakefulness during resting-state fMRI and its associations with network connectivity and affective psychopathology in young adults.
Affective disorders
Resting-state fMRI
Sleep
Journal
Journal of affective disorders
ISSN: 1573-2517
Titre abrégé: J Affect Disord
Pays: Netherlands
ID NLM: 7906073
Informations de publication
Date de publication:
01 11 2019
01 11 2019
Historique:
received:
13
03
2019
revised:
19
07
2019
accepted:
29
07
2019
pubmed:
12
8
2019
medline:
4
7
2020
entrez:
12
8
2019
Statut:
ppublish
Résumé
Drifts between wakefulness and sleep are common during resting state functional MRI (rsfMRI). Among healthy adults, within-scanner sleep can impact functional connectivity of default mode (DMN), task-positive (TPN), and thalamo-cortical networks. Because dysfunctional arousal states (i.e., sleepiness, sleep disturbance) are common in affective disorders, individuals with affective psychopathology may be more prone to unstable wakefulness during rsfMRI, hampering the estimation of clinically meaningful functional connectivity biomarkers. A transdiagnostic sample of 150 young adults (68 psychologically distressed; 82 psychiatrically healthy) completed rsfMRI and reported whether they experienced within-scanner sleep. Symptom scales were reduced into depression/anxiety and mania proneness dimensions using principal component analysis. We evaluated associations between within-scanner sleep, clinical status, and functional connectivity of the DMN, TPN, and thalamus. Within-scanner sleep during rsfMRI was reported by 44% of participants (n = 66) but was unrelated to psychiatric diagnoses or mood symptom severity (p-values > 0.05). Across all participants, self-reported within-scanner sleep was associated with connectivity signatures akin to objectively-assessed sleep, including lower within-DMN connectivity, lower DMN-TPN anti-correlation, and altered thalamo-cortical connectivity (p < 0.05, corrected). Among participants reporting sustained wakefulness (n = 84), depression/anxiety severity positively associated with averaged DMN-TPN connectivity and mania proneness negatively associated with averaged thalamus-DMN connectivity (p-values < 0.05). Both relationships were attenuated and became non-significant when participants reporting within-scanner sleep were included (p-values > 0.05). Subjective report of within-scanner sleep. Findings implicate within-scanner sleep as a source of variance in network connectivity; careful monitoring and correction for within-scanner sleep may enhance our ability to characterize network signatures underlying affective psychopathology.
Sections du résumé
BACKGROUND
Drifts between wakefulness and sleep are common during resting state functional MRI (rsfMRI). Among healthy adults, within-scanner sleep can impact functional connectivity of default mode (DMN), task-positive (TPN), and thalamo-cortical networks. Because dysfunctional arousal states (i.e., sleepiness, sleep disturbance) are common in affective disorders, individuals with affective psychopathology may be more prone to unstable wakefulness during rsfMRI, hampering the estimation of clinically meaningful functional connectivity biomarkers.
METHODS
A transdiagnostic sample of 150 young adults (68 psychologically distressed; 82 psychiatrically healthy) completed rsfMRI and reported whether they experienced within-scanner sleep. Symptom scales were reduced into depression/anxiety and mania proneness dimensions using principal component analysis. We evaluated associations between within-scanner sleep, clinical status, and functional connectivity of the DMN, TPN, and thalamus.
RESULTS
Within-scanner sleep during rsfMRI was reported by 44% of participants (n = 66) but was unrelated to psychiatric diagnoses or mood symptom severity (p-values > 0.05). Across all participants, self-reported within-scanner sleep was associated with connectivity signatures akin to objectively-assessed sleep, including lower within-DMN connectivity, lower DMN-TPN anti-correlation, and altered thalamo-cortical connectivity (p < 0.05, corrected). Among participants reporting sustained wakefulness (n = 84), depression/anxiety severity positively associated with averaged DMN-TPN connectivity and mania proneness negatively associated with averaged thalamus-DMN connectivity (p-values < 0.05). Both relationships were attenuated and became non-significant when participants reporting within-scanner sleep were included (p-values > 0.05).
LIMITATIONS
Subjective report of within-scanner sleep.
CONCLUSIONS
Findings implicate within-scanner sleep as a source of variance in network connectivity; careful monitoring and correction for within-scanner sleep may enhance our ability to characterize network signatures underlying affective psychopathology.
Identifiants
pubmed: 31401540
pii: S0165-0327(19)30653-6
doi: 10.1016/j.jad.2019.07.066
pmc: PMC6710159
mid: NIHMS1536882
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
125-132Subventions
Organisme : NIMH NIH HHS
ID : K01 MH111953
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH100041
Pays : United States
Organisme : NIMH NIH HHS
ID : R37 MH100041
Pays : United States
Informations de copyright
Copyright © 2019. Published by Elsevier B.V.
Références
Compr Psychiatry. 2002 Jan-Feb;43(1):69-73
pubmed: 11788923
Neuroimage. 2003 Jul;19(3):1233-9
pubmed: 12880848
Br J Med Psychol. 1959;32(1):50-5
pubmed: 13638508
J Neurol Neurosurg Psychiatry. 1960 Feb;23:56-62
pubmed: 14399272
Brain. 2006 Mar;129(Pt 3):655-67
pubmed: 16339798
Ind Health. 2006 Oct;44(4):564-76
pubmed: 17085917
Nat Rev Neurosci. 2007 Sep;8(9):700-11
pubmed: 17704812
J Abnorm Psychol. 1991 Aug;100(3):316-36
pubmed: 1918611
Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11376-81
pubmed: 19549821
J Neurophysiol. 2010 Jul;104(1):322-35
pubmed: 20463201
Clin Psychol Rev. 2011 Mar;31(2):225-35
pubmed: 20471738
Front Syst Neurosci. 2010 May 14;4:13
pubmed: 20577591
Neuroimage. 2010 Dec;53(4):1197-207
pubmed: 20600983
J Neurosci. 2010 Aug 25;30(34):11379-87
pubmed: 20739559
Cereb Cortex. 2011 Sep;21(9):2082-93
pubmed: 21330468
J Neurophysiol. 2011 Sep;106(3):1125-65
pubmed: 21653723
Prog Brain Res. 2011;193:277-94
pubmed: 21854969
Front Neuroinform. 2011 Aug 22;5:13
pubmed: 21897815
Annu Rev Clin Psychol. 2012;8:49-76
pubmed: 22224834
Neuroimage. 2012 Oct 15;63(1):63-72
pubmed: 22743197
Hum Brain Mapp. 2014 Jan;35(1):257-69
pubmed: 23008180
Neurosci Biobehav Rev. 2014 Jul;44:45-57
pubmed: 23092655
Evid Based Ment Health. 2013 May;16(2):40
pubmed: 23329054
Neuroimage. 2013 Oct 15;80:387-96
pubmed: 23707592
Cereb Cortex. 2014 Dec;24(12):3116-30
pubmed: 23825317
Neuroimage. 2013 Dec;83:983-90
pubmed: 23899724
Sleep. 2014 Feb 01;37(2):387-97
pubmed: 24497667
Neuron. 2014 May 7;82(3):695-708
pubmed: 24811386
Acta Neurol Scand. 2015 Mar;131(3):145-51
pubmed: 25263131
Sleep Med Clin. 2013 Sep;8(3):361-371
pubmed: 25302060
Neuron. 2014 Dec 3;84(5):892-905
pubmed: 25475184
Neuroimage. 2015 May 1;111:147-58
pubmed: 25700949
Neuroimage. 2015 Sep;118:553-62
pubmed: 26019123
Neuroimage. 2016 Jan 1;124(Pt A):24-31
pubmed: 26327245
Neuroimage. 2016 Feb 15;127:324-332
pubmed: 26712339
Hum Brain Mapp. 2016 Apr;37(4):1459-73
pubmed: 26800659
Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):9653-8
pubmed: 27512040
Neuroimage. 2017 Jul 1;154:169-173
pubmed: 27888059
J Neurosci. 2017 Jun 7;37(23):5594-5607
pubmed: 28450543
Neuroimage. 2017 Oct 15;160:55-72
pubmed: 28619656
Sci Rep. 2017 Jul 19;7(1):5908
pubmed: 28724928
Cereb Cortex. 2018 Sep 1;28(9):3095-3114
pubmed: 28981612
Sleep Med Rev. 2018 Aug;40:196-202
pubmed: 29402512
Neuroimage. 2018 Jul 1;174:263-273
pubmed: 29555427
Neuroimage. 2018 Aug 15;177:1-10
pubmed: 29704612
J Cereb Blood Flow Metab. 2018 Aug 3;:271678X18791070
pubmed: 30073858
BMC Psychiatry. 2019 Jan 25;19(1):43
pubmed: 30683074
Br J Psychol. 1970 Aug;61(3):303-21
pubmed: 5457503
Sleep. 1982;5(3):267-76
pubmed: 7134732
Br J Psychiatry. 1978 Nov;133:429-35
pubmed: 728692