Neural Network Functional Interactions Mediate or Suppress White Matter-Emotional Behavior Relationships in Infants.


Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
01 07 2023
Historique:
received: 01 08 2022
revised: 28 02 2023
accepted: 02 03 2023
pmc-release: 01 07 2024
medline: 16 6 2023
pubmed: 15 3 2023
entrez: 14 3 2023
Statut: ppublish

Résumé

Elucidating the neural basis of infant positive emotionality and negative emotionality can identify biomarkers of pathophysiological risk. Our goal was to determine how functional interactions among large-scale networks supporting emotional regulation influence white matter (WM) microstructural-emotional behavior relationships in 3-month-old infants. We hypothesized that microstructural-emotional behavior relationships would be differentially mediated or suppressed by underlying resting-state functional connectivity (rsFC), particularly between default mode network and central executive network structures. The analytic sample comprised primary caregiver-infant dyads (52 infants [42% female, mean age at scan = 15.10 weeks]), with infant neuroimaging and emotional behavior assessments conducted at 3 months. Infant WM and rsFC were assessed by diffusion-weighted imaging/tractography and resting-state magnetic resonance imaging during natural, nonsedated sleep. The Infant Behavior Questionnaire-Revised provided measures of infant positive emotionality and negative emotionality. After significant WM-emotional behavior relationships were observed, multimodal analyses were performed using whole-brain voxelwise mediation. Results revealed that greater cingulum bundle volume was significantly associated with lower infant positive emotionality (β = -0.263, p = .031); however, a pattern of lower rsFC between central executive network and default mode network structures suppressed this otherwise negative relationship. Greater uncinate fasciculus volume was significantly associated with lower infant negative emotionality (β = -0.296, p = .022); however, lower orbitofrontal cortex-amygdala rsFC suppressed this otherwise negative relationship, while greater orbitofrontal cortex-central executive network rsFC mediated this relationship. Functional interactions among neural networks have an important influence on WM microstructural-emotional behavior relationships in infancy. These relationships can elucidate neural mechanisms that contribute to future behavioral and emotional problems in childhood.

Sections du résumé

BACKGROUND
Elucidating the neural basis of infant positive emotionality and negative emotionality can identify biomarkers of pathophysiological risk. Our goal was to determine how functional interactions among large-scale networks supporting emotional regulation influence white matter (WM) microstructural-emotional behavior relationships in 3-month-old infants. We hypothesized that microstructural-emotional behavior relationships would be differentially mediated or suppressed by underlying resting-state functional connectivity (rsFC), particularly between default mode network and central executive network structures.
METHODS
The analytic sample comprised primary caregiver-infant dyads (52 infants [42% female, mean age at scan = 15.10 weeks]), with infant neuroimaging and emotional behavior assessments conducted at 3 months. Infant WM and rsFC were assessed by diffusion-weighted imaging/tractography and resting-state magnetic resonance imaging during natural, nonsedated sleep. The Infant Behavior Questionnaire-Revised provided measures of infant positive emotionality and negative emotionality.
RESULTS
After significant WM-emotional behavior relationships were observed, multimodal analyses were performed using whole-brain voxelwise mediation. Results revealed that greater cingulum bundle volume was significantly associated with lower infant positive emotionality (β = -0.263, p = .031); however, a pattern of lower rsFC between central executive network and default mode network structures suppressed this otherwise negative relationship. Greater uncinate fasciculus volume was significantly associated with lower infant negative emotionality (β = -0.296, p = .022); however, lower orbitofrontal cortex-amygdala rsFC suppressed this otherwise negative relationship, while greater orbitofrontal cortex-central executive network rsFC mediated this relationship.
CONCLUSIONS
Functional interactions among neural networks have an important influence on WM microstructural-emotional behavior relationships in infancy. These relationships can elucidate neural mechanisms that contribute to future behavioral and emotional problems in childhood.

Identifiants

pubmed: 36918062
pii: S0006-3223(23)01088-0
doi: 10.1016/j.biopsych.2023.03.004
pmc: PMC10365319
mid: NIHMS1894847
pii:
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

57-67

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH115466
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001857
Pays : United States

Informations de copyright

Copyright © 2023 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Références

Ann N Y Acad Sci. 2007 Dec;1121:546-61
pubmed: 17698998
J Abnorm Child Psychol. 2011 Feb;39(2):277-91
pubmed: 20862537
Bipolar Disord. 2019 Aug;21(5):449-457
pubmed: 30848539
PLoS One. 2019 Jan 4;14(1):e0209376
pubmed: 30608970
Neuroimage. 2012 Mar;60(1):340-52
pubmed: 22178809
Hum Brain Mapp. 2019 Jun 15;40(9):2800-2812
pubmed: 30854745
Brain Struct Funct. 2015 Mar;220(2):1173-86
pubmed: 24469153
J Perinat Neonatal Nurs. 2010 Jul-Sep;24(3):256-66
pubmed: 20697244
Dev Psychopathol. 2004 Spring;16(2):421-40
pubmed: 15487604
Biol Psychiatry Cogn Neurosci Neuroimaging. 2019 Jan;4(1):62-71
pubmed: 30316743
PLoS One. 2011 Apr 14;6(4):e18746
pubmed: 21533194
Neuropsychopharmacology. 2018 Aug;43(9):1972-1979
pubmed: 29777198
Neuropsychopharmacology. 2021 Jun;46(7):1340-1347
pubmed: 33782511
JAMA Pediatr. 2018 Oct 1;172(10):973-981
pubmed: 30177999
Infant Behav Dev. 2020 Feb;58:101389
pubmed: 31778859
Neuropsychopharmacology. 2020 Jul;45(8):1272-1279
pubmed: 32305039
Dev Sci. 2019 Sep;22(5):e12841
pubmed: 31016808
J Neurosci. 2014 Jul 23;34(30):10041-54
pubmed: 25057206
Bipolar Disord. 2017 Aug;19(5):386-395
pubmed: 28714580
Dev Cogn Neurosci. 2019 Jun;37:100604
pubmed: 30581123
J Affect Disord. 2021 Mar 1;282:465-471
pubmed: 33422824
Neuroscience. 2014 Sep 12;276:48-71
pubmed: 24378955
Biol Psychiatry. 2021 Sep 1;90(5):342-352
pubmed: 34130856
Trends Cogn Sci. 2013 Dec;17(12):627-40
pubmed: 24183779
Dev Psychol. 1997 Mar;33(2):218-27
pubmed: 9147831
Bipolar Disord. 2020 May;22(3):286-295
pubmed: 31604366
J Child Psychol Psychiatry. 2010 Jun;51(6):706-16
pubmed: 20050965
J Psychiatr Res. 2015 May;64:9-18
pubmed: 25801734
Dev Cogn Neurosci. 2021 Aug;50:100976
pubmed: 34174513
Dev Psychopathol. 2018 May;30(2):571-579
pubmed: 28803557
World J Biol Psychiatry. 2012 Dec;13(8):616-26
pubmed: 21604958
Proc Natl Acad Sci U S A. 2021 Mar 23;118(12):
pubmed: 33727420
Psychol Med. 2014 Nov;44(15):3263-73
pubmed: 25066663
Trends Cogn Sci. 2011 Oct;15(10):483-506
pubmed: 21908230
Neuroscientist. 2017 Apr;23(2):169-184
pubmed: 26929236
Nat Commun. 2021 May 12;12(1):2744
pubmed: 33980860
Hum Brain Mapp. 2021 May;42(7):2005-2017
pubmed: 33484503
Science. 1998 Feb 27;279(5355):1347-51
pubmed: 9478894
World Neurosurg. 2021 Aug;152:e625-e634
pubmed: 34144169
Trends Cogn Sci. 2004 Sep;8(9):418-25
pubmed: 15350243
Brain. 2013 Jun;136(Pt 6):1692-707
pubmed: 23649697
Cereb Cortex. 2013 Mar;23(3):594-603
pubmed: 22368080
JAMA Pediatr. 2018 Jun 1;172(6):525-533
pubmed: 29630692
Dev Cogn Neurosci. 2020 Oct;45:100815
pubmed: 32658763
Hum Brain Mapp. 2002 Nov;17(3):143-55
pubmed: 12391568
Neuroscientist. 2007 Apr;13(2):160-72
pubmed: 17404376
Pediatr Radiol. 2012 Feb;42(2):183-7
pubmed: 21861089
Child Dev. 1998 Oct;69(5):1378-89
pubmed: 9839422
Hum Brain Mapp. 2008 Jan;29(1):14-27
pubmed: 17318834
J Neurosci. 2013 Oct 9;33(41):16249-61
pubmed: 24107956
J Affect Disord. 2020 Aug 1;273:538-541
pubmed: 32560951
Neuroimage. 2006 Jan 1;29(1):203-15
pubmed: 16157491
Neural Netw. 2000 Oct-Nov;13(8-9):909-22
pubmed: 11156201
Dev Cogn Neurosci. 2020 Dec;46:100877
pubmed: 33220629
Neuropsychologia. 2013 Jan;51(1):67-78
pubmed: 23178227
Nat Hum Behav. 2019 Dec;3(12):1263-1270
pubmed: 31477910
Dev Neurosci. 2015;37(2):182-94
pubmed: 25791575
J Neurosci. 2011 Dec 14;31(50):18578-89
pubmed: 22171056
Curr Biol. 2011 Jul 26;21(14):1220-4
pubmed: 21723130
Top Magn Reson Imaging. 2019 Aug;28(4):189-196
pubmed: 31385898
Front Hum Neurosci. 2019 Dec 17;13:434
pubmed: 31920593
Dev Psychopathol. 2008 Winter;20(1):37-54
pubmed: 18211727
Commun Biol. 2023 Jul 14;6(1):726
pubmed: 37452124
Psychol Assess. 2012 Sep;24(3):647-60
pubmed: 22149326
Biol Psychiatry. 2021 Nov 15;90(10):678-688
pubmed: 34482949
IEEE Trans Med Imaging. 2010 Sep;29(9):1626-35
pubmed: 20304721
Neuroimage. 2012 Nov 15;63(3):1038-53
pubmed: 22884937
J Affect Disord. 2013 Jun;148(2-3):170-8
pubmed: 22854099
Neuroimage. 2014 Jan 1;84:320-41
pubmed: 23994314
Dev Cogn Neurosci. 2016 Feb;17:1-9
pubmed: 26562059
Annu Rev Neurosci. 2015 Jul 8;38:433-47
pubmed: 25938726
Neuroimage. 2019 Jan 15;185:388-397
pubmed: 30359729
Neuroimage. 2011 Oct 15;58(4):993-1005
pubmed: 21784163
Dev Psychobiol. 2021 Sep;63(6):e22166
pubmed: 34292595
PLoS One. 2015 Apr 07;10(4):e0123354
pubmed: 25848951
Biol Psychiatry. 2019 Jan 15;85(2):172-181
pubmed: 30122286
Proc Natl Acad Sci U S A. 2007 Jun 12;104(24):10240-5
pubmed: 17548818
J Neurosci. 2011 Jan 12;31(2):784-91
pubmed: 21228187
Transl Psychiatry. 2015 Feb 17;5:e508
pubmed: 25689569
Dev Cogn Neurosci. 2016 Apr;18:12-25
pubmed: 26499255
Dev Neurosci. 2019;41(5-6):327-340
pubmed: 32516794
J Neurosci. 2014 Jul 2;34(27):9067-75
pubmed: 24990927
Neuroimage. 2012 Jul 16;61(4):1000-16
pubmed: 22484410
Hum Brain Mapp. 2006 Aug;27(8):694-705
pubmed: 16404736
Br J Psychiatry. 1987 Jun;150:782-6
pubmed: 3651732
Brain Topogr. 2019 Nov;32(6):926-942
pubmed: 31707621
Brain. 2011 Jun;134(Pt 6):1591-609
pubmed: 21482550
Mol Psychiatry. 2017 Nov;22(11):1576-1584
pubmed: 27400854
Cortex. 2008 Sep;44(8):1105-32
pubmed: 18619589
J Abnorm Psychol. 2005 Feb;114(1):28-37
pubmed: 15709809
Soc Cogn Affect Neurosci. 2020 Jul 30;15(6):649-660
pubmed: 32577747
Neuroimage. 2017 Oct 15;160:15-31
pubmed: 28161313
Behav Brain Res. 2021 Aug 6;411:113370
pubmed: 34051230
PLoS One. 2013 Nov 15;8(11):e80713
pubmed: 24348913
Neuroimage. 2016 Nov 1;141:556-572
pubmed: 27393418
Behav Brain Res. 2011 Nov 20;225(1):341-7
pubmed: 21729721
Neuroimage. 2002 May;16(1):177-99
pubmed: 11969328
PLoS One. 2014 Aug 27;9(8):e104366
pubmed: 25162661
Hum Brain Mapp. 2017 May;38(5):2666-2682
pubmed: 28263011
J Am Acad Child Adolesc Psychiatry. 2017 Feb;56(2):157-166
pubmed: 28117062
Cereb Cortex. 2015 Sep;25(9):2919-28
pubmed: 24812084

Auteurs

Layla Banihashemi (L)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania. Electronic address: Layla.banihashemi@pitt.edu.

Vanessa J Schmithorst (VJ)

Department of Pediatric Radiology, University of Pittsburgh Medical Center Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania.

Michele A Bertocci (MA)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Alyssa Samolyk (A)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Yicheng Zhang (Y)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.

João Paulo Lima Santos (JP)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Amelia Versace (A)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Megan Taylor (M)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Gabrielle English (G)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Jessie B Northrup (JB)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Vincent K Lee (VK)

Department of Pediatric Radiology, University of Pittsburgh Medical Center Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania.

Richelle Stiffler (R)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Haris Aslam (H)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Ashok Panigrahy (A)

Department of Pediatric Radiology, University of Pittsburgh Medical Center Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania.

Alison E Hipwell (AE)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

Mary L Phillips (ML)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania.

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