Disentangling the effects of early caregiving experience and heritable factors on brain white matter development in rhesus monkeys.
Diffusion tensor imaging
Infant maltreatment
Inferior longitudinal fasciculus
Maternal care
Middle longitudinal fasciculus
Nonhuman primate
Temporal white matter
Uncinate fasciculus
Journal
NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515
Informations de publication
Date de publication:
15 08 2019
15 08 2019
Historique:
received:
25
09
2018
revised:
30
03
2019
accepted:
03
04
2019
pubmed:
13
4
2019
medline:
25
1
2020
entrez:
13
4
2019
Statut:
ppublish
Résumé
Early social experiences, particularly maternal care, shape behavioral and physiological development in primates. Thus, it is not surprising that adverse caregiving, such as child maltreatment leads to a vast array of poor developmental outcomes, including increased risk for psychopathology across the lifespan. Studies of the underlying neurobiology of this risk have identified structural and functional alterations in cortico-limbic brain circuits that seem particularly sensitive to these early adverse experiences and are associated with anxiety and affective disorders. However, it is not understood how these neurobiological alterations unfold during development as it is very difficult to study these early phases in humans, where the effects of maltreatment experience cannot be disentangled from heritable traits. The current study examined the specific effects of experience ("nurture") versus heritable factors ("nature") on the development of brain white matter (WM) tracts with putative roles in socioemotional behavior in primates from birth through the juvenile period. For this we used a randomized crossfostering experimental design in a naturalistic rhesus monkey model of infant maltreatment, where infant monkeys were randomly assigned at birth to either a mother with a history of maltreating her infants, or a competent mother. Using a longitudinal diffusion tensor imaging (DTI) atlas-based tract-profile approach we identified widespread, but also specific, maturational changes on major brain tracts, as well as alterations in a measure of WM integrity (fractional anisotropy, FA) in the middle longitudinal fasciculus (MdLF) and the inferior longitudinal fasciculus (ILF), of maltreated animals, suggesting decreased structural integrity in these tracts due to early adverse experience. Exploratory voxelwise analyses confirmed the tract-based approach, finding additional effects of early adversity, biological mother, social dominance rank, and sex in other WM tracts. These results suggest tract-specific effects of postnatal maternal care experience versus heritable or biological factors on primate WM microstructural development. Further studies are needed to determine the specific behavioral outcomes and biological mechanisms associated with these alterations in WM integrity.
Identifiants
pubmed: 30978495
pii: S1053-8119(19)30299-X
doi: 10.1016/j.neuroimage.2019.04.013
pmc: PMC7179761
mid: NIHMS1578330
pii:
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
625-642Subventions
Organisme : NIH HHS
ID : P51 OD011132
Pays : United States
Organisme : NIMH NIH HHS
ID : F31 MH086203
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD068588
Pays : United States
Organisme : NIMH NIH HHS
ID : T32 MH015755
Pays : United States
Organisme : RRD VA
ID : I01 RX002249
Pays : United States
Organisme : NCRR NIH HHS
ID : P51 RR000165
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM103650
Pays : United States
Organisme : NIMH NIH HHS
ID : P50 MH078105
Pays : United States
Organisme : NICHD NIH HHS
ID : R21 HD055255
Pays : United States
Informations de copyright
Copyright © 2019. Published by Elsevier Inc.
Références
Ann N Y Acad Sci. 1962 Dec 28;102:338-435
pubmed: 14012344
Am J Psychiatry. 2012 Jun;169(6):589-600
pubmed: 22362397
Neuroimage. 2012 Jan 16;59(2):1071-9
pubmed: 21985907
J Neurosci. 2007 Oct 24;27(43):11573-86
pubmed: 17959800
Neuroimage. 2004;23 Suppl 1:S151-60
pubmed: 15501084
PLoS Biol. 2009 Aug;7(8):e1000170
pubmed: 19668354
Physiol Behav. 2012 Jul 16;106(5):691-700
pubmed: 22210393
Neuropsychopharmacology. 2016 Jan;41(1):232-44
pubmed: 26279078
Nat Protoc. 2007;2(3):499-503
pubmed: 17406613
Horm Behav. 2006 Nov;50(4):623-31
pubmed: 16914153
Inf Process Med Imaging. 2015;24:794-805
pubmed: 26213453
Mol Psychiatry. 2007 Oct;12(10):895-7
pubmed: 17895923
Child Abuse Negl. 2018 Dec;86:178-183
pubmed: 30308348
Cortex. 2016 Dec;85:165-181
pubmed: 27289586
Neurosci Biobehav Rev. 1997 Sep;21(5):581-601
pubmed: 9353793
Neuroimage. 2010 Jan 1;49(1):199-204
pubmed: 19619664
Front Neuroendocrinol. 2016 Jan;40:52-66
pubmed: 26616341
Biol Psychiatry. 2018 Jan 15;83(2):137-147
pubmed: 29033027
Brain. 2004 Feb;127(Pt 2):340-50
pubmed: 14607785
Neuroimage. 2006 Sep;32(3):989-94
pubmed: 16854598
Neuroscience. 2014 Sep 12;276:48-71
pubmed: 24378955
Trends Cogn Sci. 2009 Feb;13(2):65-73
pubmed: 19135405
Pediatr Res. 1996 Jun;39(6):999-1005
pubmed: 8725261
Methods Mol Biol. 2011;711:127-44
pubmed: 21279600
Magn Reson Imaging. 2012 Nov;30(9):1323-41
pubmed: 22770690
Neuropsychol Rev. 2010 Jun;20(2):209-25
pubmed: 20422451
Autism Res. 2010 Oct;3(5):203-13
pubmed: 20625995
J Neurosci. 2009 Mar 11;29(10):3160-71
pubmed: 19279253
Mol Psychiatry. 2014 May;19(5):544-54
pubmed: 23689533
Soc Neurosci. 2015;10(5):512-26
pubmed: 26324227
J Int Neuropsychol Soc. 2016 Feb;22(2):180-90
pubmed: 26888615
Brain. 1989 Jun;112 ( Pt 3):799-835
pubmed: 2731030
Trends Neurosci. 2008 Jul;31(7):361-70
pubmed: 18538868
Child Dev. 2000 Mar-Apr;71(2):301-9
pubmed: 10834465
Eur J Pharmacol. 2008 Apr 7;583(2-3):174-85
pubmed: 18282566
J Magn Reson Imaging. 2001 Apr;13(4):534-46
pubmed: 11276097
J Neurosci. 2010 Aug 18;30(33):10985-90
pubmed: 20720105
Nat Rev Neurosci. 2003 Jun;4(6):469-80
pubmed: 12778119
Br J Anaesth. 2017 Sep 1;119(3):524-531
pubmed: 28969320
Neurotoxicol Teratol. 2017 Mar - Apr;60:63-68
pubmed: 27876652
Anim Behav. 1967 Jan;15(1):169-96
pubmed: 4961894
J Psychiatry Neurosci. 2011 Jan;36(1):32-40
pubmed: 20964953
Neuroimage. 2014 Oct 1;99:166-79
pubmed: 24879923
AJNR Am J Neuroradiol. 2011 May;32(5):857-63
pubmed: 21474629
Neuroreport. 1996 Jul 29;7(11):1761-4
pubmed: 8905659
Neuroscience. 2014 Sep 12;276:14-28
pubmed: 24051366
Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):3-18
pubmed: 12732219
Horm Behav. 2006 Nov;50(4):632-9
pubmed: 16876168
Dev Neurosci. 2015;37(3):243-52
pubmed: 26022835
Stroke. 1999 May;30(5):956-62
pubmed: 10229727
Child Dev. 2011 Jan-Feb;82(1):17-32
pubmed: 21291426
Anim Behav. 1998 Jan;55(1):1-11
pubmed: 9480666
Brain Res. 2012 Oct 15;1479:1-16
pubmed: 22902768
Psychopharmacology (Berl). 2011 Mar;214(1):55-70
pubmed: 20865251
Neuroimage. 2017 Apr 15;150:50-59
pubmed: 28213111
Biol Psychiatry. 2006 Oct 1;60(7):677-83
pubmed: 17008143
Prog Neuropsychopharmacol Biol Psychiatry. 1999 May;23(4):571-88
pubmed: 10390717
Neurosci Biobehav Rev. 2011 Jun;35(7):1562-92
pubmed: 21145350
Child Dev. 2013 Sep-Oct;84(5):1566-78
pubmed: 23480812
Cereb Cortex. 2010 Mar;20(3):561-9
pubmed: 19546156
Science. 2010 Nov 5;330(6005):768-9
pubmed: 21051624
J Affect Disord. 2016 Mar 1;192:167-75
pubmed: 26735328
Dev Psychopathol. 2007 Spring;19(2):367-83
pubmed: 17459175
Biol Psychiatry. 1999 May 15;45(10):1271-84
pubmed: 10349033
Biol Psychiatry. 2012 Feb 15;71(4):286-93
pubmed: 22112927
Cereb Cortex. 2013 Jan;23(1):36-48
pubmed: 22275483
J Vis. 2017 Feb 1;17(2):4
pubmed: 28196374
Dev Med Child Neurol. 2012 Jan;54(1):6-7
pubmed: 22098073
Dev Psychobiol. 2014 Jan;56(1):86-95
pubmed: 23192465
Front Neuroinform. 2014 Jan 30;8:4
pubmed: 24523693
Cereb Cortex. 2013 May;23(5):1014-24
pubmed: 22539611
Neurology. 1992 Apr;42(4):749-52
pubmed: 1565226
Proc Natl Acad Sci U S A. 2005 Jul 5;102(27):9726-9
pubmed: 15983367
Proc Natl Acad Sci U S A. 2010 May 11;107(19):8507-12
pubmed: 20442329
PLoS Biol. 2006 Sep;4(9):e302
pubmed: 16953662
Biol Psychiatry. 2014 Aug 15;76(4):297-305
pubmed: 24209775
Child Dev. 2010 Jan-Feb;81(1):28-40
pubmed: 20331653
Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16074-9
pubmed: 21911374
Horm Behav. 2009 Apr;55(4):538-47
pubmed: 19470363
J R Soc Med. 2012 Apr;105(4):151-6
pubmed: 22532655
Cereb Cortex. 2010 May;20(5):1053-63
pubmed: 19703936
Dev Psychopathol. 2010 Winter;22(1):45-53
pubmed: 20102646
Psychiatry Res. 2015 Oct 30;234(1):35-43
pubmed: 26341951
Nat Rev Neurosci. 2009 Jun;10(6):434-45
pubmed: 19401723
Curr Immunol Rev. 2010 Aug 1;6(3):195-204
pubmed: 20729991
Neuroimage. 2012 Nov 15;63(3):1038-53
pubmed: 22884937
Biol Mood Anxiety Disord. 2013 Dec 02;3(1):21
pubmed: 24289263
Neuroscience. 2014 Sep 12;276:2-13
pubmed: 25003711
Cereb Cortex. 2011 May;21(5):1012-7
pubmed: 20847151
Science. 2015 Mar 27;347(6229):1480-5
pubmed: 25814584
Brain. 2007 Mar;130(Pt 3):630-53
pubmed: 17293361
Front Neurosci. 2017 Jan 10;10:617
pubmed: 28119564
J Nerv Ment Dis. 2013 Dec;201(12):1007-20
pubmed: 24284634
Cereb Cortex. 2014 Dec;24(12):3334-49
pubmed: 23908263
Biol Psychiatry. 2010 Sep 1;68(5):408-15
pubmed: 20673872
J Neurosci Res. 2012 Feb;90(2):346-55
pubmed: 21938736
J Neurosci. 2011 Jan 12;31(2):784-91
pubmed: 21228187
Neuroimage. 2014 Jan 1;84:753-64
pubmed: 24076225
Eur Neuropsychopharmacol. 2014 Jun;24(6):907-18
pubmed: 24589292
Ann Neurol. 2012 Oct;72(4):525-35
pubmed: 23109147
Am J Primatol. 2013 May;75(5):509-17
pubmed: 23436319
Dev Psychopathol. 2001 Summer;13(3):419-49
pubmed: 11523842
Int J Dev Neurosci. 2016 May;50:26-38
pubmed: 26948153
Neurosci Biobehav Rev. 1999;23(3):411-22
pubmed: 9989428
Front Neuroinform. 2014 Jan 09;7:51
pubmed: 24409141
Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):33-44
pubmed: 12732221
J Neurosci. 2009 Dec 2;29(48):15089-99
pubmed: 19955360
Cereb Cortex. 2009 Jun;19(6):1322-9
pubmed: 18842665
Brain Struct Funct. 2016 Nov;221(8):4059-4071
pubmed: 26627483
Biol Psychiatry. 2009 Feb 1;65(3):227-34
pubmed: 18692174
JAMA Psychiatry. 2018 Jan 1;75(1):21-27
pubmed: 29188292
Schizophr Res. 2009 Jan;107(1):30-8
pubmed: 19028423
Arch Neurol. 2000 Jan;57(1):65-70
pubmed: 10634450
Annu Rev Psychol. 2007;58:145-73
pubmed: 16903808
Behav Neural Biol. 1991 Nov;56(3):307-13
pubmed: 1759948
J Neuropathol Exp Neurol. 1988 May;47(3):217-34
pubmed: 3367155
Nat Neurosci. 2009 Nov;12(11):1370-1
pubmed: 19820707
Hum Brain Mapp. 1996;4(1):58-73
pubmed: 20408186
JAMA Pediatr. 2015 Mar;169(3):211-9
pubmed: 25622303
Annu Rev Clin Psychol. 2011;7:63-85
pubmed: 21219189
Biol Psychiatry. 2002 Dec 1;52(11):1047-56
pubmed: 12460688
Dev Psychobiol. 1989 Nov;22(7):669-81
pubmed: 2806728
J Nerv Ment Dis. 1984 Feb;172(2):105-8
pubmed: 6537968
J Abnorm Psychol. 2007 Feb;116(1):176-87
pubmed: 17324028
Cereb Cortex. 2019 Apr 1;29(4):1584-1593
pubmed: 29701751
Neuroimage. 2006 Oct 15;33(1):27-38
pubmed: 16905335
J Child Neurol. 2014 Mar;29(3):318-25
pubmed: 23358628
Dev Psychobiol. 2006 Nov;48(7):537-50
pubmed: 17016838
Dev Psychopathol. 2017 Dec;29(5):1539-1551
pubmed: 29162166
Front Zool. 2015 Aug 24;12 Suppl 1:S14
pubmed: 26816514
Soc Neurosci. 2017 Feb;12(1):50-64
pubmed: 27295326
Neuroimage. 2012 Jul 2;61(3):542-57
pubmed: 22510254
Neuroimage. 2012 Jan 2;59(1):306-18
pubmed: 21803162
Pediatrics. 2012 Jan;129(1):e232-46
pubmed: 22201156
Physiol Behav. 2012 Jul 16;106(5):707-21
pubmed: 22306534
Am J Primatol. 2015 Jan;77(1):20-33
pubmed: 25066041
Pediatrics. 2006 Jun;117(6):2093-100
pubmed: 16740852
J Psychiatry Neurosci. 2012 Jan;37(1):37-45
pubmed: 22008179
Pediatrics. 2004 Apr;113(4):846-57
pubmed: 15060237
J Neuropathol Exp Neurol. 1987 May;46(3):283-301
pubmed: 3559630
J Am Acad Child Adolesc Psychiatry. 1995 May;34(5):541-65
pubmed: 7775351
Proc Natl Acad Sci U S A. 2007 May 15;104(20):8556-61
pubmed: 17483487
Biol Psychiatry. 2018 Jan 15;83(2):120-127
pubmed: 28842114
Neuroimage. 2013 May 15;72:91-105
pubmed: 23357075
Neuropsychopharmacology. 2012 Nov;37(12):2693-701
pubmed: 22850736
Neuroreport. 2008 May 28;19(8):817-20
pubmed: 18463493