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Maternal childhood maltreatment: associations to offspring brain volume and white matter connectivity

Published online by Cambridge University Press:  21 September 2023

Claudia Lugo-Candelas*
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Le Chang
Affiliation:
Department of Statistics, University of South Carolina, Columbia, USA
Jordan D. Dworkin
Affiliation:
Federation of American Scientists Washington, Washington, USA
Natalie Aw
Affiliation:
Department of Electrical and Computer Engineering, Johns Hopkins University, Baltimore, USA
Andrea Fields
Affiliation:
Department of Psychology, Columbia University, New York, USA
Hannah Reed
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Marisa Spann
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Michelle A. Gilchrist
Affiliation:
Advocate Aurora Health, Milwaukee, USA
Walter Hinds
Affiliation:
Department of Neurology, Thomas Jefferson University, Philadelphia, PA, USA
Rachel Marsh
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
William P. Fifer
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Myrna Weissman
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Bernd Uwe Foerster
Affiliation:
Department of Psychiatry, Universidade Federal de São Paulo, Sao Paulo, Brazil
Marina Giorgi Manin
Affiliation:
Department of Pediatrics, Universidade Federal de São Paulo, Sao Paulo, Brazil
Ivaldo Silva
Affiliation:
Department of Gynecology, Universidade Federal de São Paulo, Sao Paulo, Brazil
Bradley Peterson
Affiliation:
Department of Psychiatry, University of Southern California, Los Angeles, CA, USA
Ana Carolina Coelho Milani
Affiliation:
Department of Psychiatry, Universidade Federal de São Paulo, Sao Paulo, Brazil
Jay Gingrich
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Catherine Monk
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Cristiane S. Duarte
Affiliation:
Department of Psychiatry, Columbia University Irving Medical Center/New York State Psychiatric Institute, New York, USA
Andrea Jackowski
Affiliation:
Department of Psychiatry, Universidade Federal de São Paulo, Sao Paulo, Brazil
Jonathan Posner
Affiliation:
Department of Psychiatry, Duke University, Durham, NC, USA
*
Corresponding author: Claudia Lugo-Candelas; Email: claudia.lugo@nyspi.columbia.edu

Abstract

The deleterious effects of adversity are likely intergenerational, such that one generation’s adverse experiences can affect the next. Epidemiological studies link maternal adversity to offspring depression and anxiety, possibly via transmission mechanisms that influence offspring fronto-limbic connectivity. However, studies have not thoroughly disassociated postnatal exposure effects nor considered the role of offspring sex. We utilized infant neuroimaging to test the hypothesis that maternal childhood maltreatment (CM) would be associated with increased fronto-limbic connectivity in infancy and tested brain-behavior associations in childhood. Ninety-two dyads participated (32 mothers with CM, 60 without; 52 infant females, 40 infant males). Women reported on their experiences of CM and non-sedated sleeping infants underwent MRIs at 2.44 ± 2.74 weeks. Brain volumes were estimated via structural MRI and white matter structural connectivity (fiber counts) via diffusion MRI with probabilistic tractography. A subset of parents (n = 36) reported on children’s behaviors at age 5.17 ± 1.73 years. Males in the maltreatment group demonstrated greater intra-hemispheric fronto-limbic connectivity (b = 0.96, p= 0.008, [95%CI 0.25, 1.66]), no differences emerged for females. Fronto-limbic connectivity was related to somatic complaints in childhood only for males (r = 0.673, p = 0.006). Our findings suggest that CM could have intergenerational associations to offspring brain development, yet mechanistic studies are needed.

Type
Original Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

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