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Prenatal social disadvantage is associated with alterations in functional networks at birth

Nielsen, Ashley N., Triplett, Regina L., Bernardez, Lourdes M., Tooley, Ursula A., Herzberg, Max P., Lean, Rachel E., Kaplan, Sydney, Meyer, Dominique, Kenley, Jeanette K., Alexopoulos, Dimitrios, Losielle, David, Latham, Aidan, Smyser, Tara A., Agrawal, Arpana, Shimony, Josh S., Jackson, Joshua J., Miller, J. Philip, Raichle, Marcus E., Warner, Barbara B., Rogers, Cynthia E., Sylvester, Chad M., Barch, Deanna M., Luby, Joan L., Smyser, Christopher D.·2024·Proceedings of the National Academy of Sciences

Abstract

Childhood exposure to social disadvantage is a major risk factor for psychiatric disorders and poor developmental, educational, and occupational outcomes, presumably because adverse exposures alter the neurodevelopmental processes that contribute to risk trajectories. Yet, given the limited social mobility in the United States and other countries, childhood social disadvantage is frequently preceded by maternal social disadvantage during pregnancy, potentially altering fetal brain development during a period of high neuroplasticity through hormonal, microbiome, epigenetic, and immune factors that cross the placenta and fetal blood–brain barrier. The current study examines prenatal social disadvantage to determine whether these exposures in utero are associated with alterations in functional brain networks as early as birth. As part of the Early Life Adversity and Biological Embedding study, mothers were recruited during pregnancy, prenatal social disadvantage was assessed across trimesters, and their healthy, full-term offspring were imaged using resting-state functional magnetic resonance imaging during the first weeks of life. Multivariate machine learning methods revealed that neonatal functional connectivity (FC) varied as a function of prenatal exposure to social disadvantage (n = 261, R = 0.43, R 2 = 0.18), with validation in an independent sample. Alterations in FC associated with prenatal social disadvantage occurred brain-wide and were most pronounced in association networks (fronto-parietal, ventral attention, dorsal attention) and the somatomotor network. Amygdala FC was altered at birth, with a pattern shared across subcortical structures. These findings provide critical insights into how early in development functional networks begin to diverge in the context of social disadvantage and elucidate the functional networks that are most impacted.

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Metadata

Authors
Nielsen, A. N., Triplett, R. L., Bernardez, L. M., Tooley, U. A., Herzberg, M. P., Lean, R. E., Kaplan, S., Meyer, D., Kenley, J. K., Alexopoulos, D., Losielle, D., Latham, A., Smyser, T. A., Agrawal, A., Shimony, J. S., Jackson, J. J., Miller, J. P., Raichle, M. E., Warner, B. B., Rogers, C. E., Sylvester, C. M., Barch, D. M., Luby, J. L., & Smyser, C. D.
Venue
Proceedings of the National Academy of Sciences
Published
2024-12-02
Volume
121
Issue
50
ISSN
  • 0027-8424
  • 1091-6490
Cited by
10
References
7
Language
en
Funders
  • HHS | NIH | National Institute of Mental Health (R01 MH121877, R01 MH113570, R01 MH113883, T32 GR0029379)
  • HHS | NIH | NIDA | National Drug Abuse Treatment Clinical Trials Network (R01 DA046224)
  • BCM | Intellectual and Developmental Disabilities Research Center (P50 HD103525, R01 MH090786)

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