Neonatal Nucleus Accumbens Microstructure Modulates Individual Susceptibility to Preconception Maternal Stress in Relation to Externalizing Behaviors - 27/09/24
Abstract |
Objective |
Maternal stress influences in utero brain development and is a modifiable risk factor for offspring psychopathologies. Reward circuitry dysfunction underlies various internalizing and externalizing psychopathologies. This study examined (1) the association between maternal stress and microstructural characteristics of the neonatal nucleus accumbens (NAcc), a major node of the reward circuitry, and (2) whether neonatal NAcc microstructure modulates individual susceptibility to maternal stress in relation to childhood behavioral problems.
Method |
K-means longitudinal cluster analysis was performed to determine trajectories of maternal stress measures (Perceived Stress Scale [PSS], hair cortisol) from preconception to the third trimester. Neonatal NAcc microstructural measures (orientation density index [ODI] and intracellular volume fraction [ICVF]) were compared across trajectories. We then examined the interaction between maternal stress and neonatal NAcc microstructure on child internalizing and externalizing behaviors, assessed between ages 3 and 4 years.
Results |
Two trajectories of maternal stress magnitude (“low”/“high”) were identified for both PSS (n = 287) and hair cortisol (n = 336). Right neonatal NAcc ODI (rNAcc-ODI) was significantly lower in “low” relative to “high” PSS trajectories (n = 77, p = .04). PSS at preconception had the strongest association with rNAcc-ODI (r = 0.293, p = .029). No differences in NAcc microstructure were found between hair cortisol trajectories. A significant interaction between preconception PSS and rNAcc-ODI on externalizing behavior was observed (n = 47, p = .047).
Conclusion |
Our study showed that the preconception period contributes to in utero NAcc development, and that NAcc microstructure modulates individual susceptibility to preconception maternal stress in relation to externalizing problems.
Plain language summary |
In the S-PRESTO population-based cohort study conducted in Singapore with 351 women and their children, higher levels of maternal perceived stress within the year before pregnancy were associated with increased dendritic complexity within offsprings’ nucleus accumbens, indicative of a more advanced developmental profile. Variations in right nucleus accumbens microstructure significantly modulated the association between maternal perceived stress at preconception and externalizing behaviors in early childhood. Study findings suggest that maternal stress in the preconception period accelerates in-utero nucleus accumbens development, leading to differential risk to externalizing problems in later childhood.
Le texte complet de cet article est disponible en PDF.Key words : neuroimaging, maternal factors, stress, brain development, Child Behavior Checklist
Plan
| This research was supported by grants NMRC/TCR/004-NUS/2008 and NMRC/TCR/012-NUHS/2014 from the National Research Foundation, Singapore under the Translational and Clinical Research Flagship and grant OFLCG/MOH-000504 from the Open Fund Large Collaborative Grant Programmes and administered by the Singapore Ministry of Health’s National Medical Research Council, Singapore. Additional funding was provided by the Singapore Institute for Clinical Sciences, Agency for Science Technology and Research, Singapore. MJM is supported by funding from the Hope for Depression Research Foundation, USA, and the Jacobs Foundation, Switzerland. APT is supported by funding from the NMRC Transition Award (MOH-001273-00). SYC is supported by funding from the NMRC Open Fund – Young Individual Research Grant (MOH-001149-00). |
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| The research was performed with permission from the National Healthcare Group Domain Specific Review Board. |
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| Consent has been provided for descriptions of specific patient information. |
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| The data sets for this paper are derived from the Singapore PREconception Study of long-Term maternal and child Outcomes (S-PRESTO) longitudinal birth cohort study. The data are publicly-accessible using access procedures modelled after those of the National Institutes of Health through requests to the S-PRESTO Executive Committee, and directed to the corresponding author. SYC and APT had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. |
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| Authorship Contributions Conceptualization: APT; Data Acquisition: HYC, ARG, MVF; Data Processing: SYC, XZL, ZMN, ZYO, Ss/oK, MZLK; Formal Analysis: SYC, XZL; Writing original draft and visualization: SYC, XZL, APT; Writing review and editing: APT, MJM, JHZ, MZLK, PH, SYC, XZL, ZMN; Supervision: APT, MJM; Project administration and funding acquisition: MJM, YSC, PDG, TKH, JKYC |
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| Disclosure: Prof. Chong has reported being part of an academic consortium that has received research funding from Abbott Nutrition, Nestec, and Danone. Drs. Chan, Low, Kee, Huang, Rifkin-Graboi, Fortier, Zhou, and A.P. Tan, Profs. Chen, K.H. Tan, Chan, Gluckman, and Meaney, Mr. Ngoh, Ms. Ong, and Mr. Kumar have reported no biomedical financial interests or potential conflicts of interest. |
Vol 63 - N° 10
P. 1035-1046 - octobre 2024 Retour au numéro
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