Prenatal Exposure to Maternal Mood Entropy Is Associated With a Weakened and Inflexible Salience Network in Adolescence

Robert J Jirsaraie; Anton M Palma; Steven L Small; Curt A Sandman; Elysia Poggi Davis; Tallie Z Baram; Hal Stern; Laura M Glynn; Michael A Yassa

doi:10.1016/j.bpsc.2023.08.002

Prenatal Exposure to Maternal Mood Entropy Is Associated With a Weakened and Inflexible Salience Network in Adolescence

Biol Psychiatry Cogn Neurosci Neuroimaging. 2024 Feb;9(2):207-216. doi: 10.1016/j.bpsc.2023.08.002. Epub 2023 Aug 22.

Authors

Robert J Jirsaraie¹, Anton M Palma², Steven L Small³, Curt A Sandman⁴, Elysia Poggi Davis⁵, Tallie Z Baram⁶, Hal Stern², Laura M Glynn⁷, Michael A Yassa⁸

Affiliations

¹ Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California; Department of Neurobiology and Behavior, University of California, Irvine, Irvine, California.
² Department of Statistics, University of California, Irvine, Irvine, California.
³ School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, Texas.
⁴ Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, California.
⁵ Department of Psychology, University of Denver, Denver, Colorado; Department of Pediatrics, University of California, Irvine, Irvine, California.
⁶ Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California; Department of Pediatrics, University of California, Irvine, Irvine, California; Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, California.
⁷ Department of Psychology, Chapman University, Orange, California. Electronic address: lglynn@chapman.edu.
⁸ Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California; Department of Neurobiology and Behavior, University of California, Irvine, Irvine, California; Department of Psychiatry and Human Behavior, University of California, Irvine, Irvine, California; Department of Anatomy and Neurobiology, University of California, Irvine, Irvine, California. Electronic address: myassa@uci.edu.

Abstract

Background: Fetal exposure to maternal mood dysregulation influences child cognitive and emotional development, which may have long-lasting implications for mental health. However, the neurobiological alterations associated with this dimension of adversity have yet to be explored. Here, we tested the hypothesis that fetal exposure to entropy, a novel index of dysregulated maternal mood, would predict the integrity of the salience network, which is involved in emotional processing.

Methods: A sample of 138 child-mother pairs (70 females) participated in this prospective longitudinal study. Maternal negative mood level and entropy (an index of variable and unpredictable mood) were assessed 5 times during pregnancy. Adolescents engaged in a functional magnetic resonance imaging task that was acquired between 2 resting-state scans. Changes in network integrity were analyzed using mixed-effect and latent growth curve models. The amplitude of low frequency fluctuations was analyzed to corroborate findings.

Results: Prenatal maternal mood entropy, but not mood level, was associated with salience network integrity. Both prenatal negative mood level and entropy were associated with the amplitude of low frequency fluctuations of the salience network. Latent class analysis yielded 2 profiles based on changes in network integrity across all functional magnetic resonance imaging sequences. The profile that exhibited little variation in network connectivity (i.e., inflexibility) consisted of adolescents who were exposed to higher negative maternal mood levels and more entropy.

Conclusions: These findings suggest that fetal exposure to maternal mood dysregulation is associated with a weakened and inflexible salience network. More broadly, they identify maternal mood entropy as a novel marker of early adversity that exhibits long-lasting associations with offspring brain development.

Keywords: Dysregulation; Emotional processing; Maternal mood entropy; Neurodevelopment; Salience network; fMRI.

MeSH terms

Adolescent
Brain / physiology
Entropy
Female
Humans
Longitudinal Studies
Pregnancy
Prenatal Exposure Delayed Effects*
Prospective Studies

Abstract

MeSH terms

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