Alterations in amygdala–prefrontal circuits in infants exposed to prenatal maternal depression

Abstract

Prenatal exposure to maternal depression is common and puts offspring at risk for developing a range of neuropsychiatric disorders. Despite its prevalence and adverse associations, neurobiological processes by which prenatal maternal depression (PMD) confers risk remain poorly understood. Maternal mood and fetal behavior were assessed between 34 and 37 gestational weeks. Using resting-state functional magnetic resonance imaging (fMRI) and diffusion MRI, we examined functional and structural connectivity within amygdala–prefrontal circuits in 64 infants (mean age=5.8±1.7 weeks) with (n=20) and without (n=44) in utero exposure to PMD. Resting fMRI and diffusion MRI both indicated atypical amygdala–prefrontal connectivity in PMD-exposed infants: Resting fMRI indicated increased inverse, or negative, functional connectivity between the amygdala and the dorsal prefrontal cortex (PFC), bilaterally, and diffusion MRI indicated decreased structural connectivity between the right amygdala and the right ventral PFC. Spectral dynamic causal modeling supported these findings suggesting altered amygdala–PFC effective (or directed) connectivity in PMD-exposed infants. Last, path analyses supported a mechanistic account relating PMD to a third-trimester fetal behavior: PMD alters amygdala–PFC connectivity, which in turn, is associated with an increase in fetal heart rate reactivity to in utero perturbation. These data suggest that the maturation and coordination of central and peripheral physiology are altered by prenatal exposure to maternal depression. To the best of our knowledge, this is the first study to directly associate infant MRI measures with a behavior—fetal heart rate response, and supports hypotheses that PMD-associated variations in the development of amygdala–PFC circuits are relevant for future neurobehavioral maturation.

Hub distribution of the brain functional networks of newborns prenatally exposed to maternal depression and SSRI antidepressants

“…Rifkin-Graboi et al, (2013) reported that prenatal depression is associated with reduced microstructure, but not with the volume of the right amygdala in newborn infants. Altered functional connectivity of the amygdala was also reported by Posner et al (2016). Altered functional connectivity of the amygdala was also reported by Posner et al (2016).…”

Maternal Depressive Symptoms During the Pre‐ and Postnatal Periods and Infant Attention to Emotional Faces

“…Prenatal exposure to maternal psychological stress, such as depression and anxiety, has been associated with alterations in child neurodevelopment and stress regulation systems (Sandman, Class, Glynn, & Davis, ; Van den Bergh et al., ). Changes in offspring hypothalamic–pituitary–adrenal axis function and glucocorticoid receptor sensitivity (Frasch et al., ; Loman & Gunnar, ), as well as alterations in brain functional and structural development (e.g., cortical thinning, amygdala‐prefrontal connectivity), and related problems in attention and emotion regulation have been reported (Dunkel Schetter & Tanner, ; Posner et al., ; Sandman, Glynn, & Davis, ; Sandman, Class, et al., ). Moreover, higher rates of symptoms of depression and anxiety as well as attention deficit hyperactivity disorder and conduct disorders have been reported in children with prenatal stress (PS) exposure (Glover, , ; Van den Bergh et al., ).…”

“…Electronic mail may be sent to eeva-leena.kataja@utu.fi. Gunnar, 2010), as well as alterations in brain functional and structural development (e.g., cortical thinning, amygdala-prefrontal connectivity), and related problems in attention and emotion regulation have been reported (Dunkel Schetter & Tanner, 2012;Posner et al, 2016;Sandman, Class, et al, 2016). Moreover, higher rates of symptoms of depression and anxiety as well as attention deficit hyperactivity disorder and conduct disorders have been reported in children with prenatal stress (PS) exposure (Glover, 2011(Glover, , 2015Van den Bergh et al, 2017).…”

Perinatal maternal depressive symptoms alter amygdala functional connectivity in girls

“…We focused on the amygdala that has featured prominently in developmental studies examining the influence of maternal mental health. Prenatal maternal depressive symptoms associate with the amygdala microstructure of neonates (Rifkin‐Graboi et al, ) and with amygdala functional connectivity with the prefrontal and limbic cortex as well as with the sensory cortex in infants (Posner et al, ; Qiu et al, ). Moreover, 10‐year‐old children of mothers with postnatal depression show larger bilateral amygdala volumes compared with those of mothers without depression (Lupien et al, ).…”