Larger amygdala but no change in hippocampal volume in 10-year-old children exposed to maternal depressive symptomatology since birth

Abstract

Maternal separation and poor maternal care in animals have been shown to have important effects on the developing hippocampus and amygdala. In humans, children exposed to abuse/maltreatment or orphanage rearing do not present changes in hippocampal volumes. However, children reared in orphanages present enlarged amygdala volumes, suggesting that the amygdala may be particularly sensitive to severely disturbed (i.e., discontinous, neglectful) care in infancy. Maternal depressive symptomatology has been associated with reductions in overall sensitivity to the infant, and with an increased rate of withdrawn, disengaged behaviors. To determine if poor maternal care associated with maternal depressive symptomatology has a similar pattern of association to the volumes of the hippocampus and amygdala in children, as is the case for severely disturbed infant care (orphanage rearing), we measured hippocampal and amygdala volumes as well as stress hormone (glucocorticoid) levels in children exposed (n = 17) or not (n = 21) to maternal depressive symptomatology since birth. Results revealed no group difference in hippocampal volumes, but larger left and right amygdala volumes and increased levels of glucocorticoids in the children of mothers presenting depressive symptomatology since birth. Moreover, a significant positive correlation was observed between mothers' mean depressive scores and amygdala volumes in their children. The results of this study suggest that amygdala volume in human children may represent an early marker of biological sensitivity to quality of maternal care.I n all mammalian species, infants are highly dependent on their mothers not only for nutrition, but also for physical and affective interactions (1). In rodents, one of the most potent stressors for pups is separation from the dam for long periods of time. Maternal separation activates the pups' hypothalamic-pituitaryadrenal (HPA) axis, evidenced by increased circulating levels of adrenocorticotropic hormone and glucocorticoids (2). When they reach adulthood, rat pups subjected to maternal separation exhibit increased anxiety-like behavior, impaired cognitive capabilities, and dysregulation of the HPA axis (3). Similar outcomes have been reported in the offspring of mother rats that naturally display low levels of maternal care (4).Maternal separation and poor maternal care in the animal neonatal period are associated with structural changes in brain regions linked to cognition and mood regulation, including the hippocampus and the amygdala. Poor or absent maternal care in rodents is associated with decreased hippocampal volume and function in adolescence (5) and adulthood (6, 7), and these delayed effects have been shown to be related to an attenuation of the rate of synaptic development in the hippocampus (8). In contrast to the hippocampus, which shows protracted effects, the amygdala shows rapid changes in response to maternal separation or poor maternal care. For example, poor caregiving in rodents results in acceleration of amygdala develop...

Mother nurture and the social definition of neurodevelopment

“…A strength of the study is the laboratorybased assessment of maternal support during mildly stressful conditions, which very nicely mimics the challenges parents regularly face in child rearing. Maternal support at neither preschool nor school age emerged as a significant predictor of hippocampal volume, a finding consistent with cross-sectional studies showing that variations in maternal influences do not necessarily emerge as main effects in studies of neurodevelopment (2,3). However, the unique, longitudinal approach of Luby et al (1) reveals a compelling association between maternal support and hippocampal growth trajectories: hippocampal volume increased faster with age among subjects with higher levels of maternal support.…”

“…Sensitive periods for environmental signals are also regionally specific, which may explain the discrepancies noted by Luby et al (1) between their findings and those of others groups. For example, the authors note that Lupien et al (3) reported MRI findings with similarly aged subjects (mid-childhood), showing an association between postnatal maternal depression and the volume of the amygdala, but not the hippocampus. However, there are prenatal maternal influences, including maternal mood on the amygdala but not hippocampal volume, which are sustained into late childhood (9,10).…”

Invited Address: “The Times They Are A-Changin’” Gene Expression, Neuroplasticity, and Developmental Research

“…MRI and fMRI studies have indicated, for example, that exposure to harsh and unpredictable childhood conditions (e.g., parental neglect) is associated with greater volume and reactivity of the amygdala, a portion of the brain that is responsible for vigilance and emotional responsiveness to threat (e.g., Mehta et al 2009), and alteration of the prefrontal cortex, the area responsible for executive control (Hanson et al 2010;Wilson et al 2011). Other studies have reported that among adopted children, those adopted later have larger amygdala volume than those adopted earlier (Tottenham et al 2010), and that children continuously exposed to maternal depression show larger amygdala volume than those without such exposure (Lupien et al 2011). Importantly, the amygdala and prefrontal cortex, as well as their interconnection, are implicated in emotional regulation (e.g., Wager et al 2008), impulsivity (e.g., Kim and Lee 2011;Raine 2002), reactive aggression (Crowe and Blair 2008), and internalizing problems (Tottenham et al 2010).…”

Role of FKBP5 in emotion processing: results on amygdala activity, connectivity and volume

“…No study, so far, has investigated the impact of FKBP5 on amygdala volume. However this issue may be crucial, given the facts that FKBP5 is expressed in the amygdala (Scharf et al 2011) and that amygdala volume is increased following stress (Buss et al 2012;Lupien et al 2011;Tottenham et al 2010).…”