Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice

Ono, Mitsuhiro; Kikusui, Takefumi; Sasaki, Narie; Ichikawa, Masumi; Mori, Yuji; Murakami‐Murofushi, Kimiko

doi:10.1016/j.neuroscience.2008.07.078

Cited by 126 publications

(122 citation statements)

References 52 publications

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“…Our results are strikingly similar to those of two independent studies that reported enlarged amygdala volumes and no hippocampal difference in children previously reared in orphanages (25,26). These results are also consistent with animal data showing that poor caregiving in rodents is associated with acceleration of amygdala development in offspring (9,10), and with others showing that maternal deprivation in rodents (8) …”

Section: Discussionsupporting

confidence: 92%

“…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 development (9,10), increases in corticotrophin-releasing hormone-containing neurons (11), and sensitization of the amygdala in adolescence (12). In addition, nonhuman primate studies show that maternal separation alters amygdala development, and that this effect is more devastating when maternal separation occurs earlier in life (13).…”

mentioning

confidence: 99%

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

Lupien

Parent

Evans

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

339

223

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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symptomatology has been associated with reductions in overall sensitivity to the infant, and with an increased rate of withdrawn, disengaged behaviors.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...

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Section: Discussionsupporting

confidence: 92%

mentioning

confidence: 99%

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

Lupien

Parent

Evans

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

339

223

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“…Ono et al (2008) demonstrated that the concentration of glycolipid galactosylceramide, a myelin constituent, increases linearly between P21 and P54 in the basal nucleus of the mouse amygdala. Their results also indicated that myelin formation occurs later in the amygdala than in the prefrontal cortex and hippocampus (Ono et al, 2008). It thus stands to reason that the late increase in oligodendrocyte number in the amygdala might accompany delayed myelination of this structure.…”

Section: Second Stage: Myelinationmentioning

confidence: 99%

“…Indeed, oligodendrocytes produce the myelin sheath that surrounds axons (Nave, 2010), and an increase in oligodendrocyte number has been linked to an increase in axon myelination during development in the monkey visual system (O'Kusky and Colonnier, 1982). Ono et al (2008) demonstrated that the concentration of glycolipid galactosylceramide, a myelin constituent, increases linearly between P21 and P54 in the basal nucleus of the mouse amygdala. Their results also indicated that myelin formation occurs later in the amygdala than in the prefrontal cortex and hippocampus (Ono et al, 2008).…”

Section: Second Stage: Myelinationmentioning

confidence: 99%

Postnatal development of the amygdala: A stereological study in rats

Chareyron

Lavenex

2012

J of Comparative Neurology

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The amygdala is the central component of a functional brain system regulating fear and emotional behaviors. Studies of the ontogeny of fear behaviors reveal the emergence of distinct fear responses at different postnatal ages. Here, we performed a stereological analysis of the rat amygdala to characterize the cellular changes underlying its normal structural development. Distinct amygdala nuclei exhibited different patterns of postnatal development, which were largely similar to those we have previously shown in monkeys. The combined volume of the lateral, basal, and accessory basal nuclei increased by 113% from 1 to 3 weeks of age and by an additional 33% by 7 months of age. The volume of the central nucleus increased only 37% from 1 to 2 weeks of age and 38% from 2 weeks to 7 months. At 1 week of age, the medial nucleus was 77% of the 7-monthold's volume and exhibited a constant, marginal increase until 7 months. Neuron number did not differ in the amygdala from 1 week to 7 months of age. In contrast, astrocyte number decreased from 3 weeks to 2 months of age in the whole amygdala. Oligodendrocyte number increased in all amygdala nuclei from 3 weeks to 7 months of age. Our findings revealed that distinct amygdala nuclei exhibit different developmental profiles and that the rat amygdala is not fully mature for an extended period postnatally. We identified different periods of postnatal development of distinct amygdala nuclei and cellular components, which are concomitant with the ontogeny of different fear and emotional behaviors.

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“…of the dams (e.g., mom rats) ( Figure 2). By manipulating the caregiving conditions of infant rodents with the above methods, behavioral neuroscience experiments found that early life maltreatment could accelerate amygdala development [38,45,46] in terms of accelerated growth of dendrites, early myelination [37], increases in the amount of CRH-containing neurons [40] (Table 3), and functional sensitization [39]. In the central nucleus of the amygdala, decreased levels of benzodiazepine receptor binding, which plays an important role in inhibition of neuron activity, were observed among rats that received worse maternal care during infancy (Figure 4), and these rats also demonstrated higher anxiety levels behaviorally.…”

Section: Evidence From Behavioral Neuroscience Studiesmentioning

confidence: 99%

Amygdala, Childhood Adversity and Psychiatric Disorders

Yan¹

2012

The Amygdala - A Discrete Multitasking Manager

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Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice

Cited by 126 publications

References 52 publications

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

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

Postnatal development of the amygdala: A stereological study in rats

Amygdala, Childhood Adversity and Psychiatric Disorders

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