Postnatal development of the amygdala: A stereological study in macaque monkeys

Abstract

Abnormal development of the amygdala has been linked to several neurodevelopmental disorders, including schizophrenia and autism. However, the postnatal development of the amygdala is not easily explored at the cellular level in humans. Here we performed a stereological analysis of the macaque monkey amygdala in order to characterize the cellular changes underlying its normal structural development in primates. The lateral, basal, and accessory basal nuclei exhibited the same developmental pattern, with a large increase in volume between birth and 3 months of age, followed by slower growth continuing beyond 1 year of age. In contrast, the medial nucleus was near adult size at birth. At birth, the volume of the central nucleus was half of the adult value; this nucleus exhibited significant growth even after 1 year of age. Neither neuronal soma size, nor neuron or astrocyte numbers changed during postnatal development. In contrast, oligodendrocyte numbers increased substantially, in parallel with an increase in amygdala volume, after 3 months of age. At birth, the paralaminar nucleus contained a large pool of immature neurons that gradually developed into mature neurons, leading to a late increase in the volume of this nucleus. Our findings revealed that distinct amygdala nuclei exhibit different developmental profiles and that the amygdala is not fully mature for some time postnatally. We identified different periods during which pathogenic factors might lead to the abnormal development of distinct amygdala circuits, which may contribute to different human neurodevelopmental disorders associated with alterations of amygdala structure and functions.

Postnatal development of the amygdala: A stereological study in rats

“…Our major findings are as follows: 1) distinct amygdala nuclei exhibited different developmental profiles; 2) neuron number did not vary after birth in the main amygdala nuclei; 3) astrocyte number decreased between 3 weeks and 3 months of age; and 4) oligodendrocyte number increased from 1 week to beyond 3 months of age. We compare our findings with previous results in rats as well as with our previous systematic investigation carried out in monkeys (Chareyron et al, 2012). We also discuss our findings in relation to functional studies on the ontogeny of fear behaviors in the rat.…”

“…In sum, our current findings, together with previous findings in rats (Berdel et al, 1997b;Mizukami et al, 1983) and monkeys (Chareyron et al, 2012), indicate that the volume of the rat amygdala follows a developmental pattern similar to that of the whole brain, with a rapid growth up to 3 weeks of age, followed by slower but continuous growth until at least 7 months of age.…”

“…As discussed previously (see Chareyron et al, 2012), age-related differential shrinkage that might affect brain tissue during processing is unlikely to explain the specific changes in volume and cell numbers observed in the postnatally developing rat amygdala. Briefly, frozen section shrinkage is minor in the x-and y-planes compared with shrinkage in the z-plane (Carlo and Stevens, 2011).…”

“…8; Chareyron et al, 2012). The lateral, basal, and accessory basal nuclei exhibit a large increase in volume from 1 week to 3 weeks of age in rats and from birth to 3 months of age in monkeys.…”

“…It is thus important to define and characterize the postnatal development of the amygdala in order to understand the emergence of fear behaviors. We have previously used stereological techniques to describe the postnatal development of the monkey amygdala (Chareyron et al, 2012). In contrast, only scant information is available regarding the postnatal development of the rat amygdala.…”