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Immature neurons in the primate amygdala: Changes with early development and disrupted early environment
Alexandra C McHale-Matthews1, Danielle M DeCampo2, Tanzy Love3
1University of Rochester, School of Medicine and Dentistry, Department of Neuroscience, Rochester, NY 14642, USA.
Insights
The amygdala paralaminar nucleus (PL) shows neuronal maturation from infancy to adolescence in macaques. Maternal separation stress may alter this developmental trajectory, impacting neuron maturation.
Area of Science:
- Neuroscience
- Developmental Biology
- Primate Research
Background:
- The amygdala paralaminar nucleus (PL) in primates contains immature neurons.
- Understanding neuronal development in the PL is crucial for comprehending brain maturation.
Purpose of the Study:
- To investigate the developmental changes in PL neurons from infancy to adolescence in macaques.
- To examine the impact of early-life maternal separation stress on PL neuronal development in infant macaques.
Main Methods:
- Comparative analysis of PL neurons in infant and adolescent maternally-reared macaques.
- Assessment of PL neurons in infant macaques exposed to maternal separation versus controls.
- Quantification of immature and mature neurons, soma volumes, and TBR1 mRNA expression.
Main Results:
- Adolescent macaques showed fewer immature neurons, more mature neurons, and larger immature soma volumes in the PL compared to infants.
- Total neuron counts decreased in adolescent PL, suggesting migration out of the nucleus.
- Maternal separation did not alter neuron counts but correlated immature neuron soma volume with mature neuron counts and TBR1 mRNA levels in infants.
Conclusions:
- Immature neurons in the primate amygdala paralaminar nucleus gradually mature by adolescence.
- Early-life maternal separation stress may disrupt normal neuronal maturation pathways in the PL, as indicated by altered TBR1 mRNA expression and neuron maturation correlations.
Abstract:
In human and nonhuman primates, the amygdala paralaminar nucleus (PL) contains immature neurons. To explore the PL's potential for cellular growth during development, we compared PL neurons in (1) infant and adolescent macaques (control, maternally-reared), and in (2) infant macaques that experienced separation from their mother in the first month of life compared to control maternally-reared infants. In maternally-reared animals, the adolescent PL had fewer immature neurons, more mature neurons, and larger immature soma volumes compared to infant PL. There were also fewer total neurons (immature plus mature) in adolescent versus infant PL, suggesting that some neurons move out of the PL by adolescence. Maternal separation did not change mean immature or mature neuron counts in infant PL. However, across all infant animals, immature neuron soma volume was strongly correlated with mature neuron counts. TBR1 mRNA, a transcript required for glutamatergic neuron maturation, is significantly reduced in the maternally-separated infant PL (DeCampo et al., 2017), and was also positively correlated with mature neuron counts in infant PL. We conclude that immature neurons gradually mature by adolescence, and that the stress of maternal separation may shift this trajectory, as revealed by correlations between TBR1 mRNA and mature neuron numbers across animals.
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