Analogous to the experience-driven development of sensory systems, the functional maturation of limbic circuits is significantly influenced by early socio-emotional experience. In a combined light and electron microscopic study in the anterior cingulate cortex of Octodon degus, the densities of spine and shaft synapses on apical dendrites of layer III pyramidal neurons were compared in 45 day old (1) undisturbed control animals; (2) handled animals; (3) animals which were repeatedly maternally deprived during the first three postnatal weeks; (4) animals which were treated similarly to group 3 and thereafter kept in chronic social isolation. Animals in groups 2-4 showed significantly higher spine densities (up to 121%, 142% and 151% respectively) compared to control group 1. Group 3 displayed significantly longer apical dendrites compared to control group 1. The electron microscopic analysis in cortical layer II revealed significantly higher spine synapses in group 4 (up to 166%) and fewer shaft synapses in groups 3 and 4 (down to 53% and 65% respectively) compared to group 1. These results demonstrate that early traumatic emotional experience alters synaptic input of pyramidal neurons. Such experience-induced modulation of limbic cortex development may determine psychosocial and cognitive capacities during later life.

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A quantitative anatomical study in the rodent anterior cingulate and somatosensory cortex, hippocampus, and lateral amygdala revealed region-, cell-, and dendrite-specific changes of spine densities in 3-week-old Octodon degus after repeated parental separation. In parentally separated animals significantly higher spine densities were found on the apical and basal dendrites of the cingulate cortex (up to 143% on apical and 138% on basal dendrite). Branching order analysis revealed that this effect is seen on all segments of the apical dendrite, whereas on the basal dendrites significantly higher spine densities were seen only on the outer branches (third to fifth dendritic segments). Increased spine densities were also observed on the hippocampal CA1 pyramidal neurons (up to 109% on the distal apical segments and up to 106% on the basal segment) compared with the control group. In contrast, significantly reduced spine densities were observed on the granule cell dendrites in the dentate gyrus (down to 92%) and on the apical dendrites in the medial nucleus of the amygdala (down to 95%). No significant changes of spine densities were seen in the somatosensory cortex (except for an increase in the proximal apical segments) and in the lateral nucleus of the dorsal amygdala (except for an increase in the proximal basal dendritic segments). These results demonstrate that repeated stressful emotional experience alters the balance of presumably excitatory synaptic inputs of pyramidal neurons in the limbic system. Such experience-induced modulations of limbic circuits may determine psychosocial and cognitive capacities during later life.limbic system ͉ stress ͉ dendritic spines ͉ parental separation ͉ cingulate cortex

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Decades of research in the area of developmental psychobiology have shown that early life experience alters behavioral and brain development, which canalizes development to suit different environments. Recent methodological advances have begun to identify the mechanisms by which early life experiences cause these diverse adult outcomes. Here we present four different research programs that demonstrate the intricacies of early environmental influences on behavioral and brain development in both pathological and normal development. First, an animal model of schizophrenia is presented that suggests prenatal immune stimulation influences the postpubertal emergence of psychosis-related behavior in mice. Second, we describe a research program on infant rats that demonstrates how early odor learning has unique characteristics due to the unique functioning of the infant limbic system. Third, we present work on the rodent Octodon degus, which shows that early paternal and/or maternal deprivation alters development of limbic system synaptic density that corresponds to heightened emotionality. Fourth, a juvenile model of stress is presented that suggests this developmental period is important in determining adulthood emotional well being. The approach of each research program is strikingly different, yet all succeed in delineating a specific aspect of early development and its effects on infant and adult outcome that expands our understanding of the developmental impact of infant experiences on emotional and limbic system development. Together, these research programs suggest that the developing organism's developmental trajectory is influenced by environmental factors beginning in the fetus and extending through adolescence, although the specific timing and nature of the environmental influence has unique impact on adult mental health.