Refinement of dendritic and synaptic networks in the rodent anterior cingulate and orbitofrontal cortex: Critical impact of early and late social experience

Abstract

The process of weaning programs the neurobehavioral development and therefore provides a critical formative period for adult behavior. However, the neural substrates underlying these behavioral changes are largely unknown. To test the hypothesis that during childhood neuronal networks in the prefrontal cortex are reorganized in response to the timing and extent of social interactions, we analyzed the length, ramification, and spine density of apical and basal dendrites of layer II/III pyramidal neurons in four groups of male rats. (1) Early weaning at postnatal day (PND) 21 + postweaning social rearing (EWS), (2) late weaning at PND 30 + postweaning social rearing (LWS), (3) early weaning + postweaning social isolation (EWI), (4) late weaning + postweaning social isolation (LWI). Compared with late weaned animals, the early weaned animals displayed elevated spine densities on apical and basal dendrites only in the anterior cingulate (ACd), but not in the orbitofrontal cortex (OFC), irrespective of the postweaning housing conditions. For dendritic length and complexity an interaction between the factors weaning and postweaning rearing conditions was observed. In the ACd the EWI animals had longer and more complex apical dendrites compared with all other groups, whereas in the OFC the EWI animals displayed a significant reduction of apical dendritic length and complexity compared with the EWS group. Taken together, our findings show that the timing as well as the amount of social contact with family members significantly affects the refinement of prefrontal cortical synaptic networks, which are essential for emotional and cognitive behavior.

Prefrontal Plasticity and Stress Inoculation-Induced Resilience

“…Diminished usage-dependent cell loss and selective retention of synaptic connections in ventromedial prefrontal cortex may accompany the learning-like process of coping with early life stress. This possibility is consistent with evidence of experience-dependent prefrontal plasticity in adolescent rats [42] .…”

Gender- and anxiety level-dependent effects of perinatal stress exposure on medial prefrontal cortex

“…For example, brief exposure to maternal separation between P1 and P3 significantly reduces dendritic spine density in layers II-III pyramidal neurons of the anterior cingulate cortex, but separation between P14 and P16 results in an increase in these neurons (Bock et al, 2005). Besides, irrespective to postweaning social or isolation rearing conditions, early-weaned (at P21) animals display elevated spine densities on apical and basal dendrites of the anterior cingulate cortex in comparison to lateweaned (at P30) animals (Bock et al, 2008). While Muhammad and Kolb reported that male and female pups, separated daily for 3 h from the dam during P3-P21, display an increase in the spine density in the mPFC (Muhammad and Kolb, 2011a;Muhammad et al, 2012); SilvaGomez et al reported that 8 weeks of postweaning social isolation causes 48-51% decrease in the spine density of basal dendrites in the mPFC (Silva-Gomez et al, 2003).…”

Adolescent sleep patterns in humans and laboratory animals

“…Complementing the human results, developmental trends in delta power appear somewhat similar to changes observed in frontal grey matter volume (Van Eden and Uylings, 1985), but overall the results remain weak and relatively uncharacterized. Since there is evidence that cortical development during adolescence is sensitive to environmental enrichment (Bock et al, 2008), it is possible that full cortical pruning and a decline in delta power akin to human adolescents may only consistently emerge in laboratory animals living in and interacting with more natural environments. In this case, more detailed studies of delta power during NREM sleep in rodents could help pinpoint developmental stages with robust cortical plasticity (and potential vulnerability) analogous to human adolescence.…”