Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster

Abstract

The medial amygdala (Me), a brain region essential for mating behavior, changes in size during puberty. In pre-, mid-, and late pubertal (21, 35, and 49 days of age) male Syrian hamsters, we examined neuronal structure in Me and protein levels of spinophilin and synaptophysin in the amygdaloid complex for evidence of synaptic plasticity coincident with behavioral and physiological development. Body weight, testes weight, and testosterone levels increased during puberty. Mounting behavior, including ectopic, nonintromittive, and intromittive mounts, also increased. Neuronal structure in the posterodorsal medial amygdala (MePD) was assessed in Golgi-impregnated neurons. Pruning occurred during puberty in the number of dendrites emanating from the cell body and in terminal dendritic spine densities. Approximately half of all MePD neurons analyzed had an axon emanating from a dendrite rather than the cell body. However, prepubertal males were more likely to have the axon emanating from a higher order dendritic segment (secondary or tertiary) than were mid- and late pubertal males. Finally, protein levels in the amygdaloid complex varied with pubertal age. Spinophilin decreased, while synaptophysin and GAPDH protein levels increased. These results suggest that puberty is a period of dramatic synaptic plasticity in Me. Specifically, pruning of dendrites and spines, in combination with axonal changes, is likely to modify the afferent influences and electrophysiological properties of Me neurons. Because the Me is an integral component of a social behavior neural network, these changes may be related not only to sexual behavior, but also to other behaviors that mature during puberty, including aggressive, risk-taking, fear-related, and parental behaviors.

Postpubertal decrease in hippocampal dendritic spines of female rats

“…Differences between that study and ours are probably attributable to the choice of markers, spinophilin in our study, and synaptophysin in that of Andersen and Teicher (2004). These two markers do not exist in the same subcellular compartment (Choi et al 2003) and in fact, a study by Zehr et al found opposite pubertal changes in spinophilin (decrease) and synaptophysin (increase) in the amygdala of developing male hamsters (Zehr et al, 2006). …”

“…Although the mechanisms for these alterations in cognitive function are poorly understood, they may be due to developmental changes in synaptic plasticity that occur across the pubertal period. Consistent with this, reports show that synaptic density and/or dendritic spine number decrease during the transition from puberty to adulthood, as shown in monkey cortex (somatosensory: Zecevic & Rakic, 1991;prefrontal: Woo et al, 1997;visual: Bourgeois & Rakic, 1993) hamster medial amygdala (Zehr et al, 2006), and mouse hippocampus (Meyer et al, 1978).…”

“…Moreover, the elevated neurite outgrowth and arborization in hypothalamus in response to estrogens (Reier et al, 1977;Matsumoto & Arai, 1976) also leads to a prediction that such changes may occur in hippocampus. By contrast, as discussed above, puberty is accompanied by decreased synapse number in several brain regions (Zecevic & Rakic, 1991;Bourgeois et al, 1994;Zehr et al, 2006;Meyer et al, 1978). To address these issues, using high-resolution microscopy we quantified spinophilin immunoreactivity in CA1sr as a marker of dendritic spines (Hao et al, 2003;Tang et al, 2004) in female rats during the pubertal process.…”

Postnatal development of the amygdala: A stereological study in rats

“…Indeed, we found a decrease in the number of astrocytes in the rat amygdala after 3 weeks of age. Other studies have suggested a decrease in neuropil volume in the medial amygdala during puberty in the rat (Zehr et al, 2006). Similarly, a tracttracing study, using both retrograde and anterograde tracers, has shown that mPFC projections to the basal and accessory basal nuclei decrease between P25 and P90 in rats (Cressman et al, 2010).…”

An association of early puberty with disordered eating and anxiety in a population of undergraduate women and men

“…During adolescence, synaptic connections and neural circuits are still remarkably plastic. For example, neuron number in the prefrontal cortex differs in adolescent and adult rats (Markam et al, 2007), and neurons of the medial amygdala differ in structure among pre-, mid-, and late adolescent male hamsters (Zehr et al, 2006). Furthermore, adolescent rodents show differential responsiveness to anxiogenic situations, which is directly related to different effects of neurosteroids on cell excitability in adolescents and adults (Shen et al, 2007).…”