Experience -dependent plasticity in the brains of biparental mammals
The adult brain is structurally plastic. Previous studies have shown that in several brain regions, experience alters dendritic architecture and the number of dendritic spines, which are major sites of excitatory synapses. Since most of this work has been done in rodents, the degree to which dendritic plasticity is a feature of the adult primate brain remains relatively unexplored. To investigate the influence of experience on structural plasticity in the adult primate brain, we examined multiple structural and synaptic protein changes in marmosets living in complex, 'enriched' environments and found increased dendritic spine density on granule neurons of the dentate gyrus, on pyramidal neurons of the CA1 region and pyramidal neurons of layers II/III in prefrontal cortex, but not on medium spiny neurons of the striatum. Coincident changes in the abundance of synaptic proteins, including synaptophysin, spinophilin and the AMPA receptor subunit GluR2 were observed. These findings suggest that the adult primate brain undergoes dendritic and synaptic remodeling in the hippocampus and the prefrontal cortex, in response to complex experience.
Common marmosets (Callithrix jacchus) are cooperative breeders, with fathers and older siblings displaying an unusual involvement in the care of the young. To test the possibility that the experience of caregiving affects structural plasticity, we examined dendritic measures in the brains of first-time fathers, experienced fathers and age-matched controls. In both groups of fathers, we found increased dendritic spine density on pyramidal neurons of the CA1 region and layers II/II of the prefrontal cortex, but not on those of the visual cortex. We also observed increases in the V1a vasopressin receptor in association with changes in dendritic spines in the prefrontal cortex, suggesting a potential relationship between structural plasticity and a neuropeptide involved in parenting. In a preliminary study, we also observed increased dendritic spine density on cortical pyramidal neurons in juvenile marmosets living with younger siblings, compared to age-matched controls, suggesting that dendritic changes are driven by stimuli related to contact with infants, rather than hormonal changes unique to the parents.
To determine whether these effects are specific to marmosets, we further investigated the influence of parenting on dendritic structure and neuropeptide receptor expression in the brain of the biparental California mouse ( Peromyscus californicus). We found enhanced dendritic spine density on pyramidal neurons of layer II/III of the medial precentral cortex, an area which may share characteristics with the primate prefrontal cortex. Moreover, we observed increases in neuropeptide receptor abundance which paralleled changes in dendritic spine density. Given that parenting (as well as living in a complex environment) impacted multiple brain areas in the adult marmoset, it is likely that parenting experience has wide-spread effects on the California mouse brain as well. Taken together, our results suggest that parenting induces structural changes in a number of brain regions, including the prefrontal cortex and the hippocampus. These effects are not dependent on the unique status of parents, since older sibling caretakers display similar changes, nor are they specific to marmosets. It appears that interaction with infants might elicit similar types of neural changes as environmental complexity, although the exact mechanisms underlying such changes, their pervasiveness and their functional consequences, remain to be determined.