Environmental enrichment effects on synaptic and cellular physiology of hippocampal neurons.

Exposure of rodents to an enriched environment (EE) has been shown to reliably increase performance on hippocampus-dependent learning and memory tasks, compared to conspecifics living in standard housing conditions. Here we review the EE-related functional changes in synaptic and cellular properties for neurons in the dentate gyrus and area CA1, as assessed through in vivo and ex vivo electrophysiological approaches. There is a growing consensus of findings regarding the pattern of effects seen. Most prominently, there are changes in cellular excitability and synaptic plasticity in CA1, particularly with short-term and/or periodic exposure to EE. Such changes are much less evident after longer term continuous exposure to EE. In the dentate gyrus, increases in synaptic transmission as well as cell excitability become evident after short-term EE exposure, while the induction of long-term potentiation (LTP) in the dentate is remarkably insensitive, even though it is reliably enhanced by voluntary running. Recent evidence has added a new dimension to the understanding of EE effects on hippocampal electrophysiology by revealing an increased sparsity of place cell representations after long periods of EE treatment. It is possible that such connectivity change is one of the key factors contributing to the enhancement of hippocampus-dependent spatial learning over the long-term, even if there are no obvious changes in other markers such as LTP. This article is part of the Special Issue entitled "Neurobiology of Environmental Enrichment".

Adult-born dentate granule cell excitability depends on the interaction of neuron age, ontogenetic age and experience.

Early during their maturation, adult-born dentate granule cells (aDGCs) are particularly excitable, but eventually develop the electrophysiologically quiet properties of mature cells. However, the stability versus plasticity of this quiet state across time and experience remains unresolved. By birthdating two populations of aDGCs across different animal ages, we found for 10-month-old rats the expected reduction in excitability across cells aged 4-12 weeks, as determined by Egr1 immunoreactivity. Unexpectedly, cells 35 weeks old (after genesis at an animal age of 2 months) were as excitable as 4-week-old cells, in the dorsal hippocampus. This high level of excitability at maturity was specific for cells born in animals 2 months of age, as cells born later in life did not show this effect. Importantly, excitability states were not fixed once maturity was gained, but were enhanced by enriched environment exposure or LTP induction, indicating that any maturational decrease in excitability can be compensated by experience. These data reveal the importance of the animal's age for aDGC excitability, and emphasize their prolonged capability for plasticity during adulthood.