Enhanced intrinsic excitability and EPSP-spike coupling accompany enriched environment-induced facilitation of LTP in hippocampal CA1 pyramidal neurons

Dec 14, 2011Journal of neurophysiology

Improved nerve cell responsiveness and signal linking in the learning area of the brain after enriched environment exposure

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Abstract

Environmental enrichment (EE) increased action potential firing in hippocampal CA1 pyramidal neurons.

EE enhanced contextual fear memory and dendritic spine density on CA1 cells.
LTP was facilitated at Schaffer collateral inputs to CA1 pyramidal neurons following EE.
EE increased the frequency of miniature excitatory postsynaptic currents without affecting their amplitude.
Presynaptic release probability was not altered by EE, as indicated by paired-pulse ratios.
CA1 neurons exhibited reduced spiking threshold and after-hyperpolarization amplitude with EE.
The increase in excitability from EE allowed for more action potentials to be fired with the same-sized excitatory postsynaptic potential.

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Environmental enrichment (EE) is a well-established paradigm for studying naturally occurring changes in synaptic efficacy in the hippocampus that underlie experience-induced modulation of learning and memory in rodents. Earlier research on the effects of EE on hippocampal plasticity focused on long-term potentiation (LTP). Whereas many of these studies investigated changes in synaptic weight, little is known about potential contributions of neuronal excitability to EE-induced plasticity. Here, using whole-cell recordings in hippocampal slices, we address this gap by analyzing the impact of EE on both synaptic plasticity and intrinsic excitability of hippocampal CA1 pyramidal neurons. Consistent with earlier reports, EE increased contextual fear memory and dendritic spine density on CA1 cells. Furthermore, EE facilitated LTP at Schaffer collateral inputs to CA1 pyramidal neurons. Analysis of the underlying causes for enhanced LTP shows EE to increase the frequency but not amplitude of miniature excitatory postsynaptic currents. However, presynaptic release probability, assayed using paired-pulse ratios and use-dependent block of N-methyl-d-aspartate receptor currents, was not affected. Furthermore, CA1 neurons fired more action potentials (APs) in response to somatic depolarization, as well as during the induction of LTP. EE also reduced spiking threshold and after-hyperpolarization amplitude. Strikingly, this EE-induced increase in excitability caused the same-sized excitatory postsynaptic potential to fire more APs. Together, these findings suggest that EE may enhance the capacity for plasticity in CA1 neurons, not only by strengthening synapses but also by enhancing their efficacy to fire spikes-and the two combine to act as an effective substrate for amplifying LTP.

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Enhanced intrinsic excitability and EPSP-spike coupling accompany enriched environment-induced facilitation of LTP in hippocampal CA1 pyramidal neurons

Abstract

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