Enriched Environment Modulates Sharp Wave-Ripple (SPW-R) Activity in Hippocampal Slices.

Lucie Landeck,Martin E Kaiser,Andreas Draguhn,Dimitri Hefter,Martin Both

doi:10.3389/fncir.2021.758939

Abstract

Behavioral flexibility depends on neuronal plasticity which forms and adapts the central nervous system in an experience-dependent manner. Thus, plasticity depends on interactions between the organism and its environment. A key experimental paradigm for studying this concept is the exposure of rodents to an enriched environment (EE), followed by studying differences to control animals kept under standard conditions (SC). While multiple changes induced by EE have been found at the cellular-molecular and cognitive-behavioral levels, little is known about EE-dependent alterations at the intermediate level of network activity. We, therefore, studied spontaneous network activity in hippocampal slices from mice which had previously experienced EE for 10–15 days. Compared to control animals from standard conditions (SC) and mice with enhanced motor activity (MC) we found several differences in sharp wave-ripple complexes (SPW-R), a memory-related activity pattern. Sharp wave amplitude, unit firing during sharp waves, and the number of superimposed ripple cycles were increased in tissue from the EE group. On the other hand, spiking precision with respect to the ripple oscillations was reduced. Recordings from single pyramidal cells revealed a reduction in synaptic inhibition during SPW-R together with a reduced inhibition-excitation ratio. The number of inhibitory neurons, including parvalbumin-positive interneurons, was unchanged. Altered activation or efficacy of synaptic inhibition may thus underlie changes in memory-related network activity patterns which, in turn, may be important for the cognitive-behavioral effects of EE exposure.

Highlights

Complex nervous systems support experience-dependent learning, lending behavioral flexibility and individuality to animals
We focused on a particular pattern of network activity in the hippocampus called sharp wave-ripple complexes (SPWR)
Field potentials in CA1 and CA3, respectively, revealed spontaneous network events resembling sharp wave-ripple complexes (SPW-R, Maier et al, 2003, Figure 1A right panel)

Summary

Introduction

Complex nervous systems support experience-dependent learning, lending behavioral flexibility and individuality to animals. These, and multiple subsequent studies revealed a plethora of changes induced by exposure to a more challenging environment than the standard laboratory conditions which, arguably, may be characterized as a paradigm for sensory, motor, and social deprivation (Consorti et al, 2019; Rogers et al, 2019). Most of these changes converge on mechanisms increasing the adaptive plasticity of the brain, in line with the positive effects of EE on behavioral flexibility and experience-dependent learning (Donato et al, 2013; Ball et al, 2019; Gelfo, 2019). The cognitive-behavioral effects of EE include improved spatial memory formation (Leggio et al, 2005; Bennett et al, 2006; Eckert et al, 2010), highlighting the importance of hippocampal and neocortical networks which are, strongly affected by EE

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