Mechanism of altered synaptic strength due to experience: relation to long-term potentiation

doi:10.1016/0006-8993(96)00707-X

Brain Research

Volume 736, Issues 1–2, 14 October 1996, Pages 243-250

https://doi.org/10.1016/0006-8993(96)00707-X Get rights and content

Abstract

An increase in medial perforant synaptic strength can be observed for hippocampal slices from rats exposed to environmental enrichment. The expression of enhanced synaptic strength exhibits properties similar to long-term potentiation (LTP), a physiological model of memory storage. Similarities include an increase in strength of the synaptic response in the absence of an altered paired-pulse ratio and an increase in the binding of the glutamate agonist α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate. Furthermore, environmental enrichment interacts with the mechanisms responsible for the induction of UP by inhibiting further increases in synaptic strength following LTP-inducing stimulation. The results provide evidence for experience-mediated influences on postsynaptic mechanisms regulating medial perforant path synaptic strength.

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Therapeutic efficacy of environmental enrichment for substance use disorders
2020, Pharmacology Biochemistry and Behavior
Citation Excerpt :
The literature provides an abundance of convincing evidence that EE can induce structural, biochemical and functional changes in the hippocampus, a limbic region highly implicated in learning and memory. For example, EE can alter neuronal behavior (i.e., excitatory post-synaptic potentials, long-term potentiation and long-term depression) in the hippocampus (Foster et al., 1996; Duffy et al., 2001; van Praag et al., 2005; Artola et al., 2006; Hosseiny et al., 2014). Other forms of EE-induced hippocampal neuroplasticity include: neurogenesis (Kempermann et al., 1997, 1998; Brown et al., 2003; van Praag et al., 2005), synaptogenesis (Sager et al., 2018; Cefis et al., 2019), alterations in BDNF (Neeper et al., 1996; Ickes et al., 2000; Vaynman et al., 2003; Zajac et al., 2010) and nerve growth factor (NGF) (Neeper et al., 1996; Pham et al., 1999; Hall and Savage, 2016), both of which support the viability and functions of neurons and are likely mediators of activity-dependent changes in the hippocampus.
Addiction to drug and alcohol is regarded as a major health problem worldwide for which available treatments show limited effectiveness. The biggest challenge remains to enhance the capacities of interventions to reduce craving, prevent relapse and promote long-term recovery. New strategies to meet these challenges are being explored. Findings from preclinical work suggest that environmental enrichment (EE) holds therapeutic potential for the treatment of substance use disorders, as demonstrated in a number of animal models of drug abuse. The EE intervention introduced after drug exposure leads to attenuation of compulsive drug taking, attenuation of the rewarding (and reinforcing) effects of drugs, reductions in control of behavior by drug cues, and, very importantly, relapse prevention. Clinical work also suggests that multidimensional EE interventions (involving physical activity, social interaction, vocational training, recreational and community involvement) might produce similar therapeutic effects, if implemented continuously and rigorously. In this review we survey preclinical and clinical studies assessing the efficacy of EE as a behavioral intervention for substance use disorders and address related challenges. We also review work providing empirical evidence for EE-induced neuroplasticity within the mesocorticolimbic system that is believed to contribute to the seemingly therapeutic effects of EE on drug and alcohol-related behaviors.
Social enrichment reverses the isolation-induced deficits of neuronal plasticity in the hippocampus of male rats
2019, Neuropharmacology
Environmental enrichment is known to improve brain plasticity and protect synaptic function from negative insults. In the present study we used the exposure to social enrichment to ameliorate the negative effect observed in post weaning isolated male rats in which neurotrophic factors, neurogenesis, neuronal dendritic trees and spines were altered markedly in the hippocampus. After the 4 weeks of post-weaning social isolation followed by 4 weeks of reunion, different neuronal growth markers as well as neuronal morphology were evaluated using different experimental approaches. Social enrichment restored the reduction of BDNF, NGF and Arc gene expression in the whole hippocampus of social isolated rats. This effect was paralleled by an increase in density and morphology of dendritic spines, as well as in neuronal tree arborisation in granule cells of the dentate gyrus. These changes were associated with a marked increase in neuronal proliferation and neurogenesis in the same hippocampal subregion that were reduced by social isolation stress. These results further suggest that the exposure to social enrichment, by abolishing the negative effect of social isolation stress on hippocampal plasticity, may improve neuronal resilience with a beneficial effect on cognitive function.
Environmental enrichment effects on synaptic and cellular physiology of hippocampal neurons
2019, Neuropharmacology
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”.
Nonsteroidal anti-inflammatory drug, indomethacin improves spatial memory and NMDA receptor function in aged animals
2018, Neurobiology of Aging
A redox-mediated decrease in N-methyl-D-aspartate (NMDA) receptor function contributes to psychiatric diseases and impaired cognition during aging. Inflammation provides a potential source of reactive oxygen species for inducing NMDA receptor hypofunction. The present study tested the hypothesis that the nonsteroidal anti-inflammatory drug indomethacin, which improves spatial episodic memory in aging rats, would enhance NMDA receptor function through a shift in the redox state. Male F344 young and aged rats were prescreened using a 1-day version of the water maze task. Animals were then treated with the indomethacin or vehicle, delivered in a frozen milk treat (orally, twice per day, 18 days), and retested on the water maze. Indomethacin treatment enhanced water maze performance. Hippocampal slices were prepared for examination of CA3-CA1 synaptic responses, long-term potentiation, and NMDA receptor-mediated synaptic responses. No effect of treatment was observed for the total synaptic response. Long-term potentiation magnitude and NMDA receptor input-output curves were enhanced for aged indomethacin-treated animals. To examine redox regulation of NMDA receptors, a second group of aged animals was treated with indomethacin or vehicle, and the effect of the reducing agent, dithiothreitol ([DTT], 0.5 mM) on NMDA receptor-mediated synaptic responses was evaluated. As expected, DTT increased the NMDA receptor response and the effect of DTT was reduced by indomethacin treatment. The results indicate that indomethacin acted to diminish the age-related and redox-mediated NMDA receptor hypofunction and suggest that inflammation contributes to cognitive impairment through an increase in redox stress.
Environmental enrichment improves hippocampal function in aged rats by enhancing learning and memory, LTP, and mGluR5-Homer1c activity
2018, Neurobiology of Aging
Previous studies from our laboratory have shown that environmental enrichment (EE) in young rats results in improved learning ability and enhanced metabotropic glutamate receptor–dependent long-term potentiation (mGluR-dependent LTP) resulting from sustained activation of p70S6 kinase. Here, we investigated whether 1-month EE is sufficient to improve hippocampus-dependent learning and memory and enhance hippocampal LTP in 23–24 month-old Fischer 344 male rats. Aged rats were housed in environmentally enriched, socially enriched, or standard housing conditions. We find that aged rats exposed to 1-month of EE demonstrate enhanced learning and memory relative to standard housed controls when tested in the Morris water maze and novel object recognition behavioral tasks. Furthermore, we find that environmentally enriched rats perform significantly better than socially enriched or standard housed rats in the radial-arm water maze and display enhanced mGluR5-dependent hippocampal LTP. Enhanced hippocampal function results from activity-dependent increases in the levels of mGluR5, Homer1c, and phospho-p70S6 kinase. These findings demonstrate that a short exposure of EE to aged rats can have significant effects on hippocampal function.
Environmental enrichment: Evidence for an unexpected therapeutic influence
2015, Experimental Neurology
Environmental enrichment produces wide-ranging effects in the brain at molecular, cellular, network, and behavioral levels. The changes in neuronal plasticity are driven by changes in neurotransmitters, neurotrophic factors, neuronal morphology, neurogenesis, network properties of the brain, and behavioral correlates of learning and memory. Exposure to an enriched environment has also demonstrated intriguing possibilities for treatment of a variety of neurodegenerative diseases including Huntington's disease, Alzheimer's disease, and Parkinson's disease. The effect of environmental enrichment in epilepsy, a neurodegenerative disorder with pathological neuronal plasticity, is of considerable interest. Recent reports of the effect of environmental enrichment in the Bassoon mutant mouse, a genetic model of early onset epilepsy, provides a significant addition to the literature in this area.

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Research reportMechanism of altered synaptic strength due to experience: relation to long-term potentiation

Abstract

Brain Res.

Behav. Neural Biol.

Behav. Neural Biol.

Neurosci. Lett.

Brain Res.

Neuron

Brain Res.

Brain Res.

Brain Res.

Brain Res

Brain Res.

Brain Res.

Behav. Neural Biol.

Potassium-induced long-term potentiation in area CA1 of the hippocampus involves phospholipase activation

Hippocampus

A synaptic model of memory: long-term potentiation in the hippocampus

Nature

Activation of AP-5 sensitive NMDA receptors is not required to induce LTP of synaptic transmission in the lateral perforant pathway

Eur. J. Neurosci.

Differential regulation of paired-pulse plasticity following LTP in the dentate gyros

Neuroreport

Mechanisms underlying induction of long-term potentiation in rat medial and lateral perforant paths in vitro

J. Neurophysiol.

Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus

J. Physiol. (Lond.)

Temporally distinct pre- and postsynaptic mechanisms maintain long-term potentiation

Nature

Inverted-U relationship between the level of peripheral corticosterone and the magnitude of prime burts potentiation

Hippocampus

Research report
Mechanism of altered synaptic strength due to experience: relation to long-term potentiation