Ethanol modulation of synaptic plasticity

doi:10.1016/j.neuropharm.2010.12.028

Neuropharmacology

Volume 61, Issue 7, December 2011, Pages 1097-1108

https://doi.org/10.1016/j.neuropharm.2010.12.028 Get rights and content

Abstract

Synaptic plasticity in the most general terms represents the flexibility of neurotransmission in response to neuronal activity. Synaptic plasticity is essential both for the moment-by-moment modulation of neural activity in response to dynamic environmental cues and for long-term learning and memory formation. These temporal characteristics are served by an array of pre- and post-synaptic mechanisms that are frequently modulated by ethanol exposure. This modulation likely makes significant contributions to both alcohol abuse and dependence. In this review, I discuss the modulation of both short-term and long-term synaptic plasticity in the context of specific ethanol-sensitive cellular substrates. A general discussion of the available preclinical, animal-model based neurophysiology literature provides a comparison between results from in vitro and in vivo studies. Finally, in the context of alcohol abuse and dependence, the review proposes potential behavioral contributions by ethanol modulation of plasticity.

This article is part of a Special Issue entitled ‘Synaptic Plasticity and Addiction’.

Highlights

► This work reviews data describing ethanol modulation of synaptic plasticity. ► Topics include acute ethanol alterations of short- and long-term plasticity. ► Modulation by in vivo and chronic ethanol exposure is also discussed. ► The behavioral impact of ethanol–plasticity interaction is highlighted.

Section snippets

Introduction – what is synaptic plasticity?

The chemical synapse allows both the complex integration of information among neurons within a brain region as well as distant communication between distinct areas. Fine-tuning the strength of these synapses, referred to synaptic plasticity, provides flexibility and ultimately regulates behavioral outcomes associated with specific neural circuits. For example, synaptic plasticity in brain regions like the hippocampus or amygdala has been defined as making critical cellular contributions to

Short-term plasticity

Short-term synaptic plasticity has historically been thought of as a presynaptic phenomena related to calcium homeostasis in the synaptic terminal. At least on a time-frame relative to the frequency of action potentials invading a presynaptic terminal, calcium concentrations can raise substantially above resting levels due to incomplete clearance during closely-spaced or trains of presynaptic depolarizations (Zucker and Regehr, 2002). The resulting ’residual calcium’ can increase

Ethanol exposure in vivo and the plasticity of plasticity

The acute ethanol sensitivity of neurotransmitter receptors and synaptic plasticity itself quickly led to investigations of the effects of in vivo ethanol exposure and withdrawal. With a few notable, more recent exceptions (see below), much of this literature has focused on chronic ethanol exposure paradigms. And, much of the early work in this area focused on neurotransmitter receptors and system that were known to be sensitive to acute ethanol in vitro. For example, chronic exposure of mice

Conclusions & perspectives

The in vitro modulation of synaptic plasticity can be characterized by a wide array of cellular mechanisms associated with ethanol intoxication. The facilitation of short-term GABAergic plasticity and inhibition of glutamatergic short-term plasticity for example support a growing literature suggesting that acute ethanol tips the balance between GABA and glutamate neurotransmission towards the inhibitory systems. On another level, short-term synaptic plasticity serves as a “frequency filter”

Acknowledgements

This work was supported by grants from the National Institutes of Health/National Institute on Alcohol Abuse and Alcoholism (R01 AA014445 and P01 AA017056). I am grateful to Dr. Marvin Diaz and Mr. Dan Christian for their constructive comments.

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Invited reviewEthanol modulation of synaptic plasticity

Abstract

Highlights

Section snippets

Introduction – what is synaptic plasticity?

Short-term plasticity

Ethanol exposure in vivo and the plasticity of plasticity

Conclusions & perspectives

Acknowledgements

Trends. Neurosci.

Neurosci. Biobehav. Rev.

Neuroscience

Brain. Res.

Alcohol

Brain. Res.

Neuropharmacology

Int. Rev. Neurobiol.

Curr. Biol.

Brain. Res.

Brain. Res. Mol. Brain. Res.

J. Physiol. Paris

Brain. Res.

Trends. Neurosci.

Neuroscience

Trends. Cogn. Sci.

Neuroscience

Brain. Res.

Neuroscience

Neuroscience

Neuropharmacology

Neurotoxicol. Teratol.

Neuropharmacology

Neuron

Neuropharmacology

Alcohol

Int. J. Dev. Neurosci.

Neuropharmacology

Neuropharmacology

Neuron

Neuron

Neurobiol. Learn. Mem.

Dopamine modulation of excitatory currents in the striatum is dictated by the expression of D1 or D2 receptors and modified by endocannabinoids

Eur. J. Neurosci.

Mechanisms regulating GABAergic inhibitory transmission in the basolateral amygdala: implications for epilepsy and anxiety disorders

Amino. Acids.

Protein kinase C epsilon mediation of CRF- and ethanol-induced GABA release in central amygdala

Proc. Natl. Acad. Sci. U S A

Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action

Neuropsychopharmacology

Alcohol impairs long-term depression at the cerebellar parallel fiber-Purkinje cell synapse

J. Neurophysiol.

Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy

Hippocampus

Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning

J. Neurosci.

Effects of ethanol and other drugs on excitatory and inhibitory neurotransmission in the crayfish

J. Neurophysiol.

Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area

J. Neurosci.

Previous experience of ethanol withdrawal increases withdrawal-induced c-fos expression in limbic areas, but not withdrawal-induced anxiety and prevents withdrawal-induced elevations in plasma corticosterone

Psychopharmacology (Berl)

The physiological role of kainate receptors in the amygdala

Mol. Neurobiol.

Fetal alcohol exposure alters neurosteroid levels in the developing rat brain

J. Neurochem.

Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors

J. Neurosci.

Alcohol potently modulates climbing fiber-->Purkinje neuron synapses: role of metabotropic glutamate receptors

J. Neurosci.

Protein kinase Cdelta regulates ethanol intoxication and enhancement of GABA-stimulated tonic current

J. Neurosci.

A conceptualization of integrated actions of ethanol contributing to its GABAmimetic profile: a commentary

Neuropsychopharmacology

Brain regional differences in the effect of ethanol on GABA release from presynaptic terminals

J. Pharmacol. Exp. Ther.

Ethanol antagonizes kainate receptor-mediated inhibition of evoked GABA(A) inhibitory postsynaptic currents in the rat hippocampal CA1 region

J. Pharmacol. Exp. Ther.

Invited review
Ethanol modulation of synaptic plasticity