Neuron-glia synapses in the brain

Dwight E Bergles, Ronald Jabs, Christian Steinhäuser

Research output: Contribution to journalArticle

Abstract

The ability to investigate the electrophysiological properties of individual cells in acute brain tissue led to the discovery that many glial cells have the capacity to respond rapidly to neuronal activity. In particular, a distinct class of neuroglial cells known as NG2 cells, which exhibit many of the properties that have been described for glial subtypes such as complex cells, polydendrocytes, synantocytes and GluR cells, express ionotropic receptors for glutamate and GABA. In both gray and white matter, NG2 cells form direct synaptic junctions with axons, which enable transient activation of these receptors. Electrophysiological analyses have shown that these neuron-glia synapses exhibit all the hallmarks of 'classical' neuron-neuron synapses, including rapid activation, quantized responses, facilitation and depression, and presynaptic inhibition. Electron microscopy indicates that axons form morphologically distinct junctions at discrete sites along processes of NG2 cells, suggesting that NG2 cells are an overt target of axonal projections. AMPA receptors expressed by NG2 cells exhibit varying degrees of Ca2+ permeability, depending on the brain region and stage of development, and in white matter NG2 cells have also been shown to express functional NMDA receptors. Ca2+ influx through AMPA receptors following repetitive stimulation can trigger long term potentiation of synaptic currents in NG2 cells. The expression of receptors with significant Ca2+ permeability may increase the susceptibility of NG2 cells to excitotoxic injury. Future studies using transgenic mice in which expression of receptors can be manipulated selectively in NG2 cells have to define the functions of this enigmatic neuron-glia signaling in the normal and diseased CNS.

Original languageEnglish (US)
Pages (from-to)130-137
Number of pages8
JournalBrain Research Reviews
Volume63
Issue number1-2
DOIs
StatePublished - May 2010

Fingerprint

Neuroglia
Synapses
Neurons
Brain
AMPA Receptors
Axons
Permeability
Ionotropic Glutamate Receptors
Long-Term Potentiation
Central Nervous System Diseases
N-Methyl-D-Aspartate Receptors
gamma-Aminobutyric Acid
Transgenic Mice
Electron Microscopy

Keywords

  • AMPA receptor
  • GABA receptor
  • Neuroglia
  • Neuron-glia synapses
  • NG2 cell
  • Synaptic transmission

ASJC Scopus subject areas

  • Neuroscience(all)
  • Clinical Neurology

Cite this

Neuron-glia synapses in the brain. / Bergles, Dwight E; Jabs, Ronald; Steinhäuser, Christian.

In: Brain Research Reviews, Vol. 63, No. 1-2, 05.2010, p. 130-137.

Research output: Contribution to journalArticle

Bergles, Dwight E ; Jabs, Ronald ; Steinhäuser, Christian. / Neuron-glia synapses in the brain. In: Brain Research Reviews. 2010 ; Vol. 63, No. 1-2. pp. 130-137.
@article{5cf48d16a0174a058b847b0492d9e7c5,
title = "Neuron-glia synapses in the brain",
abstract = "The ability to investigate the electrophysiological properties of individual cells in acute brain tissue led to the discovery that many glial cells have the capacity to respond rapidly to neuronal activity. In particular, a distinct class of neuroglial cells known as NG2 cells, which exhibit many of the properties that have been described for glial subtypes such as complex cells, polydendrocytes, synantocytes and GluR cells, express ionotropic receptors for glutamate and GABA. In both gray and white matter, NG2 cells form direct synaptic junctions with axons, which enable transient activation of these receptors. Electrophysiological analyses have shown that these neuron-glia synapses exhibit all the hallmarks of 'classical' neuron-neuron synapses, including rapid activation, quantized responses, facilitation and depression, and presynaptic inhibition. Electron microscopy indicates that axons form morphologically distinct junctions at discrete sites along processes of NG2 cells, suggesting that NG2 cells are an overt target of axonal projections. AMPA receptors expressed by NG2 cells exhibit varying degrees of Ca2+ permeability, depending on the brain region and stage of development, and in white matter NG2 cells have also been shown to express functional NMDA receptors. Ca2+ influx through AMPA receptors following repetitive stimulation can trigger long term potentiation of synaptic currents in NG2 cells. The expression of receptors with significant Ca2+ permeability may increase the susceptibility of NG2 cells to excitotoxic injury. Future studies using transgenic mice in which expression of receptors can be manipulated selectively in NG2 cells have to define the functions of this enigmatic neuron-glia signaling in the normal and diseased CNS.",
keywords = "AMPA receptor, GABA receptor, Neuroglia, Neuron-glia synapses, NG2 cell, Synaptic transmission",
author = "Bergles, {Dwight E} and Ronald Jabs and Christian Steinh{\"a}user",
year = "2010",
month = "5",
doi = "10.1016/j.brainresrev.2009.12.003",
language = "English (US)",
volume = "63",
pages = "130--137",
journal = "Brain Research Reviews",
issn = "0165-0173",
publisher = "Elsevier",
number = "1-2",

}

TY - JOUR

T1 - Neuron-glia synapses in the brain

AU - Bergles, Dwight E

AU - Jabs, Ronald

AU - Steinhäuser, Christian

PY - 2010/5

Y1 - 2010/5

N2 - The ability to investigate the electrophysiological properties of individual cells in acute brain tissue led to the discovery that many glial cells have the capacity to respond rapidly to neuronal activity. In particular, a distinct class of neuroglial cells known as NG2 cells, which exhibit many of the properties that have been described for glial subtypes such as complex cells, polydendrocytes, synantocytes and GluR cells, express ionotropic receptors for glutamate and GABA. In both gray and white matter, NG2 cells form direct synaptic junctions with axons, which enable transient activation of these receptors. Electrophysiological analyses have shown that these neuron-glia synapses exhibit all the hallmarks of 'classical' neuron-neuron synapses, including rapid activation, quantized responses, facilitation and depression, and presynaptic inhibition. Electron microscopy indicates that axons form morphologically distinct junctions at discrete sites along processes of NG2 cells, suggesting that NG2 cells are an overt target of axonal projections. AMPA receptors expressed by NG2 cells exhibit varying degrees of Ca2+ permeability, depending on the brain region and stage of development, and in white matter NG2 cells have also been shown to express functional NMDA receptors. Ca2+ influx through AMPA receptors following repetitive stimulation can trigger long term potentiation of synaptic currents in NG2 cells. The expression of receptors with significant Ca2+ permeability may increase the susceptibility of NG2 cells to excitotoxic injury. Future studies using transgenic mice in which expression of receptors can be manipulated selectively in NG2 cells have to define the functions of this enigmatic neuron-glia signaling in the normal and diseased CNS.

AB - The ability to investigate the electrophysiological properties of individual cells in acute brain tissue led to the discovery that many glial cells have the capacity to respond rapidly to neuronal activity. In particular, a distinct class of neuroglial cells known as NG2 cells, which exhibit many of the properties that have been described for glial subtypes such as complex cells, polydendrocytes, synantocytes and GluR cells, express ionotropic receptors for glutamate and GABA. In both gray and white matter, NG2 cells form direct synaptic junctions with axons, which enable transient activation of these receptors. Electrophysiological analyses have shown that these neuron-glia synapses exhibit all the hallmarks of 'classical' neuron-neuron synapses, including rapid activation, quantized responses, facilitation and depression, and presynaptic inhibition. Electron microscopy indicates that axons form morphologically distinct junctions at discrete sites along processes of NG2 cells, suggesting that NG2 cells are an overt target of axonal projections. AMPA receptors expressed by NG2 cells exhibit varying degrees of Ca2+ permeability, depending on the brain region and stage of development, and in white matter NG2 cells have also been shown to express functional NMDA receptors. Ca2+ influx through AMPA receptors following repetitive stimulation can trigger long term potentiation of synaptic currents in NG2 cells. The expression of receptors with significant Ca2+ permeability may increase the susceptibility of NG2 cells to excitotoxic injury. Future studies using transgenic mice in which expression of receptors can be manipulated selectively in NG2 cells have to define the functions of this enigmatic neuron-glia signaling in the normal and diseased CNS.

KW - AMPA receptor

KW - GABA receptor

KW - Neuroglia

KW - Neuron-glia synapses

KW - NG2 cell

KW - Synaptic transmission

UR - http://www.scopus.com/inward/record.url?scp=77952423247&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77952423247&partnerID=8YFLogxK

U2 - 10.1016/j.brainresrev.2009.12.003

DO - 10.1016/j.brainresrev.2009.12.003

M3 - Article

C2 - 20018210

AN - SCOPUS:77952423247

VL - 63

SP - 130

EP - 137

JO - Brain Research Reviews

JF - Brain Research Reviews

SN - 0165-0173

IS - 1-2

ER -