TY - JOUR
T1 - Functional coupling between neurons and glia
AU - Alvarez-Maubecin, Veronica
AU - García-Hernández, Fernando
AU - Williams, John T.
AU - Van Bockstaele, Elisabeth J.
PY - 2000/6/1
Y1 - 2000/6/1
N2 - Neuronal-glial interactions play an important role in information processing in the CNS. Previous studies have indicated that electrotonic coupling between locus ceruleus (LC) neurons is involved in synchronizing the spontaneous activity. The results of the present study extend the functional electrotonic coupling to interactions between neurons and glia. Spontaneous oscillations in the membrane potential were observed in a subset of glia. These oscillations were synchronous with the firing of neurons, insensitive to transmitter receptor antagonists and disrupted by carbenoxolone, a gap junction blocker. Hyperpolarization of neurons with [Met] 5enkephalin blocked the oscillations in gila. Selective depolarization of glia with a glutamate transporter substrate (L-α-aminoadipic acid) increased the neuronal firing rate, suggesting that changes in the membrane potential of glia can modulate neuronal excitability through heterocellular coupling. Dye- coupling experiments further confirmed that small molecules could be transferred through gap junctions between these distinct cell types. No dye transfer was observed between neurons and oligodendrocytes or between astrocytes and oligodendrocytes, suggesting that the junctional communication was specific for astrocytes and neurons. Finally, immunoelectron microscopy studies established that connexins, the proteins that form gap junctions, were present on portions of the plasmalemma, bridging the cytoplasm of neurons and glia in LC. This heterocellular coupling extends the mechanisms by which glia participate in the network properties of the LC in which the degree of coupling is thought to influence cognitive performance.
AB - Neuronal-glial interactions play an important role in information processing in the CNS. Previous studies have indicated that electrotonic coupling between locus ceruleus (LC) neurons is involved in synchronizing the spontaneous activity. The results of the present study extend the functional electrotonic coupling to interactions between neurons and glia. Spontaneous oscillations in the membrane potential were observed in a subset of glia. These oscillations were synchronous with the firing of neurons, insensitive to transmitter receptor antagonists and disrupted by carbenoxolone, a gap junction blocker. Hyperpolarization of neurons with [Met] 5enkephalin blocked the oscillations in gila. Selective depolarization of glia with a glutamate transporter substrate (L-α-aminoadipic acid) increased the neuronal firing rate, suggesting that changes in the membrane potential of glia can modulate neuronal excitability through heterocellular coupling. Dye- coupling experiments further confirmed that small molecules could be transferred through gap junctions between these distinct cell types. No dye transfer was observed between neurons and oligodendrocytes or between astrocytes and oligodendrocytes, suggesting that the junctional communication was specific for astrocytes and neurons. Finally, immunoelectron microscopy studies established that connexins, the proteins that form gap junctions, were present on portions of the plasmalemma, bridging the cytoplasm of neurons and glia in LC. This heterocellular coupling extends the mechanisms by which glia participate in the network properties of the LC in which the degree of coupling is thought to influence cognitive performance.
KW - Connexins
KW - Electrotonic coupling
KW - Gap junction
KW - Membrane potential oscillations
KW - Neuronal-glial interactions
KW - Noradrenergic neurons
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U2 - 10.1523/jneurosci.20-11-04091.2000
DO - 10.1523/jneurosci.20-11-04091.2000
M3 - Article
C2 - 10818144
AN - SCOPUS:17344389332
SN - 0270-6474
VL - 20
SP - 4091
EP - 4098
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 11
ER -