Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

In the thalamus of the rat the reversal potential of GABA-induced anion currents is more negative in relay cells than in neurones of the reticular nucleus (nRt) due to different chloride extrusion mechanisms operating in these cells. The distribution of KCl cotransporter type 2 (KCC2), the major neuronal chloride transporter that may underlie this effect, is unknown in the thalamus. In this study the precise regional and ultrastructural localization of KCC2 was examined in the thalamus using immunocytochemical methods. The neuropil of all relay nuclei was found to display intense KCC2 immunostaining to varying degrees. In sharp contrast, the majority of the nRt was negative for KCC2. In the anterior and dorsal part of the nRt, however, KCC2 immunostaining was similar to relay nuclei and parvalbumin and calretinin were found to colocalize with KCC2. At the ultrastructural level, KCC2 immunoreactivity was mainly located in the extrasynaptic membranes of thick and thin dendrites and the somata of relay cells but was also found in close association with asymmetrical synapses formed by cortical afferents. Quantitative evaluation of KCC2 distribution at the electron microscopic level demonstrated that the density of KCC2 did not correlate with dendritic diameter or synaptic coverage but is 1.7 times higher on perisynaptic membrane surfaces than on extrasynaptic membranes. Our data demonstrate that the regional distribution of KCC2 is compatible with the difference in GABA-A reversal potential between relay and reticular nuclei. At the ultrastructural level, abundant extrasynaptic KCC2 expression will probably play a role in the regulation of extrasynaptic GABA-A receptor-mediated inhibition.

Original languageEnglish
Pages (from-to)965-975
Number of pages11
JournalEuropean Journal of Neuroscience
Volume20
Issue number4
DOIs
Publication statusPublished - Aug 2004

Fingerprint

Thalamus
gamma-Aminobutyric Acid
Membranes
Chlorides
potassium-chloride symporters
Calbindin 2
Parvalbumins
Neuropil
Carisoprodol
GABA-A Receptors
Dendrites
Synapses
Anions
Electrons
Neurons

Keywords

  • GABA
  • KCl cotransporter
  • Rat
  • Reticular nucleus
  • Thalamus

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei. / Barthó, P.; Payne, J. A.; Freund, T.; Acsády, L.

In: European Journal of Neuroscience, Vol. 20, No. 4, 08.2004, p. 965-975.

Research output: Contribution to journalArticle

@article{d560ae4c49e74f29906643ee69d8da11,
title = "Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei",
abstract = "In the thalamus of the rat the reversal potential of GABA-induced anion currents is more negative in relay cells than in neurones of the reticular nucleus (nRt) due to different chloride extrusion mechanisms operating in these cells. The distribution of KCl cotransporter type 2 (KCC2), the major neuronal chloride transporter that may underlie this effect, is unknown in the thalamus. In this study the precise regional and ultrastructural localization of KCC2 was examined in the thalamus using immunocytochemical methods. The neuropil of all relay nuclei was found to display intense KCC2 immunostaining to varying degrees. In sharp contrast, the majority of the nRt was negative for KCC2. In the anterior and dorsal part of the nRt, however, KCC2 immunostaining was similar to relay nuclei and parvalbumin and calretinin were found to colocalize with KCC2. At the ultrastructural level, KCC2 immunoreactivity was mainly located in the extrasynaptic membranes of thick and thin dendrites and the somata of relay cells but was also found in close association with asymmetrical synapses formed by cortical afferents. Quantitative evaluation of KCC2 distribution at the electron microscopic level demonstrated that the density of KCC2 did not correlate with dendritic diameter or synaptic coverage but is 1.7 times higher on perisynaptic membrane surfaces than on extrasynaptic membranes. Our data demonstrate that the regional distribution of KCC2 is compatible with the difference in GABA-A reversal potential between relay and reticular nuclei. At the ultrastructural level, abundant extrasynaptic KCC2 expression will probably play a role in the regulation of extrasynaptic GABA-A receptor-mediated inhibition.",
keywords = "GABA, KCl cotransporter, Rat, Reticular nucleus, Thalamus",
author = "P. Barth{\'o} and Payne, {J. A.} and T. Freund and L. Acs{\'a}dy",
year = "2004",
month = "8",
doi = "10.1111/j.1460-9568.2004.03562.x",
language = "English",
volume = "20",
pages = "965--975",
journal = "European Journal of Neuroscience",
issn = "0953-816X",
publisher = "Wiley-Blackwell",
number = "4",

}

TY - JOUR

T1 - Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei

AU - Barthó, P.

AU - Payne, J. A.

AU - Freund, T.

AU - Acsády, L.

PY - 2004/8

Y1 - 2004/8

N2 - In the thalamus of the rat the reversal potential of GABA-induced anion currents is more negative in relay cells than in neurones of the reticular nucleus (nRt) due to different chloride extrusion mechanisms operating in these cells. The distribution of KCl cotransporter type 2 (KCC2), the major neuronal chloride transporter that may underlie this effect, is unknown in the thalamus. In this study the precise regional and ultrastructural localization of KCC2 was examined in the thalamus using immunocytochemical methods. The neuropil of all relay nuclei was found to display intense KCC2 immunostaining to varying degrees. In sharp contrast, the majority of the nRt was negative for KCC2. In the anterior and dorsal part of the nRt, however, KCC2 immunostaining was similar to relay nuclei and parvalbumin and calretinin were found to colocalize with KCC2. At the ultrastructural level, KCC2 immunoreactivity was mainly located in the extrasynaptic membranes of thick and thin dendrites and the somata of relay cells but was also found in close association with asymmetrical synapses formed by cortical afferents. Quantitative evaluation of KCC2 distribution at the electron microscopic level demonstrated that the density of KCC2 did not correlate with dendritic diameter or synaptic coverage but is 1.7 times higher on perisynaptic membrane surfaces than on extrasynaptic membranes. Our data demonstrate that the regional distribution of KCC2 is compatible with the difference in GABA-A reversal potential between relay and reticular nuclei. At the ultrastructural level, abundant extrasynaptic KCC2 expression will probably play a role in the regulation of extrasynaptic GABA-A receptor-mediated inhibition.

AB - In the thalamus of the rat the reversal potential of GABA-induced anion currents is more negative in relay cells than in neurones of the reticular nucleus (nRt) due to different chloride extrusion mechanisms operating in these cells. The distribution of KCl cotransporter type 2 (KCC2), the major neuronal chloride transporter that may underlie this effect, is unknown in the thalamus. In this study the precise regional and ultrastructural localization of KCC2 was examined in the thalamus using immunocytochemical methods. The neuropil of all relay nuclei was found to display intense KCC2 immunostaining to varying degrees. In sharp contrast, the majority of the nRt was negative for KCC2. In the anterior and dorsal part of the nRt, however, KCC2 immunostaining was similar to relay nuclei and parvalbumin and calretinin were found to colocalize with KCC2. At the ultrastructural level, KCC2 immunoreactivity was mainly located in the extrasynaptic membranes of thick and thin dendrites and the somata of relay cells but was also found in close association with asymmetrical synapses formed by cortical afferents. Quantitative evaluation of KCC2 distribution at the electron microscopic level demonstrated that the density of KCC2 did not correlate with dendritic diameter or synaptic coverage but is 1.7 times higher on perisynaptic membrane surfaces than on extrasynaptic membranes. Our data demonstrate that the regional distribution of KCC2 is compatible with the difference in GABA-A reversal potential between relay and reticular nuclei. At the ultrastructural level, abundant extrasynaptic KCC2 expression will probably play a role in the regulation of extrasynaptic GABA-A receptor-mediated inhibition.

KW - GABA

KW - KCl cotransporter

KW - Rat

KW - Reticular nucleus

KW - Thalamus

UR - http://www.scopus.com/inward/record.url?scp=4344691956&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=4344691956&partnerID=8YFLogxK

U2 - 10.1111/j.1460-9568.2004.03562.x

DO - 10.1111/j.1460-9568.2004.03562.x

M3 - Article

C2 - 15305865

AN - SCOPUS:4344691956

VL - 20

SP - 965

EP - 975

JO - European Journal of Neuroscience

JF - European Journal of Neuroscience

SN - 0953-816X

IS - 4

ER -