Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus

Sari E Lauri, Mikael Segerstråle, Aino Vesikansa, Francois Maingret, Christophe Mulle, Graham L Collingridge, John T. R Isaac, Tomi Taira

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

Sammanfattning

Kainate receptors (KARs) are highly expressed throughout the neonatal brain, but their function during development is unclear. Here, we show that the maturation of the hippocampus is associated with a switch in the functional role of presynaptic KARs. In a developmental period restricted to the first postnatal week, endogenous L-glutamate tonically activates KARs at CA3 glutamatergic synapses to regulate release in an action potential-independent manner. At synapses onto pyramidal cells, KARs inhibit glutamate release via a G-protein and PKC-dependent mechanism. In contrast, at glutamatergic terminals onto CA3 interneurons, presynaptic KARs can facilitate release in a G-protein-independent mechanism. In both cell types, however, KAR activation strongly upregulates inhibitory transmission. We show that, through the interplay of these novel diverse mechanisms, KARs strongly regulate the characteristic synchronous network activity observed in the neonatal hippocampus. By virtue of this, KARsare likely to play a central role in the development of hippocampal synaptic circuits.
Originalspråkengelska
TidskriftJournal of Neuroscience
Volym25
Utgåva18
Sidor (från-till)4473-4484
Antal sidor12
ISSN0270-6474
DOI
StatusPublicerad - 2005
MoE-publikationstypA1 Tidskriftsartikel-refererad

Vetenskapsgrenar

  • 311 Basmedicin
  • 118 Biovetenskaper
  • 515 Psykologi

Citera det här

Lauri, Sari E ; Segerstråle, Mikael ; Vesikansa, Aino ; Maingret, Francois ; Mulle, Christophe ; Collingridge, Graham L ; Isaac, John T. R ; Taira, Tomi. / Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. I: Journal of Neuroscience. 2005 ; Vol. 25, Nr. 18. s. 4473-4484.
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abstract = "Kainate receptors (KARs) are highly expressed throughout the neonatal brain, but their function during development is unclear. Here, we show that the maturation of the hippocampus is associated with a switch in the functional role of presynaptic KARs. In a developmental period restricted to the first postnatal week, endogenous L-glutamate tonically activates KARs at CA3 glutamatergic synapses to regulate release in an action potential-independent manner. At synapses onto pyramidal cells, KARs inhibit glutamate release via a G-protein and PKC-dependent mechanism. In contrast, at glutamatergic terminals onto CA3 interneurons, presynaptic KARs can facilitate release in a G-protein-independent mechanism. In both cell types, however, KAR activation strongly upregulates inhibitory transmission. We show that, through the interplay of these novel diverse mechanisms, KARs strongly regulate the characteristic synchronous network activity observed in the neonatal hippocampus. By virtue of this, KARsare likely to play a central role in the development of hippocampal synaptic circuits.",
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Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. / Lauri, Sari E; Segerstråle, Mikael; Vesikansa, Aino; Maingret, Francois; Mulle, Christophe; Collingridge, Graham L; Isaac, John T. R; Taira, Tomi.

I: Journal of Neuroscience, Vol. 25, Nr. 18, 2005, s. 4473-4484.

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

TY - JOUR

T1 - Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus

AU - Lauri, Sari E

AU - Segerstråle, Mikael

AU - Vesikansa, Aino

AU - Maingret, Francois

AU - Mulle, Christophe

AU - Collingridge, Graham L

AU - Isaac, John T. R

AU - Taira, Tomi

PY - 2005

Y1 - 2005

N2 - Kainate receptors (KARs) are highly expressed throughout the neonatal brain, but their function during development is unclear. Here, we show that the maturation of the hippocampus is associated with a switch in the functional role of presynaptic KARs. In a developmental period restricted to the first postnatal week, endogenous L-glutamate tonically activates KARs at CA3 glutamatergic synapses to regulate release in an action potential-independent manner. At synapses onto pyramidal cells, KARs inhibit glutamate release via a G-protein and PKC-dependent mechanism. In contrast, at glutamatergic terminals onto CA3 interneurons, presynaptic KARs can facilitate release in a G-protein-independent mechanism. In both cell types, however, KAR activation strongly upregulates inhibitory transmission. We show that, through the interplay of these novel diverse mechanisms, KARs strongly regulate the characteristic synchronous network activity observed in the neonatal hippocampus. By virtue of this, KARsare likely to play a central role in the development of hippocampal synaptic circuits.

AB - Kainate receptors (KARs) are highly expressed throughout the neonatal brain, but their function during development is unclear. Here, we show that the maturation of the hippocampus is associated with a switch in the functional role of presynaptic KARs. In a developmental period restricted to the first postnatal week, endogenous L-glutamate tonically activates KARs at CA3 glutamatergic synapses to regulate release in an action potential-independent manner. At synapses onto pyramidal cells, KARs inhibit glutamate release via a G-protein and PKC-dependent mechanism. In contrast, at glutamatergic terminals onto CA3 interneurons, presynaptic KARs can facilitate release in a G-protein-independent mechanism. In both cell types, however, KAR activation strongly upregulates inhibitory transmission. We show that, through the interplay of these novel diverse mechanisms, KARs strongly regulate the characteristic synchronous network activity observed in the neonatal hippocampus. By virtue of this, KARsare likely to play a central role in the development of hippocampal synaptic circuits.

KW - 311 Basic medicine

KW - 118 Biological sciences

KW - 515 Psychology

U2 - 10.1523/JNEUROSCI.4050-04.2005

DO - 10.1523/JNEUROSCI.4050-04.2005

M3 - Article

VL - 25

SP - 4473

EP - 4484

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

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ER -