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

Research output: Contribution to journalArticleScientificpeer-review

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.
Original languageEnglish
JournalJournal of Neuroscience
Volume25
Issue number18
Pages (from-to)4473-4484
Number of pages12
ISSN0270-6474
DOIs
Publication statusPublished - 2005
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 311 Basic medicine
  • 118 Biological sciences
  • 515 Psychology

Cite this

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. In: Journal of Neuroscience. 2005 ; Vol. 25, No. 18. pp. 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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author = "Lauri, {Sari E} and Mikael Segerstr{\aa}le and Aino Vesikansa and Francois Maingret and Christophe Mulle and Collingridge, {Graham L} and Isaac, {John T. R} and Tomi Taira",
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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.

In: Journal of Neuroscience, Vol. 25, No. 18, 2005, p. 4473-4484.

Research output: Contribution to journalArticleScientificpeer-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.

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