High firing rate of neonatal hippocampal interneurons is caused by attenuation of afterhyperpolarizing potassium currents by tonically active kainate receptors

In the neonatal hippocampus, the activity of interneurons shapes early network bursts that are important for the establishment of neuronal connectivity. However, mechanisms controlling the firing of immature interneurons remain elusive. We now show that the spontaneous firing rate of CA3 stratum luc...

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Bibliographic Details
Published in:The Journal of neuroscience 2010-05, Vol.30 (19), p.6507-6514
Main Authors: Segerstråle, Mikael, Juuri, Juuso, Lanore, Frédéric, Piepponen, Petteri, Lauri, Sari E, Mulle, Christophe, Taira, Tomi
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Animals, Newborn
CA3 Region, Hippocampal - growth & development
CA3 Region, Hippocampal - physiology
Glutamic Acid - metabolism
GTP-Binding Proteins - metabolism
In Vitro Techniques
Interneurons - physiology
Life Sciences
Membrane Potentials - physiology
Mice
Mice, Inbred C57BL
Mice, Knockout
Neural Pathways - physiology
Neurons and Cognition
Patch-Clamp Techniques
Potassium - metabolism
Receptors, Kainic Acid - deficiency
Receptors, Kainic Acid - genetics
Receptors, Kainic Acid - metabolism
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Summary:In the neonatal hippocampus, the activity of interneurons shapes early network bursts that are important for the establishment of neuronal connectivity. However, mechanisms controlling the firing of immature interneurons remain elusive. We now show that the spontaneous firing rate of CA3 stratum lucidum interneurons markedly decreases during early postnatal development because of changes in the properties of GluK1 (formerly known as GluR5) subunit-containing kainate receptors (KARs). In the neonate, activation of KARs by ambient glutamate exerts a tonic inhibition of the medium-duration afterhyperpolarization (mAHP) by a G-protein-dependent mechanism, permitting a high interneuronal firing rate. During development, the amplitude of the apamine-sensitive K+ currents responsible for the mAHP increases dramatically because of decoupling between KAR activation and mAHP modulation, leading to decreased interneuronal firing. The developmental shift in the KAR function and its consequences on interneuronal activity are likely to have a fundamental role in the maturation of the synchronous neuronal oscillations typical for adult hippocampal circuitry.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.4856-09.2010