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 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.
Segerstråle
Mikael
M
Neuroscience Center and Department of Biosciences, University of Helsinki, FIN-00014 Helsinki, Finland.
Juuri
Juuso
J
Lanore
Frédéric
F
Piepponen
Petteri
P
Lauri
Sari E
SE
Mulle
Christophe
C
Taira
Tomi
T
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D000831:Animals, Newborn; D056654:CA3 Region, Hippocampal / Q000254:growth & development* / Q000502:physiology*; D019204:GTP-Binding Proteins / Q000378:metabolism; D018698:Glutamic Acid / Q000378:metabolism; D066298:In Vitro Techniques; D007395:Interneurons / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D051379:Mice; D008810:Mice, Inbred C57BL; D018345:Mice, Knockout; D009434:Neural Pathways / Q000502:physiology; D018408:Patch-Clamp Techniques; D011188:Potassium / Q000378:metabolism*; D018092:Kainic Acid Receptors / Q000172:deficiency / Q000235:genetics / Q000378:metabolism*
D019204:GTP-Binding Proteins; D018698:Glutamic Acid; D011188:Potassium; D018092:Kainic Acid Receptors
J Neurophysiol. 2006 Dec;96(6):3028-41
16971683
Trends Neurosci. 2004 Jul;27(7):422-7
15219742
J Neurophysiol. 2000 Jun;83(6):3453-61
10848561
J Neurophysiol. 2001 May;85(5):1986-97
11353015
Neuron. 2003 Jul 31;39(3):543-53
12895426
J Neurophysiol. 2000 Jan;83(1):359-66
10634879
Trends Neurosci. 1996 Apr;19(4):150-4
8658599
Nat Rev Neurosci. 2001 Jan;2(1):11-23
11253355
J Neurosci. 2000 Feb 1;20(3):1170-8
10648721
Neuropharmacology. 2007 May;52(6):1354-65
17395219
Neuron. 1998 Jun;20(6):1211-8
9655508
Prog Neurobiol. 2002 Apr;66(5):345-53
12015199
Neuron. 2006 May 4;50(3):415-29
16675396
Neuron. 2002 Mar 28;34(1):107-14
11931745
J Neurosci. 2004 May 12;24(19):4530-4
15140923
J Neurosci. 2006 Apr 19;26(16):4178-87
16624938
J Biol Chem. 1991 Aug 25;266(24):15771-81
1874734
Nat Neurosci. 2001 Jun;4(6):612-20
11369942
J Physiol. 2005 Jan 1;562(Pt 1):199-203
15539395
Neuron. 2000 Nov;28(2):475-84
11144357
Mol Cell Neurosci. 2003 Jan;22(1):107-17
12595243
J Physiol. 1995 Nov 1;488 ( Pt 3):661-72
8576856
J Physiol. 2007 Jun 1;581(Pt 2):505-14
17347263
J Neurophysiol. 2001 May;85(5):1941-51
11353011
J Neurosci. 2005 May 4;25(18):4473-84
15872094
J Neurosci. 2005 Dec 14;25(50):11710-8
16354929
J Neurosci. 2009 Sep 9;29(36):11294-303
19741136