Low expression of Kv7/M channels facilitates intrinsic and network bursting in the developing rat hippocampus.
Early in development, network activity in the hippocampus is characterized by recurrent synchronous bursts, whose cellular correlates are giant depolarizing potentials (GDPs). The propensity for generating GDPs is attributed to GABAergic synaptic transmission being depolarizing and excitatory in neonatal neurons. However, developmental regulation of intrinsic conductances may also influence GDPs generation. A likely candidate is the non-inactivating, low-threshold, muscarinic-sensitive K(+) current (M current; I(m)), which down-regulates intrinsic bursting activity in adult hippocampal pyramidal neurons. Western blot analysis of homogenates of the CA3 hippocampal region showed that expression of the Kv7.2 subunit, one of the constituents of neuronal M channels, is weak in neonatal neurons, and markedly increases after the first postnatal week. Likewise, the density of I(m) was very low in neonatal CA3 pyramidal cells and increased later on. Spontaneously occurring intrinsic bursts in neonatal neurons were longer and more robust, and recurred more regularly, than in juvenile neurons. The I(m) blocker linopirdine only mildly affected intrinsic bursting in neonatal neurons, but strongly facilitated and regularized it in juvenile neurons. We conclude that the low expression of Kv7/M channels and the depolarizing action of GABA early after birth enhance intrinsic bursting and neuronal synchronization leading to generation of GDPs within the hippocampal network.
Safiulina
Victoria F
VF
Neuroscience Programme, International School for Advanced Studies, Trieste, Italy.
Zacchi
Paola
P
Taglialatela
Maurizio
M
Yaari
Yoel
Y
Cherubini
Enrico
E
D000200:Action Potentials / Q000187:drug effects; D000818:Animals; D000831:Animals, Newborn; D002219:Carbamates / Q000494:pharmacology; D006624:Hippocampus / Q000166:cytology / Q000187:drug effects / Q000254:growth & development / Q000378:metabolism*; D066298:In Vitro Techniques; D007211:Indoles / Q000494:pharmacology; D051658:KCNQ2 Potassium Channel / Q000819:agonists / Q000037:antagonists & inhibitors / Q000378:metabolism*; D007700:Kinetics; D009415:Nerve Net / Q000166:cytology / Q000254:growth & development / Q000378:metabolism; D010655:Phenylenediamines / Q000494:pharmacology; D026902:Potassium Channel Blockers / Q000494:pharmacology; D017966:Pyramidal Cells / Q000187:drug effects / Q000378:metabolism; D011725:Pyridines / Q000494:pharmacology; D051381:Rats; D017208:Rats, Wistar; D049994:Sodium Potassium Chloride Symporter Inhibitors; D028021:Sodium-Potassium-Chloride Symporters / Q000378:metabolism; D064506:Solute Carrier Family 12, Member 2; D009435:Synaptic Transmission / Q000187:drug effects; D005680:gamma-Aminobutyric Acid / Q000378:metabolism / Q000494:pharmacology
D002219:Carbamates; D007211:Indoles; D051658:KCNQ2 Potassium Channel; D010655:Phenylenediamines; D026902:Potassium Channel Blockers; D011725:Pyridines; C578879:Slc12a2 protein, rat; D049994:Sodium Potassium Chloride Symporter Inhibitors; D028021:Sodium-Potassium-Chloride Symporters; D064506:Solute Carrier Family 12, Member 2; C101866:ezogabine; D005680:gamma-Aminobutyric Acid; C061017:linopirdine
J Neurosci Methods. 1991 Mar;37(1):15-26
2072734
J Neurosci. 2004 Jan 21;24(3):592-7
14736843
J Physiol. 1992;451:159-85
1403809
Br J Pharmacol. 1995 Aug;115(7):1163-8
7582539
J Physiol. 1995 Sep 1;487 ( Pt 2):319-29
8558466
Neuron. 1996 Jan;16(1):151-62
8562079
Trends Neurosci. 1996 Dec;19(12):530-4
8961481
Neuron. 1997 Feb;18(2):243-55
9052795
Eur J Neurosci. 1997 Mar;9(3):605-16
9104602
Nat Genet. 1998 Jan;18(1):53-5
9425900
J Pharmacol Exp Ther. 1998 Aug;286(2):709-17
9694925
FEBS Lett. 1998 Nov 6;438(3):171-6
9827540
Science. 1998 Dec 4;282(5395):1890-3
9836639
Nature. 1998 Dec 17;396(6712):687-90
9872318
Trends Neurosci. 2005 Jun;28(6):278-83
15927682
J Neurosci. 2005 Jun 1;25(22):5280-9
15930375
Trends Neurosci. 1991 Dec;14(12):515-9
1726341
J Neurosci. 2000 Mar 1;20(5):1710-21
10684873
J Physiol. 2000 Feb 1;522 Pt 3:349-55
10713961
Neuroscience. 2000;97(2):227-41
10799755
Mol Pharmacol. 2000 Aug;58(2):253-62
10908292
J Biol Chem. 2000 Aug 4;275(31):24089-95
10816588
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9741-6
10931951
Mol Pharmacol. 2000 Sep;58(3):591-600
10953053
Arzneimittelforschung. 2000 Dec;50(12):1063-70
11190770
J Neurosci. 2001 Feb 15;21(4):1096-103
11160379
Nat Rev Neurosci. 2000 Oct;1(1):21-30
11252765
J Physiol. 2001 Apr 1;532(Pt 1):205-16
11283235
J Neurosci. 2001 Aug 1;21(15):5535-45
11466425
Nat Rev Neurosci. 2002 Sep;3(9):728-39
12209121
J Physiol. 2002 Oct 1;544(Pt 1):29-37
12356878
Mol Cell Neurosci. 2003 Jan;22(1):107-17
12595243
Eur J Neurosci. 2005 Jul;22(1):107-18
16029200
J Physiol. 2005 Aug 1;566(Pt 3):689-715
15890705
J Physiol. 2005 Aug 15;567(Pt 1):79-93
15919718
Nat Med. 2005 Nov;11(11):1205-13
16227993
Proc Natl Acad Sci U S A. 2005 Nov 8;102(45):16454-9
16263935
J Neurosci. 2006 Mar 8;26(10):2599-613
16525039
Brain Res. 2006 Mar 10;1077(1):1-6
16500630
Neurosci Lett. 2006 May 29;400(1-2):101-4
16513263
Eur J Neurosci. 2006 May;23(9):2330-8
16706841
J Neurophysiol. 2006 Jun;95(6):3480-95
16495357
J Physiol. 2006 Jun 15;573(Pt 3):765-73
16644806
J Physiol. 2006 Oct 1;576(Pt 1):235-56
16840518
J Neurophysiol. 2007 Jan;97(1):283-95
17050829
Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13176-81
17656555
Physiol Rev. 2007 Oct;87(4):1215-84
17928584
J Physiol. 2008 Mar 1;586(5):1351-63
18187471
J Neurophysiol. 2003 Nov;90(5):2964-72
12867526
J Physiol. 2008 Apr 1;586(7):1791-801
18238816
J Neurosci. 2004 Feb 4;24(5):1236-44
14762142
Proc Natl Acad Sci U S A. 2004 Mar 16;101(11):3967-72
15007179
J Neurosci. 2004 May 12;24(19):4614-24
15140933
Science. 2004 Jun 25;304(5679):1926-9
15218136
J Physiol. 2004 Aug 15;559(Pt 1):129-39
15218067
Nature. 1980 Feb 14;283(5748):673-6
6965523
Brain Res. 1982 Oct 28;250(1):71-92
6128061
J Physiol. 1982 Nov;332:263-72
6984074
J Physiol. 1989 Feb;409:171-90
2585290
J Physiol. 1989 Sep;416:303-25
2575165