title: Bidirectional pattern-specific plasticity of the slow afterhyperpolarization in rats: role for high-voltage activated Ca2+ channels and I h.
abstract: A burst of action potentials in hippocampal neurons is followed by a slow afterhyperpolarization (sAHP) that serves to limit subsequent firing. A reduction in the sAHP accompanies acquisition of several types of learning, whereas increases in the sAHP are correlated with cognitive impairment. The present study demonstrates in vitro that activity-dependent bidirectional plasticity of the sAHP does not require synaptic activation, and depends on the pattern of action potential firing. Whole-cell current-clamp recordings from CA1 pyramidal neurons in hippocampal slices from young rats (postnatal days 14-24) were performed in blockers of synaptic transmission. The sAHP was evoked by action potential firing at gamma-related (50 Hz, gamma-AHP) or theta frequencies (5 Hz, theta-AHP), two firing frequencies implicated in attention and memory. Interestingly, when the gamma-AHP and theta-AHP were evoked in the same cell, a gradual potentiation of the gamma-AHP (186 ± 31%) was observed that was blocked using Ca(2+) channel blockers nimodipine (10 μm) or ω-conotoxin MVIIC (1 μm). In experiments that exclusively evoked the sAHP with 50 Hz firing, the gamma-AHP was similarly potentiated (198 ± 44%). However, theta-burst firing pattern alone resulted in a decrease (65 ± 19%) of the sAHP. In these experiments, application of the h-channel blocker ZD7288 (25 μm) selectively prevented enhancement of the gamma-AHP. These data demonstrate that induction requirements for bidirectional AHP plasticity depend on the pattern of action potential firing, and result from distinct mechanisms. The identification of novel mechanisms underlying AHP plasticity in vitro provides additional insight into the dynamic processes that may regulate neuronal excitability during learning in vivo.
authors.affiliation: Department of Physiology and Institute for Neuroscience, Northwestern University Feinberg School of Medicine, Chicago, IL, USA. ckaczorowski@mcw.edu
authors.forename: C C
authors.initials: CC
authors.lastname: Kaczorowski
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D002121:Calcium Channel Blockers / Q000378:metabolism; D020746:Calcium Channels, L-Type / Q000378:metabolism*; D006624:Hippocampus / Q000166:cytology / Q000502:physiology; D008297:Male; D008564:Membrane Potentials / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000502:physiology; D018408:Patch-Clamp Techniques; D051381:Rats; D017208:Rats, Wistar
chemical_list: D002121:Calcium Channel Blockers; D020746:Calcium Channels, L-Type
references.citation: Fundam Clin Pharmacol. 1991;5(4):299-317
references.pmid: 1717356
references.citation: Science. 1995 Apr 14;268(5208):297-300
references.pmid: 7716524
references.citation: Life Sci. 1996;59(5-6):413-20
references.pmid: 8761329
references.citation: J Neurophysiol. 2000 May;83(5):2554-61
references.pmid: 10805657
references.citation: J Physiol. 2005 Aug 1;566(Pt 3):689-715
references.pmid: 15890705
references.citation: Neurobiol Aging. 2011 Aug;32(8):1452-65
references.pmid: 19833411
references.citation: Neuroreport. 1994 Sep 8;5(14):1813-6
references.pmid: 7827339
references.citation: Annu Rev Physiol. 1996;58:299-327
references.pmid: 8815797
references.citation: Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4662-7
references.pmid: 10200319
references.citation: J Neurosci. 2005 Mar 9;25(10):2609-16
references.pmid: 15758171
references.citation: Nat Neurosci. 2005 Nov;8(11):1542-51
references.pmid: 16234810
references.citation: J Neurosci. 2008 Feb 27;28(9):2274-86
references.pmid: 18305260
references.citation: J Neurosci. 2009 Jul 1;29(26):8396-407
references.pmid: 19571130
references.citation: J Physiol. 1987 Aug;389:187-203
references.pmid: 2445972
references.citation: Cereb Cortex. 2006 Apr;16(4):460-8
references.pmid: 15958777
references.citation: Annu Rev Physiol. 1993;55:455-72
references.pmid: 7682045
references.citation: J Neurosci. 2000 Jul 15;20(14):5476-82
references.pmid: 10884331
references.citation: Nat Rev Neurosci. 2003 Nov;4(11):885-900
references.pmid: 14595400
references.citation: Eur J Neurosci. 2003 Jun;17(12):2727-34
references.pmid: 12823479
references.citation: Neuron. 2003 Jan 23;37(2):311-22
references.pmid: 12546825
references.citation: Nat Neurosci. 2002 Aug;5(8):767-74
references.pmid: 12118259
references.citation: J Physiol Paris. 2006 Mar-May;99(2-3):180-92
references.pmid: 16458491
references.citation: Hippocampus. 2005;15(7):913-22
references.pmid: 16161035
references.citation: J Physiol. 1994 Mar 1;475(2):229-39
references.pmid: 8021830
references.citation: J Neurophysiol. 1989 May;61(5):971-81
references.pmid: 2542473
references.citation: Hippocampus. 2004;14(8):1011-25
references.pmid: 15390171
references.citation: Front Aging Neurosci. 2010 Feb 03;2:2
references.pmid: 20552042
references.citation: Brain Res. 1988 Oct 11;462(1):118-25
references.pmid: 3179727
references.citation: Physiology (Bethesda). 2010 Oct;25(5):319-29
references.pmid: 20940437
references.citation: Prog Brain Res. 1990;83:161-87
references.pmid: 2203097
references.citation: Science. 2008 Sep 19;321(5896):1686-9
references.pmid: 18802001
references.citation: Cell. 2004 Nov 24;119(5):719-32
references.pmid: 15550252
references.citation: Prog Brain Res. 1990;83:287-300
references.pmid: 2392566
references.citation: Hippocampus. 2000;10(2):198-206
references.pmid: 10791842
references.citation: J Neurophysiol. 1990 Jan;63(1):72-81
references.pmid: 2299387
references.citation: J Physiol. 1989 Feb;409:171-90
references.pmid: 2585290
references.citation: J Neurophysiol. 1999 Aug;82(2):526-32
references.pmid: 10444652
references.citation: J Neurophysiol. 1992 Dec;68(6):2100-9
references.pmid: 1491260
references.citation: Eur J Neurosci. 1998 Apr;10(4):1518-23
references.pmid: 9749805
references.citation: J Neurophysiol. 1993 Jul;70(1):97-116
references.pmid: 8395591
references.citation: J Neurophysiol. 2003 Oct;90(4):2171-9
references.pmid: 12815013
references.citation: Hippocampus. 1991 Apr;1(2):181-92
references.pmid: 1669292
references.citation: J Neurosci. 2008 Apr 9;28(15):3877-86
references.pmid: 18400886
references.citation: Neuron. 2002 Mar 28;34(1):107-14
references.pmid: 11931745
references.citation: J Physiol. 2007 Feb 1;578(Pt 3):799-818
references.pmid: 17138601
references.citation: Curr Opin Neurobiol. 1996 Jun;6(3):318-23
references.pmid: 8794088
references.citation: Nature. 1991 May 9;351(6322):145-7
references.pmid: 1709448
references.citation: Exp Brain Res. 1990;80(3):456-62
references.pmid: 2387347
references.citation: Neuroreport. 1999 Jun 23;10(9):1951-6
references.pmid: 10501539
references.citation: Science. 1995 Mar 10;267(5203):1512-5
references.pmid: 7878473
references.citation: Pflugers Arch. 1999 Jan;437(2):261-6
references.pmid: 9929568
references.citation: Exp Neurol. 1973 Nov;41(2):461-531
references.pmid: 4355646
references.citation: J Neurosci. 2001 Feb 15;21(4):1385-92
references.pmid: 11160410
references.citation: J Neurophysiol. 1988 Feb;59(2):450-67
references.pmid: 3351570
references.citation: Science. 1986 May 23;232(4753):985-8
references.pmid: 3704635
references.citation: Aging Cell. 2007 Jun;6(3):327-36
references.pmid: 17517042
references.citation: Brain Res. 1987 Dec 1;435(1-2):387-92
references.pmid: 3123013
references.citation: J Neurophysiol. 2009 Nov;102(5):2763-70
references.pmid: 19726729
references.citation: J Neurophysiol. 1993 Jun;69(6):2129-36
references.pmid: 7688802
references.citation: Eur J Neurosci. 2006 Apr;23(8):2235-40
references.pmid: 16630070
references.citation: J Neurosci. 2002 Mar 1;22(5):1618-28
references.pmid: 11880492
references.citation: Hippocampus. 2011 Feb;21(2):133-41
references.pmid: 20014384
references.citation: Trends Neurosci. 1996 Apr;19(4):150-4
references.pmid: 8658599
references.citation: J Neurophysiol. 1995 Oct;74(4):1714-29
references.pmid: 8989407
references.citation: J Neurosci. 2005 Dec 14;25(50):11710-8
references.pmid: 16354929
references.citation: Pflugers Arch. 1996 Mar;431(5):723-8
references.pmid: 8596722
references.citation: Learn Mem. 2009 May 23;16(6):362-6
references.pmid: 19470651
references.citation: J Neurophysiol. 1996 Sep;76(3):1836-49
references.pmid: 8890296
references.citation: J Neurosci. 2009 Mar 18;29(11):3453-62
references.pmid: 19295151
references.citation: Nature. 2009 Nov 19;462(7271):353-7
references.pmid: 19924214
references.citation: J Neurosci. 2003 Nov 12;23(32):10238-48
references.pmid: 14614082
references.citation: Proc Natl Acad Sci U S A. 2002 Jul 9;99(14):9538-43
references.pmid: 12093909
references.citation: J Neurophysiol. 1998 Jun;79(6):3252-6
references.pmid: 9636123
references.citation: Proc Natl Acad Sci U S A. 1986 Apr;83(8):2733-7
references.pmid: 3458232
references.citation: J Physiol. 1999 May 15;517 ( Pt 1):201-16
references.pmid: 10226160
references.citation: Learn Mem. 1994 May-Jun;1(1):74-82
references.pmid: 10467587
references.citation: J Physiol. 1984 Sep;354:319-31
references.pmid: 6434729
references.citation: Brain Res. 1986 Mar 19;368(2):347-50
references.pmid: 3697730
references.citation: Ageing Res Rev. 2004 Nov;3(4):383-406
references.pmid: 15541708
references.citation: J Neurosci. 1996 Sep 1;16(17):5536-46
references.pmid: 8757265