title: SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro.
abstract: Understanding the mechanistic substrates of neural computations that lead to behavior remains a fundamental problem in neuroscience. In particular, the contributions of intrinsic neural properties such as burst firing and dendritic morphology to the processing of behaviorally relevant sensory input have received much interest recently. Pyramidal cells within the electrosensory lateral line lobe of weakly electric fish display an intrinsic bursting mechanism that relies on somato-dendritic interactions when recorded in vitro: backpropagating somatic action potentials trigger dendritic action potentials that lead to a depolarizing afterpotential (DAP) at the soma. We recorded intracellularly from these neurons in vivo and found firing patterns that were quite different from those seen in vitro: we found no evidence for DAPs as each somatic action potential was followed by a pronounced afterhyperpolarization (AHP). Calcium chelators injected in vivo reduced the AHP, thereby unmasking the DAP and inducing in vitro-like bursting in pyramidal cells. These bursting dynamics significantly reduced the cell's ability to encode the detailed time course of sensory input. We performed additional in vivo pharmacological manipulations and mathematical modeling to show that calcium influx through N-methyl-d-aspartate (NMDA) receptors activate dendritic small conductance (SK) calcium-activated potassium channels, which causes an AHP that counteracts the DAP and leads to early termination of the burst. Our results show that ion channels located in dendrites can have a profound influence on the processing of sensory input by neurons in vivo through the modulation of an intrinsic bursting mechanism.
authors.affiliation: Department of Physiology, Center for Nonlinear Dynamics, McGill University, Montreal, Quebec, Canada.
authors.forename: Natalia
authors.initials: N
authors.lastname: Toporikova
authors.forename: Maurice J
authors.initials: MJ
authors.lastname: Chacron
mesh_terms: D000200:Action Potentials / Q000187:drug effects; D000465:Algorithms; D000473:Alkanes / Q000494:pharmacology; D000818:Animals; D002118:Calcium / Q000378:metabolism; D002531:Cerebellum / Q000187:drug effects / Q000502:physiology; D002614:Chelating Agents / Q000494:pharmacology; D003198:Computer Simulation; D003712:Dendrites / Q000187:drug effects / Q000502:physiology*; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000494:pharmacology; D023702:Gymnotiformes; D007700:Kinetics; D008274:Magnesium / Q000378:metabolism; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology*; D008839:Microelectrodes; D008959:Models, Neurological; D017966:Pyramidal Cells / Q000187:drug effects / Q000502:physiology*; D011806:Quinolinium Compounds / Q000494:pharmacology; D016194:Receptors, N-Methyl-D-Aspartate / Q000037:antagonists & inhibitors / Q000378:metabolism; D051640:Small-Conductance Calcium-Activated Potassium Channels / Q000037:antagonists & inhibitors / Q000378:metabolism*; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology*
chemical_list: C110349:6,10-diaza-3(1,3),8(1,4)dibenzena-1,5(1,4)diquinolinacyclodecaphane; D000473:Alkanes; D002614:Chelating Agents; D011806:Quinolinium Compounds; D016194:Receptors, N-Methyl-D-Aspartate; D051640:Small-Conductance Calcium-Activated Potassium Channels; D004533:Egtazic Acid; D008274:Magnesium; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; D002118:Calcium
references.citation: J Neurophysiol. 2008 Aug;100(2):852-67
references.pmid: 18509073
references.citation: J Neurophysiol. 2001 Oct;86(4):1612-21
references.pmid: 11600624
references.citation: Trends Neurosci. 1996 Apr;19(4):150-4
references.pmid: 8658599
references.citation: Annu Rev Neurosci. 2005;28:503-32
references.pmid: 16033324
references.citation: Neuron. 2004 Mar 4;41(5):767-79
references.pmid: 15003176
references.citation: Neuroscience. 2008 Jan 24;151(2):403-9
references.pmid: 18055124
references.citation: Trends Neurosci. 2001 Feb;24(2):122-6
references.pmid: 11164943
references.citation: J Neurophysiol. 2007 Sep;98(3):1526-37
references.pmid: 17615127
references.citation: Curr Opin Neurobiol. 2003 Jun;13(3):372-83
references.pmid: 12850223
references.citation: J Comput Neurosci. 2002 Jan-Feb;12(1):5-25
references.pmid: 11932557
references.citation: J Neurophysiol. 1998 Dec;80(6):3352-5
references.pmid: 9862931
references.citation: J Neurophysiol. 1996 Oct;76(4):2483-96
references.pmid: 8899621
references.citation: Nature. 1984 Feb 2-8;307(5950):462-5
references.pmid: 6320006
references.citation: Nature. 2003 Jan 30;421(6922):539-43
references.pmid: 12556894
references.citation: J Chem Neuroanat. 1991 Jan-Feb;4(1):1-38
references.pmid: 2012682
references.citation: J Neurophysiol. 2006 May;95(5):2933-46
references.pmid: 16495358
references.citation: Nature. 2003 May 1;423(6935):77-81
references.pmid: 12721628
references.citation: Philos Trans R Soc Lond B Biol Sci. 2002 Dec 29;357(1428):1695-708
references.pmid: 12626004
references.citation: Nat Neurosci. 2005 May;8(5):673-8
references.pmid: 15806098
references.citation: J Comp Neurol. 2008 Apr 20;507(6):1964-78
references.pmid: 18273887
references.citation: J Neurophysiol. 1998 Dec;80(6):3214-32
references.pmid: 9862917
references.citation: J Comp Neurol. 1995 Oct 23;361(3):512-24
references.pmid: 8550896
references.citation: J Neurosci. 2002 Jun 1;22(11):4577-90
references.pmid: 12040065
references.citation: Nat Neurosci. 1999 Nov;2(11):947-57
references.pmid: 10526332
references.citation: J Comput Neurosci. 2001 Mar-Apr;10(2):213-21
references.pmid: 11361260
references.citation: J Neurosci. 2001 May 15;21(10):3312-21
references.pmid: 11331360
references.citation: J Neurophysiol. 2007 Apr;97(4):2731-43
references.pmid: 17409176
references.citation: J Physiol. 1995 Jun 1;485 ( Pt 2):383-402
references.pmid: 7545230
references.citation: J Comp Neurol. 1979 Jan 15;183(2):323-63
references.pmid: 762262
references.citation: J Comp Neurol. 1997 Dec 8;389(1):65-80
references.pmid: 9390760
references.citation: J Neurosci. 2004 May 5;24(18):4351-62
references.pmid: 15128849
references.citation: Prog Neurobiol. 2002 Apr;66(5):345-53
references.pmid: 12015199
references.citation: J Physiol Paris. 2002 Sep-Dec;96(5-6):451-8
references.pmid: 14692493
references.citation: J Exp Biol. 1999 May;202(Pt 10):1319-26
references.pmid: 10210672
references.citation: J Neurosci. 2007 Aug 29;27(35):9491-502
references.pmid: 17728462
references.citation: J Neurosci. 2003 Feb 15;23(4):1524-34
references.pmid: 12598641
references.citation: Nat Neurosci. 2005 May;8(5):642-9
references.pmid: 15852011
references.citation: J Physiol. 1987 Dec;394:501-27
references.pmid: 2451020
references.citation: Neuroreport. 1996 Feb 29;7(3):809-14
references.pmid: 8733751
references.citation: Biophys J. 1994 Jul;67(1):447-56
references.pmid: 7919018
references.citation: J Neurophysiol. 2008 May;99(5):2641-55
references.pmid: 18367702
references.citation: J Neurosci. 2001 Jul 15;21(14):5328-43
references.pmid: 11438609
references.citation: J Neurosci. 1998 Nov 15;18(22):9500-16
references.pmid: 9801387
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2005 Nov;72(5 Pt 1):051917
references.pmid: 16383655
references.citation: Nat Neurosci. 2005 May;8(5):635-41
references.pmid: 15852010
references.citation: J Neurophysiol. 2001 Jul;86(1):1-39
references.pmid: 11431485
references.citation: Vis Neurosci. 2000 Jan-Feb;17(1):55-62
references.pmid: 10750826
references.citation: J Neurophysiol. 2000 Sep;84(3):1519-30
references.pmid: 10980024
references.citation: J Comput Neurosci. 2007 Dec;23(3):301-11
references.pmid: 17436067
references.citation: Adv Pharmacol. 1990;21:101-26
references.pmid: 2148268
references.citation: Ann N Y Acad Sci. 1999 Apr 30;868:370-8
references.pmid: 10414306
references.citation: Curr Opin Neurobiol. 1998 Jun;8(3):321-9
references.pmid: 9687354
references.citation: J Physiol. 1988 May;399:247-66
references.pmid: 2457089
references.citation: J Exp Biol. 1999 May;202(# (Pt 10)):1255-65
references.pmid: 10210666
references.citation: J Neurosci. 1998 Mar 15;18(6):2283-300
references.pmid: 9482813
references.citation: J Neurophysiol. 1998 Dec;80(6):3197-213
references.pmid: 9862916
references.citation: J Comp Physiol A. 1993 May;172(4):409-23
references.pmid: 7686228
references.citation: J Neurosci. 2003 Oct 22;23(29):9650-63
references.pmid: 14573545
references.citation: J Comput Neurosci. 2004 Sep-Oct;17(2):127-36
references.pmid: 15306735
references.citation: J Neurophysiol. 1999 Apr;81(4):1531-47
references.pmid: 10200189
references.citation: Clin Exp Pharmacol Physiol. 2007 Oct;34(10):1077-83
references.pmid: 17714097
references.citation: J Neurophysiol. 2001 Oct;86(4):1523-45
references.pmid: 11600618
references.citation: Trends Neurosci. 1997 Jan;20(1):38-43
references.pmid: 9004418
references.citation: Neuroscience. 1988 Jan;24(1):19-28
references.pmid: 3368048
references.citation: Neural Comput. 2003 Nov;15(11):2523-64
references.pmid: 14577853
references.citation: J Physiol Paris. 2008 Jul-Nov;102(4-6):195-208
references.pmid: 18992813
references.citation: J Neurosci. 2000 Jul 1;20(13):4829-43
references.pmid: 10864940
references.citation: J Neurosci. 2005 Jun 8;25(23):5521-32
references.pmid: 15944380
references.citation: Brain Res. 2004 Sep 3;1019(1-2):293-6
references.pmid: 15306267
references.citation: Network. 2003 Nov;14(4):803-24
references.pmid: 14653504
references.citation: Nat Neurosci. 2005 Dec;8(12):1760-7
references.pmid: 16261132
references.citation: J Neurophysiol. 2007 Apr;97(4):2744-57
references.pmid: 17409177
references.citation: J Neurophysiol. 1996 Oct;76(4):2497-507
references.pmid: 8899622
references.citation: Curr Opin Neurobiol. 1997 Aug;7(4):536-46
references.pmid: 9287205
references.citation: Science. 1996 Sep 20;273(5282):1709-14
references.pmid: 8781233
references.citation: Curr Opin Neurobiol. 2005 Jun;15(3):305-11
references.pmid: 15922588
references.citation: Network. 2003 Feb;14(1):103-18
references.pmid: 12613553
references.citation: J Comput Neurosci. 2003 May-Jun;14(3):329-42
references.pmid: 12766431
references.citation: Nature. 1986 May 29-Jun 4;321(6069):519-22
references.pmid: 3012362
references.citation: J Neurophysiol. 2008 Apr;99(4):1825-35
references.pmid: 18256161
references.citation: Nature. 1996 Dec 12;384(6609):564-7
references.pmid: 8955269
references.citation: J Neurophysiol. 2003 Jan;89(1):324-37
references.pmid: 12522183
references.citation: J Neurophysiol. 2006 Jun;95(6):3297-308
references.pmid: 16554502
references.citation: Nat Rev Neurosci. 2004 Jan;5(1):13-23
references.pmid: 14661065
references.citation: J Neurosci. 2007 Jan 24;27(4):771-81
references.pmid: 17251416
references.citation: J Neurophysiol. 1998 Dec;80(6):3173-96
references.pmid: 9862915
references.citation: J Neurosci. 1994 Nov;14(11 Pt 1):6453-71
references.pmid: 7965050
references.citation: Neural Comput. 2001 Jan;13(1):227-48
references.pmid: 11177434
references.citation: Neural Comput. 1997 Aug 15;9(6):1179-209
references.pmid: 9248061
references.citation: J Neurophysiol. 2003 Feb;89(2):822-32
references.pmid: 12574460
references.citation: J Physiol. 1996 Mar 15;491 ( Pt 3):757-72
references.pmid: 8815209
references.citation: J Neurosci. 2004 Nov 24;24(47):10731-40
references.pmid: 15564591
references.citation: J Neurosci. 2002 Oct 15;22(20):9053-62
references.pmid: 12388612
references.citation: J Comp Neurol. 1992 Nov 8;325(2):135-51
references.pmid: 1460110
references.citation: J Neurophysiol. 2001 Jan;85(1):10-22
references.pmid: 11152701