PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of transbThe Royal Society PublishingPhilosophical Transactions BAboutBrowse By SubjectAlertsFree Trial
 
Philos Trans R Soc Lond B Biol Sci. 2003 April 29; 358(1432): 667–674.
PMCID: PMC1693145

Active dendrites, potassium channels and synaptic plasticity.

Abstract

The dendrites of CA1 pyramidal neurons in the hippocampus express numerous types of voltage-gated ion channel, but the distributions or densities of many of these channels are very non-uniform. Sodium channels in the dendrites are responsible for action potential (AP) propagation from the axon into the dendrites (back-propagation); calcium channels are responsible for local changes in dendritic calcium concentrations following back-propagating APs and synaptic potentials; and potassium channels help regulate overall dendritic excitability. Several lines of evidence are presented here to suggest that back-propagating APs, when coincident with excitatory synaptic input, can lead to the induction of either long-term depression (LTD) or long-term potentiation (LTP). The induction of LTD or LTP is correlated with the magnitude of the rise in intracellular calcium. When brief bursts of synaptic potentials are paired with postsynaptic APs in a theta-burst pairing paradigm, the induction of LTP is dependent on the invasion of the AP into the dendritic tree. The amplitude of the AP in the dendrites is dependent, in part, on the activity of a transient, A-type potassium channel that is expressed at high density in the dendrites and correlates with the induction of the LTP. Furthermore, during the expression phase of the LTP, there are local changes in dendritic excitability that may result from modulation of the functioning of this transient potassium channel. The results support the view that the active properties of dendrites play important roles in synaptic integration and synaptic plasticity of these neurons.

Full Text

The Full Text of this article is available as a PDF (151K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD. The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem. 2000 Dec;75(6):2277–2287. [PubMed]
  • Anderson AE, Adams JP, Qian Y, Cook RG, Pfaffinger PJ, Sweatt JD. Kv4.2 phosphorylation by cyclic AMP-dependent protein kinase. J Biol Chem. 2000 Feb 25;275(8):5337–5346. [PubMed]
  • Bi G, Poo M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci. 2001;24:139–166. [PubMed]
  • Brown TH, Kairiss EW, Keenan CL. Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci. 1990;13:475–511. [PubMed]
  • Camodeca N, Rowan MJ, Anwyl R. Induction of LTD by increasing extracellular Ca2+ from a low level in the dentate gyrus in vitro. Neurosci Lett. 1998 Oct 9;255(1):53–56. [PubMed]
  • Chavez-Noriega LE, Halliwell JV, Bliss TV. A decrease in firing threshold observed after induction of the EPSP-spike (E-S) component of long-term potentiation in rat hippocampal slices. Exp Brain Res. 1990;79(3):633–641. [PubMed]
  • Christie BR, Magee JC, Johnston D. Dendritic calcium channels and hippocampal long-term depression. Hippocampus. 1996;6(1):17–23. [PubMed]
  • Christie BR, Magee JC, Johnston D. The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. Learn Mem. 1996 Sep-Oct;3(2-3):160–169. [PubMed]
  • Christie BR, Schexnayder LK, Johnston D. Contribution of voltage-gated Ca2+ channels to homosynaptic long-term depression in the CA1 region in vitro. J Neurophysiol. 1997 Mar;77(3):1651–1655. [PubMed]
  • Colbert CM, Johnston D. Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci. 1996 Nov 1;16(21):6676–6686. [PubMed]
  • Colbert Costa M, Pan Enhui. Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci. 2002 Jun;5(6):533–538. [PubMed]
  • Debanne D, Gähwiler BH, Thompson SM. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol. 1998 Feb 15;507(Pt 1):237–247. [PubMed]
  • Dudek SM, Bear MF. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4363–4367. [PubMed]
  • Feldman DE. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron. 2000 Jul;27(1):45–56. [PubMed]
  • Gasparini Sonia, Magee Jeffrey C. Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons. J Physiol. 2002 Jun 15;541(Pt 3):665–672. [PubMed]
  • Golding NL, Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron. 1998 Nov;21(5):1189–1200. [PubMed]
  • Golding NL, Kath WL, Spruston N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J Neurophysiol. 2001 Dec;86(6):2998–3010. [PubMed]
  • Golding Nace L, Staff Nathan P, Spruston Nelson. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature. 2002 Jul 18;418(6895):326–331. [PubMed]
  • Hoffman DA, Johnston D. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci. 1998 May 15;18(10):3521–3528. [PubMed]
  • Hoffman DA, Johnston D. Neuromodulation of dendritic action potentials. J Neurophysiol. 1999 Jan;81(1):408–411. [PubMed]
  • Hoffman DA, Magee JC, Colbert CM, Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature. 1997 Jun 26;387(6636):869–875. [PubMed]
  • Hoffman DA, Sprengel R, Sakmann B. Molecular dissection of hippocampal theta-burst pairing potentiation. Proc Natl Acad Sci U S A. 2002 May 28;99(11):7740–7745. [PubMed]
  • Jaffe DB, Johnston D, Lasser-Ross N, Lisman JE, Miyakawa H, Ross WN. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature. 1992 May 21;357(6375):244–246. [PubMed]
  • Johnston D, Magee JC, Colbert CM, Cristie BR. Active properties of neuronal dendrites. Annu Rev Neurosci. 1996;19:165–186. [PubMed]
  • Johnston D, Hoffman DA, Colbert CM, Magee JC. Regulation of back-propagating action potentials in hippocampal neurons. Curr Opin Neurobiol. 1999 Jun;9(3):288–292. [PubMed]
  • Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol. 2000 May 15;525(Pt 1):75–81. [PubMed]
  • Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci. 1998 Oct 1;18(19):7613–7624. [PubMed]
  • Magee JC, Johnston D. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol. 1995 Aug 15;487(Pt 1):67–90. [PubMed]
  • Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 1997 Jan 10;275(5297):209–213. [PubMed]
  • Magee JC, Christofi G, Miyakawa H, Christie B, Lasser-Ross N, Johnston D. Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. J Neurophysiol. 1995 Sep;74(3):1335–1342. [PubMed]
  • Magee J, Hoffman D, Colbert C, Johnston D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol. 1998;60:327–346. [PubMed]
  • Maletic-Savatic M, Lenn NJ, Trimmer JS. Differential spatiotemporal expression of K+ channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J Neurosci. 1995 May;15(5 Pt 2):3840–3851. [PubMed]
  • Markram H, Lübke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 1997 Jan 10;275(5297):213–215. [PubMed]
  • Mickus T, Jung H y, Spruston N. Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. Biophys J. 1999 Feb;76(2):846–860. [PubMed]
  • Migliore M, Hoffman DA, Magee JC, Johnston D. Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci. 1999 Jul-Aug;7(1):5–15. [PubMed]
  • Miyakawa H, Ross WN, Jaffe D, Callaway JC, Lasser-Ross N, Lisman JE, Johnston D. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron. 1992 Dec;9(6):1163–1173. [PubMed]
  • Mockett Bruce, Coussens Christine, Abraham Wickliffe C. NMDA receptor-mediated metaplasticity during the induction of long-term depression by low-frequency stimulation. Eur J Neurosci. 2002 Jun;15(11):1819–1826. [PubMed]
  • Mulkey RM, Malenka RC. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron. 1992 Nov;9(5):967–975. [PubMed]
  • Poolos Nicholas P, Migliore Michele, Johnston Daniel. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci. 2002 Aug;5(8):767–774. [PubMed]
  • Roberson ED, English JD, Sweatt JD. A biochemist's view of long-term potentiation. Learn Mem. 1996 Jul-Aug;3(1):1–24. [PubMed]
  • Sabatini BL, Svoboda K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature. 2000 Nov 30;408(6812):589–593. [PubMed]
  • Serôdio P, Rudy B. Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain. J Neurophysiol. 1998 Feb;79(2):1081–1091. [PubMed]
  • Sheng M, Tsaur ML, Jan YN, Jan LY. Subcellular segregation of two A-type K+ channel proteins in rat central neurons. Neuron. 1992 Aug;9(2):271–284. [PubMed]
  • Spruston N, Schiller Y, Stuart G, Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science. 1995 Apr 14;268(5208):297–300. [PubMed]
  • Stuart GJ, Häusser M. Dendritic coincidence detection of EPSPs and action potentials. Nat Neurosci. 2001 Jan;4(1):63–71. [PubMed]
  • Watanabe Shigeo, Hoffman Dax A, Migliore Michele, Johnston Daniel. Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8366–8371. [PubMed]
  • Yuan Li-Lian, Adams J Paige, Swank Michael, Sweatt J David, Johnston Daniel. Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci. 2002 Jun 15;22(12):4860–4868. [PubMed]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society