Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons.

This review discusses recent data regarding the different types of voltage-gated Na+, Ca2+, and K+ channels in dendrites of CA1 pyramidal neurons and their function for synaptic integration and plasticity. Na+ and Ca2+ channels are uniformly distributed throughout the dendrites, although Na+ channels in the soma and proximal dendrites differ in their inactivation properties from Na+ channels in more distal regions. Also, different regions of the neuron express different subtypes of Ca2+ channels. K+ channels are unevenly distributed, with the distal dendrites expressing a more than fivefold greater density of a transient A-type K+ channel than proximal regions. These K+ channels exert profound control over the excitability of the pyramidal neurons and the spread of synaptic potentials throughout the dendrites. The ways in which the active properties of dendrites may contribute toward the induction and maintenance of long-term synaptic plasticity are discussed.

[1]  P. Andersen.  Interhippocampal impulses. II. Apical dendritic activation of CAI neurons. , 1960, Acta physiologica Scandinavica.

[2]  E. Kandel,et al.  Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. , 1961, Journal of neurophysiology.

[3]  E. Kandel,et al.  ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: IV. FAST PREPOTENTIALS. , 1961, Journal of neurophysiology.

[4]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[5]  J. O’Keefe.  A review of the hippocampal place cells , 1979, Progress in Neurobiology.

[6]  W. Levy,et al.  Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus , 1983, Neuroscience.

[7]  J. Barker,et al.  Rat hippocampal neurons in culture: potassium conductances. , 1984, Journal of neurophysiology.

[8]  M A Rogawski,et al.  A transient potassium conductance regulates the excitability of cultured hippocampal and spinal neurons , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  H. Scharfman,et al.  Postsynaptic firing during repetitive stimulation is required for long-term potentiation in hippocampus , 1985, Brain Research.

[10]  J. Halliwell,et al.  Central action of dendrotoxin: selective reduction of a transient K conductance in hippocampus and binding to localized acceptors. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[11]  S. Kelso,et al.  Differential conditioning of associative synaptic enhancement in hippocampal brain slices. , 1986, Science.

[12]  R. Aldrich,et al.  Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. , 1987, Science.

[13]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Johan F. Storm,et al.  Temporal integration by a slowly inactivating K+ current in hippocampal neurons , 1988, Nature.

[15]  B. Rudy,et al.  Diversity and ubiquity of K channels , 1988, Neuroscience.

[16]  Idan Segev,et al.  Methods in Neuronal Modeling , 1988 .

[17]  M. Kennedy.  Regulation of neuronal function by calcium , 1989, Trends in Neurosciences.

[18]  William A. Catterall,et al.  Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons , 1989, Neuron.

[19]  C. Pavlides,et al.  Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  G. Buzsáki.  Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[21]  William A. Catterall,et al.  Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons , 1990, Nature.

[22]  H. Eichenbaum,et al.  Learning‐related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long‐term potentiation , 1991, Hippocampus.

[23]  T. J. Baldwin,et al.  Characterization of a mammalian cDNA for an inactivating voltage-sensitive K+ channel , 1991, Neuron.

[24]  S. Roberds,et al.  Functional characterization of RK5, a voltage‐gated K+ channel cloned from the rat cardiovascular system , 1991, FEBS letters.

[25]  J. Barker,et al.  The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Hell,et al.  Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. , 1992, Neuron.

[27]  Y. Jan,et al.  Subcellular segregation of two A-type K+ channel proteins in rat central neurons , 1992, Neuron.

[28]  Joel L. Davis,et al.  Single neuron computation , 1992 .

[29]  J. Hell,et al.  Biochemical properties and subcellular distribution of an N-type calcium hannel α1 subunit , 1992, Neuron.

[30]  M. Barish,et al.  Two pharmacologically and kinetically distinct transient potassium currents in cultured embryonic mouse hippocampal neurons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  I. Spigelman,et al.  N-type Ca2+ channels are located on somata, dendrites, and a subpopulation of dendritic spines on live hippocampal pyramidal neurons , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  O. Pongs,et al.  Inactivation properties of voltage-gated K+ channels altered by presence of β-subunit , 1994, Nature.

[33]  J. Lisman.  The CaM kinase II hypothesis for the storage of synaptic memory , 1994, Trends in Neurosciences.

[34]  B. Rudy,et al.  Identification of molecular components of A-type channels activating at subthreshold potentials. , 1994, Journal of neurophysiology.

[35]  L. Salkoff,et al.  Elimination of rapid potassium channel inactivation by phosphorylation of the inactivation gate , 1994, Neuron.

[36]  W. N. Ross,et al.  Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. , 1995, Journal of neurophysiology.

[37]  U. Heinemann,et al.  Comparison of voltage-dependent potassium currents in rat pyramidal neurons acutely isolated from hippocampal regions CA1 and CA3. , 1995, Journal of neurophysiology.

[38]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[39]  A. Borst.  The theoretical foundation of dendritic function edited by I. Segev, J. Rinzel and G.M. Shepherd, The MIT Press, 1995. $55.00 (vii + 465 pages) ISBN 0 262 19356 6 , 1995, Trends in Neurosciences.

[40]  D. Johnston,et al.  Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. , 1995, Journal of neurophysiology.

[41]  J. Lambert,et al.  Regenerative properties of pyramidal cell dendrites in area CA1 of the rat hippocampus. , 1995, The Journal of physiology.

[42]  D. Johnston,et al.  Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. , 1995, Science.

[43]  C. Stevens,et al.  Facilitation and depression at single central synapses , 1995, Neuron.

[44]  G. Buzsáki,et al.  Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells , 1995, Hippocampus.

[45]  D. Johnston,et al.  Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. , 1995, Journal of neurophysiology.

[46]  D. Johnston,et al.  Characterization of single voltage‐gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. , 1995, The Journal of physiology.

[47]  J. Hell,et al.  Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  P. Schwindt,et al.  Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. , 1995, Journal of neurophysiology.

[49]  J. Trimmer,et al.  Differential spatiotemporal expression of K+ channel polypeptides in rat hippocampal neurons developing in situ and in vitro , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  G. Buzsáki,et al.  Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  D Johnston.  The calcium code. , 1996, Biophysical journal.

[52]  R. Lipowsky,et al.  Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells. , 1996, Journal of neurophysiology.

[53]  W. N. Ross,et al.  IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

[54]  D. Johnston,et al.  Multiple Channel Types Contribute to the Low-Voltage-Activated Calcium Current in Hippocampal CA3 Pyramidal Neurons , 1996, The Journal of Neuroscience.

[55]  D. Johnston,et al.  Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

[56]  D. Johnston,et al.  Active properties of neuronal dendrites. , 1996, Annual review of neuroscience.

[57]  D. Johnston,et al.  Axonal Action-Potential Initiation and Na+ Channel Densities in the Soma and Axon Initial Segment of Subicular Pyramidal Neurons , 1996, The Journal of Neuroscience.

[58]  D. Johnston,et al.  The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. , 1996, Learning & memory.

[59]  J. Hell,et al.  N-methyl-D-aspartate receptor-induced proteolytic conversion of postsynaptic class C L-type calcium channels in hippocampal neurons. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[60]  K. I. Blum,et al.  Impaired Hippocampal Representation of Space in CA1-Specific NMDAR1 Knockout Mice , 1996, Cell.

[61]  B. Sakmann,et al.  Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. , 1996, Biophysical journal.

[62]  D. Johnston,et al.  K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons , 1997, Nature.

[63]  D. Johnston,et al.  Active dendrites reduce location-dependent variability of synaptic input trains. , 1997, Journal of neurophysiology.

[64]  N. Spruston,et al.  Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons , 1997, The Journal of Neuroscience.

[65]  D. Johnston,et al.  Slow Recovery from Inactivation of Na+ Channels Underlies the Activity-Dependent Attenuation of Dendritic Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1997, The Journal of Neuroscience.

[66]  W. N. Ross,et al.  Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. , 1997, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  S. Hoffman,et al.  Funding for malaria genome sequencing , 1997, Nature.

[68]  N. Spruston,et al.  Action potential initiation and backpropagation in neurons of the mammalian CNS , 1997, Trends in Neurosciences.

[69]  Y. Jan,et al.  Cloned potassium channels from eukaryotes and prokaryotes. , 1997, Annual review of neuroscience.

[70]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[71]  J. Lisman.  Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

[72]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[73]  R. Tsien,et al.  Preferential Interaction of ω-Conotoxins with Inactivated N-type Ca2+ Channels , 1997, The Journal of Neuroscience.

[74]  Min Zhuo,et al.  Dendritic Ca2+ Channels Characterized by Recordings from Isolated Hippocampal Dendritic Segments , 1997, Neuron.

[75]  G. Alonso,et al.  Clustering of KV4.2 potassium channels in postsynaptic membrane of rat supraoptic neurons: an ultrastructural study. , 1997, Neuroscience.

[76]  T. Gillessen,et al.  Amplification of EPSPs by low Ni(2+)- and amiloride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. , 1997, Journal of neurophysiology.

[77]  D. Kleinfeld,et al.  In vivo dendritic calcium dynamics in neocortical pyramidal neurons , 1997, Nature.

[78]  Protein Kinase C Activation Decreases Activity-Dependent Attenuation of Dendritic Na / Current in Hippocampal CA 1 Pyramidal Neurons , 1998 .

[79]  D. Johnston,et al.  Protein kinase C activation decreases activity-dependent attenuation of dendritic Na+ current in hippocampal CA1 pyramidal neurons. , 1998, Journal of neurophysiology.