Role of an A-Type K+ Conductance in the Back-Propagation of Action Potentials in the Dendrites of Hippocampal Pyramidal Neurons

Action potentials elicited in the axon actively back-propagate into the dendritic tree. During this process their amplitudes can be modulated by internal and external factors. We used a compartmental model of a hippocampal CA1 pyramidal neuron to illustrate how this modulation could depend on (1) the properties of an A-type K+ conductance that is expressed at high density in hippocampal dendrites and (2) the relative timing of synaptic activation. The simulations suggest that the time relationship between pre- and postsynaptic activity could help regulate the amplitude of back-propagating action potentials, especially in the distal portion of the dendritic tree.

[1]  J. Jefferys.  Proceedings: Propagation of action potentials into the dendrites of hippocampal granule cells in vitro. , 1975, The Journal of physiology.

[2]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

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

[4]  T. H. Brown,et al.  Associative long-term potentiation in hippocampal slices. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

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

[6]  K. Rockland,et al.  Terminal arbors of individual “Feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris‐leucoagglutinin , 1989, The Journal of comparative neurology.

[7]  H. Wigström,et al.  Onset Characteristics of Long‐Term Potentiation in the Guinea‐Pig Hippocampal CA1 Region in Vitro , 1989, The European journal of neuroscience.

[8]  C. Stevens,et al.  Computational implications of NMDA receptor channels. , 1990, Cold Spring Harbor symposia on quantitative biology.

[9]  T. H. Brown,et al.  Biophysical model of a Hebbian synapse. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. Koch,et al.  Amplification and linearization of distal synaptic input to cortical pyramidal cells. , 1994, Journal of neurophysiology.

[11]  M. Häusser,et al.  Initiation and spread of sodium action potentials in cerebellar purkinje cells , 1994, Neuron.

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

[13]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[14]  R. Aldrich,et al.  Regulation of Shaker K+ channel inactivation gating by the cAMP-dependent protein kinase , 1994, Neuron.

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

[16]  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.

[17]  T. Sejnowski,et al.  A model of spike initiation in neocortical pyramidal neurons , 1995, Neuron.

[18]  Idan Segev,et al.  Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  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.

[20]  M. Migliore.  Modeling the attenuation and failure of action potentials in the dendrites of hippocampal neurons. , 1996, Biophysical journal.

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

[22]  E. Tongiorgi,et al.  Activity-Dependent Dendritic Targeting of BDNF and TrkB mRNAs in Hippocampal Neurons , 1997, The Journal of Neuroscience.

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

[24]  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.

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

[26]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

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

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

[29]  J. Magee.  Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons , 1998, The Journal of Neuroscience.

[30]  D. Clapham,et al.  NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation , 1998, Nature Neuroscience.

[31]  D. Johnston,et al.  Downregulation of Transient K+ Channels in Dendrites of Hippocampal CA1 Pyramidal Neurons by Activation of PKA and PKC , 1998, The Journal of Neuroscience.

[32]  R. Yuste,et al.  Input Summation by Cultured Pyramidal Neurons Is Linear and Position-Independent , 1998, The Journal of Neuroscience.

[33]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Carol M. Petito.  The Synaptic Organization of the Brain, 4th Ed , 1998 .

[35]  M. Migliore,et al.  Energy efficient modulation of dendritic processing functions. , 1998, Bio Systems.

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

[37]  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.

[38]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[39]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[40]  R. Yuste,et al.  Linear Summation of Excitatory Inputs by CA1 Pyramidal Neurons , 1999, Neuron.

[41]  J. Magee.  Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. , 1999, Nature neuroscience.

[42]  D. Johnston,et al.  Neuromodulation of dendritic action potentials. , 1999, Journal of neurophysiology.

[43]  N. Spruston,et al.  Properties of slow, cumulative sodium channel inactivation in rat hippocampal CA1 pyramidal neurons. , 1999, Biophysical journal.