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The Journal of Neuroscience, October 1, 1998, 18(19):7613-7624

Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons

Jeffrey C. Magee

Neuroscience Center, Louisiana State University Medical Center, New Orleans, Louisiana 70112

Step hyperpolarizations evoked slowly activating, noninactivating, and slowly deactivating inward currents from membrane patches recorded in the cell-attached patch configuration from the soma and apical dendrites of hippocampal CA1 pyramidal neurons. The density of these hyperpolarization-activated currents (Ih) increased over sixfold from soma to distal dendrites. Activation curves demonstrate that a significant fraction of Ih channels is active near rest and that the range is hyperpolarized relatively more in the distal dendrites. Ih activation and deactivation kinetics are voltage-and temperature-dependent, with time constants of activation and deactivation decreasing with hyperpolarization and depolarization, respectively. Ih demonstrated a mixed Na+-K+ conductance and was sensitive to low concentrations of external CsCl. Dual whole-cell recordings revealed regional differences in input resistance (Rin) and membrane polarization rates (tau mem) across the somatodendritic axis that are attributable to the spatial gradient of Ih channels. As a result of these membrane effects the propagation of subthreshold voltage transients is directionally specific. The elevated dendritic Ih density decreases EPSP amplitude and duration and reduces the time window over which temporal summation takes place. The backpropagation of action potentials into the dendritic arborization was impacted only slightly by dendritic Ih, with the most consistent effect being a decrease in dendritic action potential duration and an increase in afterhyperpolarization. Overall, Ih acts to dampen dendritic excitability, but its largest impact is on the subthreshold range of membrane potentials where the integration of inhibitory and excitatory synaptic inputs takes place.

Key words: hyperpolarization-activated current; dendrite; hippocampus; synaptic integration; CA1 pyramidal neuron; action potential backpropagation


Copyright © 1998 Society for Neuroscience  0270-6474/98/18197613-12$05.00/0


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T. R. Anderson, B. Hu, K. Iremonger, and Z. H. T. Kiss
Selective Attenuation of Afferent Synaptic Transmission as a Mechanism of Thalamic Deep Brain Stimulation-Induced Tremor Arrest
J. Neurosci., January 18, 2006; 26(3): 841 - 850.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
A. R. A. Rodrigues and D. Oertel
Hyperpolarization-Activated Currents Regulate Excitability in Stellate Cells of the Mammalian Ventral Cochlear Nucleus
J Neurophysiol, January 1, 2006; 95(1): 76 - 87.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. Migliore, M. Ferrante, and G. A. Ascoli
Signal Propagation in Oblique Dendrites of CA1 Pyramidal Cells
J Neurophysiol, December 1, 2005; 94(6): 4145 - 4155.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
T. A Simeone, J. M Rho, and T. Z Baram
Single channel properties of hyperpolarization-activated cation currents in acutely dissociated rat hippocampal neurones
J. Physiol., October 15, 2005; 568(2): 371 - 380.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
N. L Golding, T. J Mickus, Y. Katz, W. L Kath, and N. Spruston
Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites
J. Physiol., October 1, 2005; 568(1): 69 - 82.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
R. Yamada, H. Kuba, T. M. Ishii, and H. Ohmori
Hyperpolarization-Activated Cyclic Nucleotide-Gated Cation Channels Regulate Auditory Coincidence Detection in Nucleus Laminaris of the Chick
J. Neurosci., September 28, 2005; 25(39): 8867 - 8877.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
M. Day, D. B. Carr, S. Ulrich, E. Ilijic, T. Tkatch, and D. J. Surmeier
Dendritic Excitability of Mouse Frontal Cortex Pyramidal Neurons Is Shaped by the Interaction among HCN, Kir2, and Kleak Channels
J. Neurosci., September 21, 2005; 25(38): 8776 - 8787.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
N. Gu, K. Vervaeke, H. Hu, and J. F Storm
Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells
J. Physiol., August 1, 2005; 566(3): 689 - 715.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. Wu and J. J. Hablitz
Cooperative Activation of D1 and D2 Dopamine Receptors Enhances a Hyperpolarization-Activated Inward Current in Layer I Interneurons
J. Neurosci., July 6, 2005; 25(27): 6322 - 6328.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
X.-J. Cao and D. Oertel
Temperature Affects Voltage-Sensitive Conductances Differentially in Octopus Cells of the Mammalian Cochlear Nucleus
J Neurophysiol, July 1, 2005; 94(1): 821 - 832.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
T. Yasui, S. Fujisawa, M. Tsukamoto, N. Matsuki, and Y. Ikegaya
Dynamic synapses as archives of synaptic history: state-dependent redistribution of synaptic efficacy in the rat hippocampal CA1
J. Physiol., July 1, 2005; 566(1): 143 - 160.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. M. Swensen and B. P. Bean
Robustness of Burst Firing in Dissociated Purkinje Neurons with Acute or Long-Term Reductions in Sodium Conductance
J. Neurosci., April 6, 2005; 25(14): 3509 - 3520.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
S.-W. Ying and P. A. Goldstein
Propofol-Block of SK Channels in Reticular Thalamic Neurons Enhances GABAergic Inhibition in Relay Neurons
J Neurophysiol, April 1, 2005; 93(4): 1935 - 1948.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. Ariel and N. Kogo
Shunting Inhibition in Accessory Optic System Neurons
J Neurophysiol, April 1, 2005; 93(4): 1959 - 1969.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
C. Chen and N. G. Bazan
Endogenous PGE2 Regulates Membrane Excitability and Synaptic Transmission in Hippocampal CA1 Pyramidal Neurons
J Neurophysiol, February 1, 2005; 93(2): 929 - 941.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
S. Gasparini, M. Migliore, and J. C. Magee
On the Initiation and Propagation of Dendritic Spikes in CA1 Pyramidal Neurons
J. Neurosci., December 8, 2004; 24(49): 11046 - 11056.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
M. Toledo-Rodriguez, B. Blumenfeld, C. Wu, J. Luo, B. Attali, P. Goodman, and H. Markram
Correlation Maps Allow Neuronal Electrical Properties to be Predicted from Single-cell Gene Expression Profiles in Rat Neocortex
Cereb Cortex, December 1, 2004; 14(12): 1310 - 1327.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
B. Santoro, B. J. Wainger, and S. A. Siegelbaum
Regulation of HCN Channel Surface Expression by a Novel C-Terminal Protein-Protein Interaction
J. Neurosci., November 24, 2004; 24(47): 10750 - 10762.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. S. Chan, R. Shigemoto, J. N. Mercer, and D. J. Surmeier
HCN2 and HCN1 Channels Govern the Regularity of Autonomous Pacemaking and Synaptic Resetting in Globus Pallidus Neurons
J. Neurosci., November 3, 2004; 24(44): 9921 - 9932.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
B. Gravante, A. Barbuti, R. Milanesi, I. Zappi, C. Viscomi, and D. DiFrancesco
Interaction of the Pacemaker Channel HCN1 with Filamin A
J. Biol. Chem., October 15, 2004; 279(42): 43847 - 43853.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
N. A. Otmakhova and J. E. Lisman
Contribution of Ih and GABAB to Synaptically Induced Afterhyperpolarizations in CA1: A Brake on the NMDA Response
J Neurophysiol, October 1, 2004; 92(4): 2027 - 2039.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
W. W. Wu, C. S. Chan, and J. F. Disterhoft
Slow Afterhyperpolarization Governs the Development of NMDA Receptor-Dependent Afterdepolarization in CA1 Pyramidal Neurons During Synaptic Stimulation
J Neurophysiol, October 1, 2004; 92(4): 2346 - 2356.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
B. K. Andrasfalvy and J. C. Magee
Changes in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones
J. Physiol., September 1, 2004; 559(2): 543 - 554.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
X. Chen and D. Johnston
Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus
J. Physiol., August 15, 2004; 559(1): 187 - 203.
[Abstract] [Full Text] [PDF]


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ScienceHome page
C. Bernard, A. Anderson, A. Becker, N. P. Poolos, H. Beck, and D. Johnston
Acquired Dendritic Channelopathy in Temporal Lobe Epilepsy
Science, July 23, 2004; 305(5683): 532 - 535.
[Abstract] [Full Text] [PDF]


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GENES CELLSHome page
K. Kimura, J. Kitano, Y. Nakajima, and S. Nakanishi
Hyperpolarization-activated, cyclic nucleotide-gated HCN2 cation channel forms a protein assembly with multiple neuronal scaffold proteins in distinct modes of protein-protein interaction
Genes Cells, July 1, 2004; 9(7): 631 - 640.
[Abstract] [Full Text] [PDF]



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