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The Journal of Neuroscience, May 15, 1998, 18(10):3501-3510
Determinants of Voltage Attenuation in Neocortical Pyramidal
Neuron Dendrites
Greg
Stuart1, 3 and
Nelson
Spruston2, 3
1 Division of Neuroscience, John Curtin School of
Medical Research, Australian National University, Canberra, A.C.T.
0200, Australia, 2 Department of Neurobiology and
Physiology, Institute for Neuroscience, Northwestern University,
Evanston, Illinois 60208-3520, and 3 Max Planck Institut
für Medizinische Forschung, Abteilung Zellphysiologie,
Heidelberg, 69120, Germany
How effectively synaptic and regenerative potentials propagate
within neurons depends critically on the membrane properties and
intracellular resistivity of the dendritic tree. These properties therefore are important determinants of neuronal function. Here we use
simultaneous whole-cell patch-pipette recordings from the soma and
apical dendrite of neocortical layer 5 pyramidal neurons to directly
measure voltage attenuation in cortical neurons. When combined with
morphologically realistic compartmental models of the same cells, the
data suggest that the intracellular resistivity of neocortical
pyramidal neurons is relatively low (~70 to 100 cm), but that
voltage attenuation is substantial because of nonuniformly distributed
resting conductances present at a higher density in the distal apical
dendrites. These conductances, which were largely blocked by bath
application of CsCl (5 mM), significantly increased steady-state voltage attenuation and decreased EPSP integral and peak
in a manner that depended on the location of the synapse. Together
these findings suggest that nonuniformly distributed Cs-sensitive and
-insensitive resting conductances generate a "leaky" apical
dendrite, which differentially influences the integration of spatially
segregated synaptic inputs.
Key words:
voltage attenuation; dendrite; intracellular resistivity; neocortical pyramidal neuron; hyperpolarization-activated conductance; Ih; sag; cesium
Copyright © 1998 Society for Neuroscience 0270-6474/98/18103501-10$05.00/0
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84(3):
1445 - 1452.
[Abstract]
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N. Ho and A. Destexhe
Synaptic Background Activity Enhances the Responsiveness of Neocortical Pyramidal Neurons
J Neurophysiol,
September 1, 2000;
84(3):
1488 - 1496.
[Abstract]
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J J. Zhu
Maturation of layer 5 neocortical pyramidal neurons: amplifying salient layer 1 and layer 4 inputs by Ca2+ action potentials in adult rat tuft dendrites
J. Physiol.,
August 1, 2000;
526(3):
571 - 587.
[Abstract]
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B. Santoro, S. Chen, A. Luthi, P. Pavlidis, G. P. Shumyatsky, G. R. Tibbs, and S. A. Siegelbaum
Molecular and Functional Heterogeneity of Hyperpolarization-Activated Pacemaker Channels in the Mouse CNS
J. Neurosci.,
July 15, 2000;
20(14):
5264 - 5275.
[Abstract]
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D. L. Pettit and G. J. Augustine
Distribution of Functional Glutamate and GABA Receptors on Hippocampal Pyramidal Cells and Interneurons
J Neurophysiol,
July 1, 2000;
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28 - 38.
[Abstract]
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H. Tsubokawa, S. Offermanns, M. Simon, and M. Kano
Calcium-Dependent Persistent Facilitation of Spike Backpropagation in the CA1 Pyramidal Neurons
J. Neurosci.,
July 1, 2000;
20(13):
4878 - 4884.
[Abstract]
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J. S. Nettleton and W. J. Spain
Linear to Supralinear Summation of AMPA-Mediated EPSPs in Neocortical Pyramidal Neurons
J Neurophysiol,
June 1, 2000;
83(6):
3310 - 3322.
[Abstract]
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S. R. Williams and G. J. Stuart
Site Independence of EPSP Time Course Is Mediated by Dendritic Ih in Neocortical Pyramidal Neurons
J Neurophysiol,
May 1, 2000;
83(5):
3177 - 3182.
[Abstract]
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P. Varona, J. M. Ibarz, L. Lopez-Aguado, and O. Herreras
Macroscopic and Subcellular Factors Shaping Population Spikes
J Neurophysiol,
April 1, 2000;
83(4):
2192 - 2208.
[Abstract]
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B. S. Mleux and L. E. Moore
Active Dendritic Membrane Properties of Xenopus Larval Spinal Neurons Analyzed With a Whole Cell Soma Voltage Clamp
J Neurophysiol,
March 1, 2000;
83(3):
1381 - 1393.
[Abstract]
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D. Durstewitz, J. K. Seamans, and T. J. Sejnowski
Dopamine-Mediated Stabilization of Delay-Period Activity in a Network Model of Prefrontal Cortex
J Neurophysiol,
March 1, 2000;
83(3):
1733 - 1750.
[Abstract]
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R. K. Powers and M. D. Binder
Summation of Effective Synaptic Currents and Firing Rate Modulation in Cat Spinal Motoneurons
J Neurophysiol,
January 1, 2000;
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483 - 500.
[Abstract]
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G. Y. Shen, W. R. Chen, J. Midtgaard, G. M. Shepherd, and M. L. Hines
Computational Analysis of Action Potential Initiation in Mitral Cell Soma and Dendrites Based on Dual Patch Recordings
J Neurophysiol,
December 1, 1999;
82(6):
3006 - 3020.
[Abstract]
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D. B. Jaffe and N. T. Carnevale
Passive Normalization of Synaptic Integration Influenced by Dendritic Architecture
J Neurophysiol,
December 1, 1999;
82(6):
3268 - 3285.
[Abstract]
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D. Feldmeyer, V. Egger, J. Lubke, and B. Sakmann
Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex
J. Physiol.,
November 15, 1999;
521(1):
169 - 190.
[Abstract]
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M. London, C. Meunier, and I. Segev
Signal Transfer in Passive Dendrites with Nonuniform Membrane Conductance
J. Neurosci.,
October 1, 1999;
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8219 - 8233.
[Abstract]
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L. E. Moore, N. Chub, J. Tabak, and M. O'Donovan
NMDA-Induced Dendritic Oscillations during a Soma Voltage Clamp of Chick Spinal Neurons
J. Neurosci.,
October 1, 1999;
19(19):
8271 - 8280.
[Abstract]
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S. Antic, G. Major, and D. Zecevic
Fast Optical Recordings of Membrane Potential Changes From Dendrites of Pyramidal Neurons
J Neurophysiol,
September 1, 1999;
82(3):
1615 - 1621.
[Abstract]
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R. Wessel, W. B. Kristan Jr, and D. Kleinfeld
Supralinear Summation of Synaptic Inputs by an Invertebrate Neuron: Dendritic Gain Is Mediated by an "Inward Rectifier" K+ Current
J. Neurosci.,
July 15, 1999;
19(14):
5875 - 5888.
[Abstract]
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A. Destexhe and D. Pare
Impact of Network Activity on the Integrative Properties of Neocortical Pyramidal Neurons In Vivo
J Neurophysiol,
April 1, 1999;
81(4):
1531 - 1547.
[Abstract]
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R. A Chitwood, A. Hubbard, and D. B Jaffe
Passive electrotonic properties of rat hippocampal CA3 interneurones
J. Physiol.,
March 15, 1999;
515(3):
743 - 756.
[Abstract]
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J. C. Magee
Dendritic Hyperpolarization-Activated Currents Modify the Integrative Properties of Hippocampal CA1 Pyramidal Neurons
J. Neurosci.,
October 1, 1998;
18(19):
7613 - 7624.
[Abstract]
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