 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 13, 5312-5323, Copyright © 1993 by Society for Neuroscience
Ionic flux contributions to neocortical slow waves and nucleus basalis- mediated activation: whole-cell recordings in vivo
R Metherate and JH Ashe
Department of Neuroscience, University of California, Riverside 92521.
Slow, rhythmic membrane potential (Vm) fluctuations occur spontaneously in
cortical neurons of urethane-anesthetized rats, and likely underlie EEG
activity in the same low-frequency (1-4 Hz or delta) range. Nucleus basalis
(NB) stimulation elicits neocortical activation, simultaneously modifying
Vm and EEG fluctuations, by way of cortical muscarinic ACh receptors
(Metherate et al., 1992). To investigate the nature of spontaneous
fluctuations and their modification by NB stimulation, we have obtained
intracellular recordings from auditory cortex using the whole-cell
recording technique in vivo. Spontaneous Vm fluctuations appeared to
contain three components whose polarity and time course resembled the EPSP,
putative Cl(-)-mediated IPSP, and putative K(+)- mediated, long-lasting
IPSP elicited by thalamic stimulation. The spontaneous, long-lasting
hyperpolarization, whose rhythmic occurrence appeared to set the slow-wave
rhythm, was associated with an increased conductance that could shunt the
thalamocortical EPSP. We hypothesized that spontaneous Vm fluctuations
arise from intermixed rapid depolarizations, rapid Cl(-)-mediated
hyperpolarizations, and long- lasting, K(+)-mediated hyperpolarizations.
NB-mediated cortical activation might then result from muscarinic
suppression of K+ permeability, allowing the rapid depolarizations and Cl-
fluxes to continue uninterrupted. Tests of this hypothesis showed that (1)
intracellular blockade of K+ channels by rapid diffusion of Cs+ from the
recording pipette resulted in suppression of spontaneous, long- lasting
hyperpolarizations, mimicking the effect of NB stimulation, and reducing
shunting of the thalamocortical EPSP; (2) effects of Cs+ and NB stimulation
suggested overlapping, or converging, mechanisms of action; however, there
were important differential effects on the spontaneous, long-lasting
hyperpolarizations and the K(+)-mediated IPSP; and (3) modifying Cl- fluxes
with intracellular picrotoxin or high intracellular Cl- concentrations
resulted in spontaneous and NB- elicited large-amplitude depolarizations.
We conclude that spontaneous, long-lasting hyperpolarizations are K+
fluxes, but are not "spontaneous" K(+)-mediated IPSPs. Since NB-mediated
reduction of spontaneous hyperpolarizations implies muscarinic suppression
of a K+ conductance, the spontaneous hyperpolarizations more likely result
from the calcium-activated K+ current, IK(Ca). Finally, Cl- fluxes form an
important component of activated Vm fluctuations that acts to restrain
excessive depolarization.
This article has been cited by other articles:
|
|
|
|
 
M. V. Sanchez-Vives, V. F. Descalzo, R. Reig, N. A. Figueroa, A. Compte, and R. Gallego
Rhythmic Spontaneous Activity in the Piriform Cortex
Cereb Cortex,
May 1, 2008;
18(5):
1179 - 1192.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. B. McCracken and A. A. Grace
High-Frequency Deep Brain Stimulation of the Nucleus Accumbens Region Suppresses Neuronal Activity and Selectively Modulates Afferent Drive in Rat Orbitofrontal Cortex In Vivo
J. Neurosci.,
November 14, 2007;
27(46):
12601 - 12610.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Hasenstaub, R. N. S. Sachdev, and D. A. McCormick
State Changes Rapidly Modulate Cortical Neuronal Responsiveness
J. Neurosci.,
September 5, 2007;
27(36):
9607 - 9622.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Haider, A. Duque, A. R. Hasenstaub, Y. Yu, and D. A. McCormick
Enhancement of Visual Responsiveness by Spontaneous Local Network Activity In Vivo
J Neurophysiol,
June 1, 2007;
97(6):
4186 - 4202.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. A. Johnson and D. V. Buonomano
Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices
J. Neurosci.,
May 30, 2007;
27(22):
5915 - 5925.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Rudolph, M. Pospischil, I. Timofeev, and A. Destexhe
Inhibition Determines Membrane Potential Dynamics and Controls Action Potential Generation in Awake and Sleeping Cat Cortex
J. Neurosci.,
May 16, 2007;
27(20):
5280 - 5290.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. B. Carr and D. J. Surmeier
M1 Muscarinic Receptor Modulation of Kir2 Channels Enhances Temporal Summation of Excitatory Synaptic Potentials in Prefrontal Cortex Pyramidal Neurons
J Neurophysiol,
May 1, 2007;
97(5):
3432 - 3438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Rigas and M. A. Castro-Alamancos
Thalamocortical Up States: Differential Effects of Intrinsic and Extrinsic Cortical Inputs on Persistent Activity
J. Neurosci.,
April 18, 2007;
27(16):
4261 - 4272.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Khanbabaie, A. S. Mahani, and R. Wessel
Contextual Interaction of GABAergic Circuitry With Dynamic Synapses
J Neurophysiol,
April 1, 2007;
97(4):
2802 - 2811.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Schuz, D. Chaimow, D. Liewald, and M. Dortenman
Quantitative Aspects of Corticocortical Connections: A Tracer Study in the Mouse
Cereb Cortex,
October 1, 2006;
16(10):
1474 - 1486.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Haider, A. Duque, A. R. Hasenstaub, and D. A. McCormick
Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition.
J. Neurosci.,
April 26, 2006;
26(17):
4535 - 4545.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Morishima and Y. Kawaguchi
Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex.
J. Neurosci.,
April 19, 2006;
26(16):
4394 - 4405.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. A. Milojkovic, M. S. Radojicic, and S. D. Antic
A Strict Correlation between Dendritic and Somatic Plateau Depolarizations in the Rat Prefrontal Cortex Pyramidal Neurons
J. Neurosci.,
April 13, 2005;
25(15):
3940 - 3951.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. J. L Arnold, F. Hofmann, C. P. Bengtson, M. Wittmann, P. Vanhoutte, and H. Bading
Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity
J. Physiol.,
April 1, 2005;
564(1):
3 - 19.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. R. Deweese and A. M. Zador
Shared and Private Variability in the Auditory Cortex
J Neurophysiol,
September 1, 2004;
92(3):
1840 - 1855.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Y. Y. Tan, L. I. Zhang, M. M. Merzenich, and C. E. Schreiner
Tone-Evoked Excitatory and Inhibitory Synaptic Conductances of Primary Auditory Cortex Neurons
J Neurophysiol,
July 1, 2004;
92(1):
630 - 643.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Kaur, R. Lazar, and R. Metherate
Intracortical Pathways Determine Breadth of Subthreshold Frequency Receptive Fields in Primary Auditory Cortex
J Neurophysiol,
June 1, 2004;
91(6):
2551 - 2567.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Birtoli and D. Ulrich
Firing Mode-Dependent Synaptic Plasticity in Rat Neocortical Pyramidal Neurons
J. Neurosci.,
May 26, 2004;
24(21):
4935 - 4940.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. Wu, C. L. Ma, and J. B. Kelly
Contribution of AMPA, NMDA, and GABAA Receptors to Temporal Pattern of Postsynaptic Responses in the Inferior Colliculus of the Rat
J. Neurosci.,
May 12, 2004;
24(19):
4625 - 4634.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Shu, A. Hasenstaub, M. Badoual, T. Bal, and D. A. McCormick
Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons
J. Neurosci.,
November 12, 2003;
23(32):
10388 - 10401.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. McCormick, Y. Shu, A. Hasenstaub, M. Sanchez-Vives, M. Badoual, and T. Bal
Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability
Cereb Cortex,
November 1, 2003;
13(11):
1219 - 1231.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Compte, M. V. Sanchez-Vives, D. A. McCormick, and X.-J. Wang
Cellular and Network Mechanisms of Slow Oscillatory Activity (<1 Hz) and Wave Propagations in a Cortical Network Model
J Neurophysiol,
May 1, 2003;
89(5):
2707 - 2725.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Bazhenov, I. Timofeev, M. Steriade, and T. J. Sejnowski
Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States
J. Neurosci.,
October 1, 2002;
22(19):
8691 - 8704.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kawaguchi
Distinct Firing Patterns of Neuronal Subtypes in Cortical Synchronized Activities
J. Neurosci.,
September 15, 2001;
21(18):
7261 - 7272.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Saar, Y. Grossman, and E. Barkai
Long-Lasting Cholinergic Modulation Underlies Rule Learning in Rats
J. Neurosci.,
February 15, 2001;
21(4):
1385 - 1392.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. E. Latham, B. J. Richmond, P. G. Nelson, and S. Nirenberg
Intrinsic Dynamics in Neuronal Networks. I. Theory
J Neurophysiol,
February 1, 2000;
83(2):
808 - 827.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. S. Lukatch and M. B. Maciver
Physiology, Pharmacology, and Topography of Cholinergic Neocortical Oscillations In Vitro
J Neurophysiol,
May 1, 1997;
77(5):
2427 - 2445.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
