Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges

Caroline Geisler, Nicolas Brunel, Xiao-Jing Wang

Research output: Contribution to journalArticle

Abstract

During fast oscillations in the local field potential (40-100 Hz gamma, 100-200 Hz sharp-wave ripples) single cortical neurons typically fire irregularly at rates that are much lower than the oscillation frequency. Recent computational studies have provided a mathematical description of such fast oscillations, using the leaky integrate-and-fire (LIF) neuron model. Here, we extend this theoretical framework to populations of more realistic Hodgkin-Huxley-type conductance-based neurons. In a noisy network of GABAergic neurons that are connected randomly and sparsely by chemical synapses, coherent oscillations emerge with a frequency that depends sensitively on the single cell's membrane dynamics. The population frequency can be predicted analytically from the synaptic time constants and the preferred phase of discharge during the oscillatory cycle of a single cell subjected to noisy sinusoidal input. The latter depends significantly on the single cell's membrane properties and can be understood in the context of the simplified exponential integrate-and-fire (EIF) neuron. We find that 200-Hz oscillations can be generated, provided the effective input conductance of single cells is large, so that the single neuron's phase shift is sufficiently small. In a two-population network of excitatory pyramidal cells and inhibitory neurons, recurrent excitation can either decrease or increase the population rhythmic frequency, depending on whether in a neuron the excitatory synaptic current follows or precedes the inhibitory synaptic current in an oscillatory cycle. Detailed single-cell properties have a substantial impact on population oscillations, even though rhythmicity does not originate from pacemaker neurons and is an emergent network phenomenon.

Original languageEnglish (US)
Pages (from-to)4344-4361
Number of pages18
JournalJournal of Neurophysiology
Volume94
Issue number6
DOIs
StatePublished - Dec 2005

Fingerprint

Neurons
Membranes
Population
Cell Membrane
GABAergic Neurons
Pyramidal Cells
Periodicity
Synapses

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. / Geisler, Caroline; Brunel, Nicolas; Wang, Xiao-Jing.

In: Journal of Neurophysiology, Vol. 94, No. 6, 12.2005, p. 4344-4361.

Research output: Contribution to journalArticle

@article{71f3df81a7c94cfd9c627492626d6772,
title = "Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges",
abstract = "During fast oscillations in the local field potential (40-100 Hz gamma, 100-200 Hz sharp-wave ripples) single cortical neurons typically fire irregularly at rates that are much lower than the oscillation frequency. Recent computational studies have provided a mathematical description of such fast oscillations, using the leaky integrate-and-fire (LIF) neuron model. Here, we extend this theoretical framework to populations of more realistic Hodgkin-Huxley-type conductance-based neurons. In a noisy network of GABAergic neurons that are connected randomly and sparsely by chemical synapses, coherent oscillations emerge with a frequency that depends sensitively on the single cell's membrane dynamics. The population frequency can be predicted analytically from the synaptic time constants and the preferred phase of discharge during the oscillatory cycle of a single cell subjected to noisy sinusoidal input. The latter depends significantly on the single cell's membrane properties and can be understood in the context of the simplified exponential integrate-and-fire (EIF) neuron. We find that 200-Hz oscillations can be generated, provided the effective input conductance of single cells is large, so that the single neuron's phase shift is sufficiently small. In a two-population network of excitatory pyramidal cells and inhibitory neurons, recurrent excitation can either decrease or increase the population rhythmic frequency, depending on whether in a neuron the excitatory synaptic current follows or precedes the inhibitory synaptic current in an oscillatory cycle. Detailed single-cell properties have a substantial impact on population oscillations, even though rhythmicity does not originate from pacemaker neurons and is an emergent network phenomenon.",
author = "Caroline Geisler and Nicolas Brunel and Xiao-Jing Wang",
year = "2005",
month = "12",
doi = "10.1152/jn.00510.2004",
language = "English (US)",
volume = "94",
pages = "4344--4361",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "6",

}

TY - JOUR

T1 - Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges

AU - Geisler, Caroline

AU - Brunel, Nicolas

AU - Wang, Xiao-Jing

PY - 2005/12

Y1 - 2005/12

N2 - During fast oscillations in the local field potential (40-100 Hz gamma, 100-200 Hz sharp-wave ripples) single cortical neurons typically fire irregularly at rates that are much lower than the oscillation frequency. Recent computational studies have provided a mathematical description of such fast oscillations, using the leaky integrate-and-fire (LIF) neuron model. Here, we extend this theoretical framework to populations of more realistic Hodgkin-Huxley-type conductance-based neurons. In a noisy network of GABAergic neurons that are connected randomly and sparsely by chemical synapses, coherent oscillations emerge with a frequency that depends sensitively on the single cell's membrane dynamics. The population frequency can be predicted analytically from the synaptic time constants and the preferred phase of discharge during the oscillatory cycle of a single cell subjected to noisy sinusoidal input. The latter depends significantly on the single cell's membrane properties and can be understood in the context of the simplified exponential integrate-and-fire (EIF) neuron. We find that 200-Hz oscillations can be generated, provided the effective input conductance of single cells is large, so that the single neuron's phase shift is sufficiently small. In a two-population network of excitatory pyramidal cells and inhibitory neurons, recurrent excitation can either decrease or increase the population rhythmic frequency, depending on whether in a neuron the excitatory synaptic current follows or precedes the inhibitory synaptic current in an oscillatory cycle. Detailed single-cell properties have a substantial impact on population oscillations, even though rhythmicity does not originate from pacemaker neurons and is an emergent network phenomenon.

AB - During fast oscillations in the local field potential (40-100 Hz gamma, 100-200 Hz sharp-wave ripples) single cortical neurons typically fire irregularly at rates that are much lower than the oscillation frequency. Recent computational studies have provided a mathematical description of such fast oscillations, using the leaky integrate-and-fire (LIF) neuron model. Here, we extend this theoretical framework to populations of more realistic Hodgkin-Huxley-type conductance-based neurons. In a noisy network of GABAergic neurons that are connected randomly and sparsely by chemical synapses, coherent oscillations emerge with a frequency that depends sensitively on the single cell's membrane dynamics. The population frequency can be predicted analytically from the synaptic time constants and the preferred phase of discharge during the oscillatory cycle of a single cell subjected to noisy sinusoidal input. The latter depends significantly on the single cell's membrane properties and can be understood in the context of the simplified exponential integrate-and-fire (EIF) neuron. We find that 200-Hz oscillations can be generated, provided the effective input conductance of single cells is large, so that the single neuron's phase shift is sufficiently small. In a two-population network of excitatory pyramidal cells and inhibitory neurons, recurrent excitation can either decrease or increase the population rhythmic frequency, depending on whether in a neuron the excitatory synaptic current follows or precedes the inhibitory synaptic current in an oscillatory cycle. Detailed single-cell properties have a substantial impact on population oscillations, even though rhythmicity does not originate from pacemaker neurons and is an emergent network phenomenon.

UR - http://www.scopus.com/inward/record.url?scp=28044433619&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=28044433619&partnerID=8YFLogxK

U2 - 10.1152/jn.00510.2004

DO - 10.1152/jn.00510.2004

M3 - Article

VL - 94

SP - 4344

EP - 4361

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 6

ER -