Recovery of cable properties through active and passive modeling of subthreshold membrane responses from laterodorsal tegmental neurons

A. Surkis, C. S. Peskin, D. Tranchina, C. S. Leonard

Research output: Contribution to journalArticle

Abstract

The laterodorsal tegmental nucleus (LDT) is located in the dorsolateral pontine reticular formation. Cholinergic neurons in the LDT and the adjacent pedunculopontine tegmental nucleus (PPT) are hypothesized to play a critical role in the generation of the electroencephalographic-desynchronized states of wakefulness and rapid eye movement sleep. A quantitative analysis of the cable properties of these cells was undertaken to provide a more detailed understanding of their integrative behavior. The data used in this analysis were the morphologies of intracellularly labeled guinea pig LDT neurons and the voltage responses of these cells to somatic current injection. Initial attempts to model the membrane behavior near resting potential and in the presence of tetrodotoxin (TTX, 1 μM) as purely passive produced fits that did not capture many features of the experimental data. Moreover, the recovered values of membrane conductance or intracellular resistivity were often very far from those reported for other neurons, suggesting that a passive description of cell behavior near rest was not adequate. An active membrane model that included a subthreshold A-type K+ current and/or a hyperpolarization-activated cation current (H-current) then was used to model cell behavior. The voltage traces calculated using this model were better able to reproduce the experimental data, and the cable parameters determined using this methodology were more consistent with those reported for other cells. Additionally, the use of the active model parameter extraction methodology eliminated a problem encountered with the passive model in which parameter sets with widely varying values, sometimes spanning an order of magnitude or more, would produce effectively indistinguishable fits to the data. The use of an active model to directly fit the experimentally measured voltage responses to both long and short current pulses is a novel approach that is of general utility.

Original languageEnglish (US)
Pages (from-to)2593-2607
Number of pages15
JournalJournal of Neurophysiology
Volume80
Issue number5
StatePublished - Nov 1998

Fingerprint

Neurons
Membranes
Pedunculopontine Tegmental Nucleus
Cholinergic Neurons
Wakefulness
REM Sleep
Tetrodotoxin
Membrane Potentials
Cations
Sleep
Guinea Pigs
Injections

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Recovery of cable properties through active and passive modeling of subthreshold membrane responses from laterodorsal tegmental neurons. / Surkis, A.; Peskin, C. S.; Tranchina, D.; Leonard, C. S.

In: Journal of Neurophysiology, Vol. 80, No. 5, 11.1998, p. 2593-2607.

Research output: Contribution to journalArticle

@article{c34f16d5274a4e5dbd600618aff1e1ca,
title = "Recovery of cable properties through active and passive modeling of subthreshold membrane responses from laterodorsal tegmental neurons",
abstract = "The laterodorsal tegmental nucleus (LDT) is located in the dorsolateral pontine reticular formation. Cholinergic neurons in the LDT and the adjacent pedunculopontine tegmental nucleus (PPT) are hypothesized to play a critical role in the generation of the electroencephalographic-desynchronized states of wakefulness and rapid eye movement sleep. A quantitative analysis of the cable properties of these cells was undertaken to provide a more detailed understanding of their integrative behavior. The data used in this analysis were the morphologies of intracellularly labeled guinea pig LDT neurons and the voltage responses of these cells to somatic current injection. Initial attempts to model the membrane behavior near resting potential and in the presence of tetrodotoxin (TTX, 1 μM) as purely passive produced fits that did not capture many features of the experimental data. Moreover, the recovered values of membrane conductance or intracellular resistivity were often very far from those reported for other neurons, suggesting that a passive description of cell behavior near rest was not adequate. An active membrane model that included a subthreshold A-type K+ current and/or a hyperpolarization-activated cation current (H-current) then was used to model cell behavior. The voltage traces calculated using this model were better able to reproduce the experimental data, and the cable parameters determined using this methodology were more consistent with those reported for other cells. Additionally, the use of the active model parameter extraction methodology eliminated a problem encountered with the passive model in which parameter sets with widely varying values, sometimes spanning an order of magnitude or more, would produce effectively indistinguishable fits to the data. The use of an active model to directly fit the experimentally measured voltage responses to both long and short current pulses is a novel approach that is of general utility.",
author = "A. Surkis and Peskin, {C. S.} and D. Tranchina and Leonard, {C. S.}",
year = "1998",
month = "11",
language = "English (US)",
volume = "80",
pages = "2593--2607",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "5",

}

TY - JOUR

T1 - Recovery of cable properties through active and passive modeling of subthreshold membrane responses from laterodorsal tegmental neurons

AU - Surkis, A.

AU - Peskin, C. S.

AU - Tranchina, D.

AU - Leonard, C. S.

PY - 1998/11

Y1 - 1998/11

N2 - The laterodorsal tegmental nucleus (LDT) is located in the dorsolateral pontine reticular formation. Cholinergic neurons in the LDT and the adjacent pedunculopontine tegmental nucleus (PPT) are hypothesized to play a critical role in the generation of the electroencephalographic-desynchronized states of wakefulness and rapid eye movement sleep. A quantitative analysis of the cable properties of these cells was undertaken to provide a more detailed understanding of their integrative behavior. The data used in this analysis were the morphologies of intracellularly labeled guinea pig LDT neurons and the voltage responses of these cells to somatic current injection. Initial attempts to model the membrane behavior near resting potential and in the presence of tetrodotoxin (TTX, 1 μM) as purely passive produced fits that did not capture many features of the experimental data. Moreover, the recovered values of membrane conductance or intracellular resistivity were often very far from those reported for other neurons, suggesting that a passive description of cell behavior near rest was not adequate. An active membrane model that included a subthreshold A-type K+ current and/or a hyperpolarization-activated cation current (H-current) then was used to model cell behavior. The voltage traces calculated using this model were better able to reproduce the experimental data, and the cable parameters determined using this methodology were more consistent with those reported for other cells. Additionally, the use of the active model parameter extraction methodology eliminated a problem encountered with the passive model in which parameter sets with widely varying values, sometimes spanning an order of magnitude or more, would produce effectively indistinguishable fits to the data. The use of an active model to directly fit the experimentally measured voltage responses to both long and short current pulses is a novel approach that is of general utility.

AB - The laterodorsal tegmental nucleus (LDT) is located in the dorsolateral pontine reticular formation. Cholinergic neurons in the LDT and the adjacent pedunculopontine tegmental nucleus (PPT) are hypothesized to play a critical role in the generation of the electroencephalographic-desynchronized states of wakefulness and rapid eye movement sleep. A quantitative analysis of the cable properties of these cells was undertaken to provide a more detailed understanding of their integrative behavior. The data used in this analysis were the morphologies of intracellularly labeled guinea pig LDT neurons and the voltage responses of these cells to somatic current injection. Initial attempts to model the membrane behavior near resting potential and in the presence of tetrodotoxin (TTX, 1 μM) as purely passive produced fits that did not capture many features of the experimental data. Moreover, the recovered values of membrane conductance or intracellular resistivity were often very far from those reported for other neurons, suggesting that a passive description of cell behavior near rest was not adequate. An active membrane model that included a subthreshold A-type K+ current and/or a hyperpolarization-activated cation current (H-current) then was used to model cell behavior. The voltage traces calculated using this model were better able to reproduce the experimental data, and the cable parameters determined using this methodology were more consistent with those reported for other cells. Additionally, the use of the active model parameter extraction methodology eliminated a problem encountered with the passive model in which parameter sets with widely varying values, sometimes spanning an order of magnitude or more, would produce effectively indistinguishable fits to the data. The use of an active model to directly fit the experimentally measured voltage responses to both long and short current pulses is a novel approach that is of general utility.

UR - http://www.scopus.com/inward/record.url?scp=0031761847&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0031761847&partnerID=8YFLogxK

M3 - Article

C2 - 9819266

AN - SCOPUS:0031761847

VL - 80

SP - 2593

EP - 2607

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 5

ER -