Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network

Gamma frequency rhythms have been implicated in numerous studies for their role in healthy and abnormal brain function. The frequency band has been described to encompass as broad a range as 30–150 Hz. Crucial to understanding the role of gamma in brain function is an identification of the underlyin...

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Main Authors: Shane eLee, Stephanie R Jones
Format: Article
Language:English
Published: Frontiers Media S.A. 2013-12-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnhum.2013.00869/full
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spelling doaj-2d244514bca34534a865ef1c80c7a7bb2020-11-25T03:32:29ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612013-12-01710.3389/fnhum.2013.0086968869Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical networkShane eLee0Stephanie R Jones1Brown UniversityBrown UniversityGamma frequency rhythms have been implicated in numerous studies for their role in healthy and abnormal brain function. The frequency band has been described to encompass as broad a range as 30–150 Hz. Crucial to understanding the role of gamma in brain function is an identification of the underlying neural mechanisms, which is particularly difficult in the absence of invasive recordings in macroscopic human signals such as those from magnetoencephalography (MEG) and electroencephalography (EEG). Here, we studied features of current dipole (CD) signals from two distinct mechanisms of gamma generation, using a computational model of a laminar cortical circuit designed specifically to simulate CDs in a biophysically principled manner (Jones et al., 2007; Jones et al., 2009). We simulated spiking pyramidal interneuronal gamma (PING) whose period is regulated by the decay time constant of GABAA-mediated synaptic inhibition and also subthreshold gamma driven by gamma-periodic exogenous excitatory synaptic drive. Our model predicts distinguishable CD features created by spiking PING compared to subthreshold driven gamma that can help to disambiguate mechanisms of gamma oscillations in human signals. We found that gamma rhythms in neocortical layer 5 can obscure a simultaneous, independent gamma in layer 2/3. Further, we arrived at a novel interpretation of the origin of high gamma frequency rhythms (100–150 Hz), showing that they emerged from a specific temporal feature of CDs associated with single cycles of PING activity and did not reflect a separate rhythmic process. Last we show that the emergence of observable subthreshold gamma required highly coherent exogenous drive. Our results are the first to demonstrate features of gamma oscillations in human current source signals that distinguish cellular and circuit level mechanisms of these rhythms and may help guide understanding of their functional role.http://journal.frontiersin.org/Journal/10.3389/fnhum.2013.00869/fullgamma oscillationsElectroencephalography (EEG)Magnetoencephalography (MEG)pyramidal interneuronal gammalaminar neocortexand computational neuroscience
collection DOAJ
language English
format Article
sources DOAJ
author Shane eLee
Stephanie R Jones
spellingShingle Shane eLee
Stephanie R Jones
Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
Frontiers in Human Neuroscience
gamma oscillations
Electroencephalography (EEG)
Magnetoencephalography (MEG)
pyramidal interneuronal gamma
laminar neocortex
and computational neuroscience
author_facet Shane eLee
Stephanie R Jones
author_sort Shane eLee
title Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
title_short Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
title_full Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
title_fullStr Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
title_full_unstemmed Distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
title_sort distinguishing mechanisms of gamma frequency oscillations in human current source signals using a computational model of a laminar neocortical network
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2013-12-01
description Gamma frequency rhythms have been implicated in numerous studies for their role in healthy and abnormal brain function. The frequency band has been described to encompass as broad a range as 30–150 Hz. Crucial to understanding the role of gamma in brain function is an identification of the underlying neural mechanisms, which is particularly difficult in the absence of invasive recordings in macroscopic human signals such as those from magnetoencephalography (MEG) and electroencephalography (EEG). Here, we studied features of current dipole (CD) signals from two distinct mechanisms of gamma generation, using a computational model of a laminar cortical circuit designed specifically to simulate CDs in a biophysically principled manner (Jones et al., 2007; Jones et al., 2009). We simulated spiking pyramidal interneuronal gamma (PING) whose period is regulated by the decay time constant of GABAA-mediated synaptic inhibition and also subthreshold gamma driven by gamma-periodic exogenous excitatory synaptic drive. Our model predicts distinguishable CD features created by spiking PING compared to subthreshold driven gamma that can help to disambiguate mechanisms of gamma oscillations in human signals. We found that gamma rhythms in neocortical layer 5 can obscure a simultaneous, independent gamma in layer 2/3. Further, we arrived at a novel interpretation of the origin of high gamma frequency rhythms (100–150 Hz), showing that they emerged from a specific temporal feature of CDs associated with single cycles of PING activity and did not reflect a separate rhythmic process. Last we show that the emergence of observable subthreshold gamma required highly coherent exogenous drive. Our results are the first to demonstrate features of gamma oscillations in human current source signals that distinguish cellular and circuit level mechanisms of these rhythms and may help guide understanding of their functional role.
topic gamma oscillations
Electroencephalography (EEG)
Magnetoencephalography (MEG)
pyramidal interneuronal gamma
laminar neocortex
and computational neuroscience
url http://journal.frontiersin.org/Journal/10.3389/fnhum.2013.00869/full
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