Frequency-selective control of cortical and subcortical networks by central thalamus

Central thalamus plays a critical role in forebrain arousal and organized behavior. However, network-level mechanisms that link its activity to brain state remain enigmatic. Here, we combined optogenetics, fMRI, electrophysiology, and video-EEG monitoring to characterize the central thalamus-driven...

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Main Authors: Jia Liu, Hyun Joo Lee, Andrew J Weitz, Zhongnan Fang, Peter Lin, ManKin Choy, Robert Fisher, Vadim Pinskiy, Alexander Tolpygo, Partha Mitra, Nicholas Schiff, Jin Hyung Lee
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2015-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/09215
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spelling doaj-feb5874de8c94ec5ab879c3a387fe5052021-05-05T00:09:26ZengeLife Sciences Publications LtdeLife2050-084X2015-12-01410.7554/eLife.09215Frequency-selective control of cortical and subcortical networks by central thalamusJia Liu0Hyun Joo Lee1Andrew J Weitz2Zhongnan Fang3Peter Lin4ManKin Choy5Robert Fisher6Vadim Pinskiy7Alexander Tolpygo8Partha Mitra9Nicholas Schiff10Jin Hyung Lee11Department of Neurology and Neurological Sciences, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United States; Department of Bioengineering, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United States; Department of Electrical Engineering, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United StatesCold Spring Harbor Laboratory, Cold Spring Harbor, United StatesCold Spring Harbor Laboratory, Cold Spring Harbor, United StatesCold Spring Harbor Laboratory, Cold Spring Harbor, United StatesDepartment of Neurology, Weill Cornell Medical College, New York, United StatesDepartment of Neurology and Neurological Sciences, Stanford University, Stanford, United States; Department of Bioengineering, Stanford University, Stanford, United States; Department of Electrical Engineering, Stanford University, Stanford, United States; Department of Neurosurgery, Stanford University, Stanford, United StatesCentral thalamus plays a critical role in forebrain arousal and organized behavior. However, network-level mechanisms that link its activity to brain state remain enigmatic. Here, we combined optogenetics, fMRI, electrophysiology, and video-EEG monitoring to characterize the central thalamus-driven global brain networks responsible for switching brain state. 40 and 100 Hz stimulations of central thalamus caused widespread activation of forebrain, including frontal cortex, sensorimotor cortex, and striatum, and transitioned the brain to a state of arousal in asleep rats. In contrast, 10 Hz stimulation evoked significantly less activation of forebrain, inhibition of sensory cortex, and behavioral arrest. To investigate possible mechanisms underlying the frequency-dependent cortical inhibition, we performed recordings in zona incerta, where 10, but not 40, Hz stimulation evoked spindle-like oscillations. Importantly, suppressing incertal activity during 10 Hz central thalamus stimulation reduced the evoked cortical inhibition. These findings identify key brain-wide dynamics underlying central thalamus arousal regulation.https://elifesciences.org/articles/09215Central thalamusFunctional MRIOptogeneticsArousal
collection DOAJ
language English
format Article
sources DOAJ
author Jia Liu
Hyun Joo Lee
Andrew J Weitz
Zhongnan Fang
Peter Lin
ManKin Choy
Robert Fisher
Vadim Pinskiy
Alexander Tolpygo
Partha Mitra
Nicholas Schiff
Jin Hyung Lee
spellingShingle Jia Liu
Hyun Joo Lee
Andrew J Weitz
Zhongnan Fang
Peter Lin
ManKin Choy
Robert Fisher
Vadim Pinskiy
Alexander Tolpygo
Partha Mitra
Nicholas Schiff
Jin Hyung Lee
Frequency-selective control of cortical and subcortical networks by central thalamus
eLife
Central thalamus
Functional MRI
Optogenetics
Arousal
author_facet Jia Liu
Hyun Joo Lee
Andrew J Weitz
Zhongnan Fang
Peter Lin
ManKin Choy
Robert Fisher
Vadim Pinskiy
Alexander Tolpygo
Partha Mitra
Nicholas Schiff
Jin Hyung Lee
author_sort Jia Liu
title Frequency-selective control of cortical and subcortical networks by central thalamus
title_short Frequency-selective control of cortical and subcortical networks by central thalamus
title_full Frequency-selective control of cortical and subcortical networks by central thalamus
title_fullStr Frequency-selective control of cortical and subcortical networks by central thalamus
title_full_unstemmed Frequency-selective control of cortical and subcortical networks by central thalamus
title_sort frequency-selective control of cortical and subcortical networks by central thalamus
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2015-12-01
description Central thalamus plays a critical role in forebrain arousal and organized behavior. However, network-level mechanisms that link its activity to brain state remain enigmatic. Here, we combined optogenetics, fMRI, electrophysiology, and video-EEG monitoring to characterize the central thalamus-driven global brain networks responsible for switching brain state. 40 and 100 Hz stimulations of central thalamus caused widespread activation of forebrain, including frontal cortex, sensorimotor cortex, and striatum, and transitioned the brain to a state of arousal in asleep rats. In contrast, 10 Hz stimulation evoked significantly less activation of forebrain, inhibition of sensory cortex, and behavioral arrest. To investigate possible mechanisms underlying the frequency-dependent cortical inhibition, we performed recordings in zona incerta, where 10, but not 40, Hz stimulation evoked spindle-like oscillations. Importantly, suppressing incertal activity during 10 Hz central thalamus stimulation reduced the evoked cortical inhibition. These findings identify key brain-wide dynamics underlying central thalamus arousal regulation.
topic Central thalamus
Functional MRI
Optogenetics
Arousal
url https://elifesciences.org/articles/09215
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