Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans

Emerging neuroimaging studies emphasize the dynamic organization of spontaneous brain activity in both human and non-human primates, even under anesthesia. In a recent study, we were able to characterize the heterogeneous architecture of intrinsic functional flexibility in the awake, resting human b...

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Main Authors: Dazhi Yin, Zhao Zhang, Zhiwei Wang, Kristina Zeljic, Qian Lv, Danchao Cai, Yingwei Wang, Zheng Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-02-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.00174/full
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author Dazhi Yin
Zhao Zhang
Zhiwei Wang
Kristina Zeljic
Kristina Zeljic
Qian Lv
Danchao Cai
Yingwei Wang
Zheng Wang
author_facet Dazhi Yin
Zhao Zhang
Zhiwei Wang
Kristina Zeljic
Kristina Zeljic
Qian Lv
Danchao Cai
Yingwei Wang
Zheng Wang
author_sort Dazhi Yin
collection DOAJ
description Emerging neuroimaging studies emphasize the dynamic organization of spontaneous brain activity in both human and non-human primates, even under anesthesia. In a recent study, we were able to characterize the heterogeneous architecture of intrinsic functional flexibility in the awake, resting human brain using time-resolved analysis and a probabilistic model. However, it is unknown whether this organizational principle is preserved in the anesthetized monkey brain, and how anesthesia affects dynamic and static measurements of spontaneous brain activity. To investigate these issues, we collected resting-state functional magnetic resonance imaging (fMRI) datasets from 178 awake humans and 11 anesthetized monkeys (all healthy). Our recently established method, a complexity measurement (i.e., Shannon entropy) of dynamic functional connectivity patterns of each brain region, was used to map the intrinsic functional flexibility across the cerebral cortex. To further explore the potential effects of anesthesia, we performed time series analysis and correlation analysis between dynamic and static measurements within awake human and anesthetized monkey brains, respectively. We observed a heterogeneous profile of intrinsic functional flexibility in the anesthetized monkey brain, which showed some similarities to that of awake humans (r = 0.30, p = 0.007). However, we found that brain activity in anesthetized monkeys generally shifted toward random fluctuations. Moreover, there is a negative correlation between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength in anesthetized monkeys, but not in awake humans. Our findings indicate that the heterogeneous architecture of intrinsic functional flexibility across cortex probably reflects an evolutionarily conserved aspect of functional brain organization, which persists across levels of cognitive processing (states of consciousness). The coupling between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength may serve as a potential signature of anesthesia. This study not only offers fresh insight into the evolution of brain functional architecture, but also advances our understanding of the dynamics of spontaneous brain activity.
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spelling doaj.art-0c2d2f6e5cc54cb3b1e94d2938939c4c2022-12-22T03:33:17ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-02-011310.3389/fnins.2019.00174432781Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake HumansDazhi Yin0Zhao Zhang1Zhiwei Wang2Kristina Zeljic3Kristina Zeljic4Qian Lv5Danchao Cai6Yingwei Wang7Zheng Wang8Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Anesthesiology, Huashan Hospital, Fudan University, Shanghai, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaDepartment of Anesthesiology, Huashan Hospital, Fudan University, Shanghai, ChinaInstitute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, ChinaEmerging neuroimaging studies emphasize the dynamic organization of spontaneous brain activity in both human and non-human primates, even under anesthesia. In a recent study, we were able to characterize the heterogeneous architecture of intrinsic functional flexibility in the awake, resting human brain using time-resolved analysis and a probabilistic model. However, it is unknown whether this organizational principle is preserved in the anesthetized monkey brain, and how anesthesia affects dynamic and static measurements of spontaneous brain activity. To investigate these issues, we collected resting-state functional magnetic resonance imaging (fMRI) datasets from 178 awake humans and 11 anesthetized monkeys (all healthy). Our recently established method, a complexity measurement (i.e., Shannon entropy) of dynamic functional connectivity patterns of each brain region, was used to map the intrinsic functional flexibility across the cerebral cortex. To further explore the potential effects of anesthesia, we performed time series analysis and correlation analysis between dynamic and static measurements within awake human and anesthetized monkey brains, respectively. We observed a heterogeneous profile of intrinsic functional flexibility in the anesthetized monkey brain, which showed some similarities to that of awake humans (r = 0.30, p = 0.007). However, we found that brain activity in anesthetized monkeys generally shifted toward random fluctuations. Moreover, there is a negative correlation between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength in anesthetized monkeys, but not in awake humans. Our findings indicate that the heterogeneous architecture of intrinsic functional flexibility across cortex probably reflects an evolutionarily conserved aspect of functional brain organization, which persists across levels of cognitive processing (states of consciousness). The coupling between nodal entropy for the distribution of dynamic functional connectivity patterns and static functional connectivity strength may serve as a potential signature of anesthesia. This study not only offers fresh insight into the evolution of brain functional architecture, but also advances our understanding of the dynamics of spontaneous brain activity.https://www.frontiersin.org/article/10.3389/fnins.2019.00174/fulldynamic brain organizationintrinsic functional flexibilityevolutionmonkeyanesthesiaresting-state fMRI
spellingShingle Dazhi Yin
Zhao Zhang
Zhiwei Wang
Kristina Zeljic
Kristina Zeljic
Qian Lv
Danchao Cai
Yingwei Wang
Zheng Wang
Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
Frontiers in Neuroscience
dynamic brain organization
intrinsic functional flexibility
evolution
monkey
anesthesia
resting-state fMRI
title Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
title_full Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
title_fullStr Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
title_full_unstemmed Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
title_short Brain Map of Intrinsic Functional Flexibility in Anesthetized Monkeys and Awake Humans
title_sort brain map of intrinsic functional flexibility in anesthetized monkeys and awake humans
topic dynamic brain organization
intrinsic functional flexibility
evolution
monkey
anesthesia
resting-state fMRI
url https://www.frontiersin.org/article/10.3389/fnins.2019.00174/full
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