Modular architecture of metabolic brain network and its effects on the spread of perturbation impact

Tianhao Zhang; Qi Huang; Chunxiang Jiao; Hua Liu; Binbin Nie; Shengxiang Liang; Panlong Li; Xi Sun; Ting Feng; Lin Xu; Baoci Shan

doi:10.1016/j.neuroimage.2018.11.003

Modular architecture of metabolic brain network and its effects on the spread of perturbation impact

Neuroimage. 2019 Feb 1:186:146-154. doi: 10.1016/j.neuroimage.2018.11.003. Epub 2018 Nov 5.

Authors

Tianhao Zhang¹, Qi Huang², Chunxiang Jiao³, Hua Liu⁴, Binbin Nie⁵, Shengxiang Liang⁶, Panlong Li⁷, Xi Sun⁸, Ting Feng⁹, Lin Xu¹⁰, Baoci Shan¹¹

Affiliations

¹ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; School of Nuclear Science and Technology, University of Chinese Academy of Sciences, Beijing, 100049, China. Electronic address: thzhang@ihep.ac.cn.
² Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; School of Nuclear Science and Technology, University of Chinese Academy of Sciences, Beijing, 100049, China. Electronic address: huangq@ihep.ac.cn.
³ Yunnan Provincial Key Laboratory of Entomological Biopharmaceutical Research and Development, College of Pharmacy and Chemistry, Dali University, Dali, 671000, China; Key Laboratory of Animal Models and Human Disease Mechanisms, and Laboratory of Learning and Memory, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China. Electronic address: jiaocx_123@163.com.
⁴ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; School of Nuclear Science and Technology, University of Chinese Academy of Sciences, Beijing, 100049, China. Electronic address: liuhua@ihep.ac.cn.
⁵ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; School of Nuclear Science and Technology, University of Chinese Academy of Sciences, Beijing, 100049, China. Electronic address: neibb@ihep.ac.cn.
⁶ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; Department of Physics, Zhengzhou University, Zhengzhou, Henan, 450001, China. Electronic address: liangsx@ihep.ac.cn.
⁷ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; Department of Physics, Zhengzhou University, Zhengzhou, Henan, 450001, China. Electronic address: lipl@ihep.ac.cn.
⁸ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; Department of Physics, Zhengzhou University, Zhengzhou, Henan, 450001, China. Electronic address: sunxi@ihep.ac.cn.
⁹ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; Department of Physics, Zhengzhou University, Zhengzhou, Henan, 450001, China. Electronic address: fengt@ihep.ac.cn.
¹⁰ CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai, China; Key Laboratory of Animal Models and Human Disease Mechanisms, and Laboratory of Learning and Memory, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China. Electronic address: lxu@vip.163.com.
¹¹ Beijing Engineering Research Center of Radiographic Techniques and Equipment, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, 100049, China; School of Nuclear Science and Technology, University of Chinese Academy of Sciences, Beijing, 100049, China; CAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai, China. Electronic address: shanbc@ihep.ac.cn.

PMID: 30408597
DOI: 10.1016/j.neuroimage.2018.11.003

Abstract

Metabolic brain network, which is based on functional correlation patterns of ¹⁸F-fluorodeoxyglucose (FDG) positron emission tomography (PET) images, has been widely applied in both basic and clinical neuroscience. Exploring the properties of the metabolic brain network can provide valuable insight to the physiologic and pathologic processes of the brain. Based on the network theory, modular architecture has the ability to limit the spread of local perturbation impact and therefore modular networks are more robust against external damage. However, whether the metabolic brain network has modular architecture remains unknown.

Methods: 77 rats performed ¹⁸F-FDG PET brain imaging. The metabolic brain network was then constructed by measuring interregional metabolic correlation in inter-subject manner. Afterwards, modular architecture of the network was detected by a greedy algorithm. Further, we perturbed the metabolic brain network by inducing focal photothrombotic ischemia in the bilateral motor cortex and then measured the glucose metabolic change of each brain region using FDG-PET.

Results: A significant modular architecture was found in the metabolic brain network. The network could be divided into four modules which corresponding approximately to executive, learning/memory, visual/auditory and sensorimotor processing functional domains. After inducing the focal ischemia on the bilateral motor cortex, most of the significantly changed brain regions (13 of 17) belong to the sensorimotor module.

Conclusion: Our results revealed an inherent modular architecture in the metabolic brain network and gave an experimental evidence that the modularity of the metabolism brain network could limit the spread of local perturbation impact.

Keywords: Brain network; FDG-PET; Metabolic connectivity; Modularity; Perturbation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brain / diagnostic imaging
Brain / metabolism*
Brain / physiopathology
Brain Ischemia / diagnostic imaging
Brain Ischemia / metabolism*
Brain Ischemia / physiopathology
Fluorodeoxyglucose F18
Male
Motor Cortex / diagnostic imaging
Motor Cortex / metabolism
Motor Cortex / physiopathology
Nerve Net / diagnostic imaging
Nerve Net / metabolism*
Nerve Net / physiopathology
Positron-Emission Tomography / methods*
Rats
Rats, Sprague-Dawley

Substances

Fluorodeoxyglucose F18