title: Different topological organization of human brain functional networks with eyes open versus eyes closed.
abstract: Opening and closing the eyes are fundamental behaviors for directing attention to the external versus internal world. However, it remains unclear whether the states of eyes-open (EO) relative to eyes-closed (EC) are associated with different topological organizations of functional neural networks for exteroceptive and interoceptive processing (processing the external world and internal state, respectively). Here, we used resting-state functional magnetic resonance imaging and neural network analysis to investigate the topological properties of functional networks of the human brain when the eyes were open versus closed. The brain networks exhibited higher cliquishness and local efficiency, but lower global efficiency during the EO state compared to the EC state. These properties suggest an increase in specialized information processing along with a decrease in integrated information processing in EO (vs. EC). More importantly, the "exteroceptive" network, including the attentional system (e.g., superior parietal gyrus and inferior parietal lobule), ocular motor system (e.g., precentral gyrus and superior frontal gyrus), and arousal system (e.g., insula and thalamus), showed higher regional nodal properties (nodal degree, efficiency and betweenness centrality) in EO relative to EC. In contrast, the "interoceptive" network, composed of visual system (e.g., lingual gyrus, fusiform gyrus and cuneus), auditory system (e.g., Heschl's gyurs), somatosensory system (e.g., postcentral gyrus), and part of the default mode network (e.g., angular gyrus and anterior cingulate gyrus), showed significantly higher regional properties in EC vs. EO. In addition, the connections across sensory modalities were altered by volitional eye opening. The synchronicity between the visual system and the motor, somatosensory and auditory systems, characteristic of EC, was attenuated in EO. Further, the connections between the visual system and the attention, arousal and subcortical systems were increased in EO. These results may indicate that EO leads to a suppression of sensory modalities (other than visual) to allocate resources to exteroceptive processing. Our findings suggest that the topological organization of human brain networks dynamically switches corresponding to the information processing modes as we open or close our eyes.
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
authors.forename: Pengfei
authors.initials: P
authors.lastname: Xu
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China; Brain Imaging Center, Center for Studies of Psychological Application, Guangdong Key Laboratory of Mental Health and Cognitive Science, School of Psychology, South China Normal University, Guangzhou 510631, China. Electronic address: ruiwang.huang@gmail.com.
authors.forename: Ruiwang
authors.initials: R
authors.lastname: Huang
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
authors.forename: Jinhui
authors.initials: J
authors.lastname: Wang
authors.affiliation: Department of Psychiatry, New York University School of Medicine, New York, NY 10016, USA.
authors.forename: Nicholas T
authors.initials: NT
authors.lastname: Van Dam
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
authors.forename: Teng
authors.initials: T
authors.lastname: Xie
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
authors.forename: Zhangye
authors.initials: Z
authors.lastname: Dong
authors.affiliation: Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Chunping
authors.initials: C
authors.lastname: Chen
authors.affiliation: Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Ruolei
authors.initials: R
authors.lastname: Gu
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China; Center for Cognition and Brain Disorders, Affiliated Hospital, Hangzhou Normal University, Hangzhou 310015, China.
authors.forename: Yu-Feng
authors.initials: YF
authors.lastname: Zang
authors.affiliation: State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China; IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
authors.forename: Yong
authors.initials: Y
authors.lastname: He
authors.affiliation: Department of Psychology, Queens College, The City University of New York, New York, NY 11367, USA; Department of Psychiatry, Ichan School of Medicine at Mount Sinai, New York, NY 10029, USA; Fishberg Department of Neuroscience, Ichan School of Medicine at Mount Sinai, New York, NY 10029, USA; Friedman Brain Institute, Ichan School of Medicine at Mount Sinai, New York, NY 10029, USA.
authors.forename: Jin
authors.initials: J
authors.lastname: Fan
authors.affiliation: Institute of Affective and Social Neuroscience, Shenzhen University, Shenzhen 518060, China. Electronic address: luoyj@bnu.edu.cn.
authors.forename: Yue-jia
authors.initials: YJ
authors.lastname: Luo
mesh_terms: D001364:Awareness / Q000502:physiology*; D001921:Brain / Q000033:anatomy & histology* / Q000502:physiology; D001931:Brain Mapping; D005123:Eye; D005260:Female; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging; D008297:Male; D009415:Nerve Net / Q000033:anatomy & histology* / Q000502:physiology; D012146:Rest; D055815:Young Adult
keywords: Connectome; Exteroceptive; Graph theory; Interoceptive; Resting-state functional MRI