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Compressed sensorimotor-to-transmodal hierarchical organization in schizophrenia

Published online by Cambridge University Press:  08 June 2021

Debo Dong Open the ORCID record for Debo Dong [Opens in a new window] ,
Dezhong Yao ,
Yulin Wang ,
Seok-Jun Hong ,
Sarah Genon ,
Fei Xin ,
Kyesam Jung ,
Hui He ,
Xuebin Chang  and
Mingjun Duan
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Debo Dong
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China
Dezhong Yao
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu, China
Yulin Wang
Affiliation:
Faculty of Psychological and Educational Sciences, Department of Experimental and Applied Psychology, Vrije Universiteit Brussel, Belgium Faculty of Psychology and Educational Sciences, Department of Data Analysis, Ghent University, Belgium
Seok-Jun Hong
Affiliation:
Center for the Developing Brain, Child Mind Institute, NY, USA Department of Biomedical Engineering, Center for Neuroscience Imaging Research, Institute for Basic Science, Sungkyunkwan University, South Korea
Sarah Genon
Affiliation:
Institute for Systems Neuroscience, Heinrich Heine University Düsseldorf, Düsseldorf, Germany Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany
Fei Xin
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China
Kyesam Jung
Affiliation:
Institute for Systems Neuroscience, Heinrich Heine University Düsseldorf, Düsseldorf, Germany Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany
Hui He
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China Department of Psychiatry, The Fourth People's Hospital of Chengdu, Chengdu, China
Xuebin Chang
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China
Mingjun Duan
Affiliation:
Department of Psychiatry, The Fourth People's Hospital of Chengdu, Chengdu, China
Boris C. Bernhardt
Affiliation:
Multimodal Imaging and Connectome Analysis Lab, McConnell Brain Imaging Centre, Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec, Canada
Daniel S. Margulies
Affiliation:
Centre National de la Recherche Scientifique (CNRS) UMR 7225, Institut du Cerveau et de la Moelle épinière, Paris, France
Jorge Sepulcre
Affiliation:
Department of Radiology, Gordon Center for Medical Imaging, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA, USA
Simon B. Eickhoff
Affiliation:
Institute for Systems Neuroscience, Heinrich Heine University Düsseldorf, Düsseldorf, Germany Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany
Cheng Luo*
Affiliation:
The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, School of Life Science and Technology, University of Electronic Science and Technology of China, China Department of Neurology, Brain Disorders and Brain Function Key Laboratory, First Affiliated Hospital of Hainan Medical University, Haikou, China
*
Author for correspondence: Cheng Luo, E-mail: chengluo@uestc.edu.cn
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Abstract

Background

Schizophrenia has been primarily conceptualized as a disorder of high-order cognitive functions with deficits in executive brain regions. Yet due to the increasing reports of early sensory processing deficit, recent models focus more on the developmental effects of impaired sensory process on high-order functions. The present study examined whether this pathological interaction relates to an overarching system-level imbalance, specifically a disruption in macroscale hierarchy affecting integration and segregation of unimodal and transmodal networks.

Methods

We applied a novel combination of connectome gradient and stepwise connectivity analysis to resting-state fMRI to characterize the sensorimotor-to-transmodal cortical hierarchy organization (96 patients v. 122 controls).

Results

We demonstrated compression of the cortical hierarchy organization in schizophrenia, with a prominent compression from the sensorimotor region and a less prominent compression from the frontal−parietal region, resulting in a diminished separation between sensory and fronto-parietal cognitive systems. Further analyses suggested reduced differentiation related to atypical functional connectome transition from unimodal to transmodal brain areas. Specifically, we found hypo-connectivity within unimodal regions and hyper-connectivity between unimodal regions and fronto-parietal and ventral attention regions along the classical sensation-to-cognition continuum (voxel-level corrected, p < 0.05).

Conclusions

The compression of cortical hierarchy organization represents a novel and integrative system-level substrate underlying the pathological interaction of early sensory and cognitive function in schizophrenia. This abnormal cortical hierarchy organization suggests cascading impairments from the disruption of the somatosensory−motor system and inefficient integration of bottom-up sensory information with attentional demands and executive control processes partially account for high-level cognitive deficits characteristic of schizophrenia.

Keywords

SchizophreniaCortical hierarchySomatosensory-motor systemFunctional connectivityConnectome gradientStepwise connectivity
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 3 , February 2023 , pp. 771 - 784
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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