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Spatial and temporal autocorrelation weave complexity in brain networks

View ORCID ProfileMaxwell Shinn, Amber Hu, Laurel Turner, Stephanie Noble, Katrin H. Preller, Jie Lisa Ji, Flora Moujaes, Sophie Achard, Dustin Scheinost, View ORCID ProfileR. Todd Constable, John H. Krystal, Franz X. Vollenweider, Daeyeol Lee, Alan Anticevic, Edward T. Bullmore, View ORCID ProfileJohn D. Murray
doi: https://doi.org/10.1101/2021.06.01.446561
Maxwell Shinn
1Interdepartmental Neuroscience Program, Yale University
2Department of Psychiatry, Yale University
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Amber Hu
3Yale College, Yale University
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Laurel Turner
3Yale College, Yale University
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Stephanie Noble
4Department of Radiology and Biomedical Imaging, Yale University
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Katrin H. Preller
2Department of Psychiatry, Yale University
5Department of Psychiatry, Psychotherapy and Psychosomatics, University Hospital for Psychiatry, Zurich
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Jie Lisa Ji
2Department of Psychiatry, Yale University
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Flora Moujaes
5Department of Psychiatry, Psychotherapy and Psychosomatics, University Hospital for Psychiatry, Zurich
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Sophie Achard
6University of Grenoble Alpes, CNRS, Inria, Grenoble INP, LJK, 38000 Grenoble, France
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Dustin Scheinost
1Interdepartmental Neuroscience Program, Yale University
4Department of Radiology and Biomedical Imaging, Yale University
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R. Todd Constable
1Interdepartmental Neuroscience Program, Yale University
4Department of Radiology and Biomedical Imaging, Yale University
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John H. Krystal
2Department of Psychiatry, Yale University
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Franz X. Vollenweider
5Department of Psychiatry, Psychotherapy and Psychosomatics, University Hospital for Psychiatry, Zurich
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Daeyeol Lee
7Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University
8Kavli Discovery Neuroscience Institute, Johns Hopkins University
9Department of Psychological and Brain Sciences, Johns Hopkins University
10Department of Neuroscience, Johns Hopkins University
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Alan Anticevic
1Interdepartmental Neuroscience Program, Yale University
2Department of Psychiatry, Yale University
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Edward T. Bullmore
11Department of Psychiatry, University of Cambridge
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John D. Murray
1Interdepartmental Neuroscience Program, Yale University
2Department of Psychiatry, Yale University
12Department of Physics, Yale University
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  • For correspondence: [email protected]
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Abstract

High-throughput experimental methods in neuroscience have led to an explosion of techniques for measuring complex interactions and multi-dimensional patterns. However, whether sophisticated measures of emergent phenomena can be traced back to simpler low-dimensional statistics is largely unknown. To explore this question, we examine resting state fMRI (rs-fMRI) data using complex topology measures from network neuroscience. We show that spatial and temporal autocorrelation are reliable statistics which explain numerous measures of network topology. Surrogate timeseries with subject-matched spatial and temporal autocorrelation capture nearly all reliable individual and regional variation in these topology measures. Network topology changes during aging are driven by spatial autocorrelation, and multiple serotonergic drugs causally induce the same topographic change in temporal autocorrelation. This reductionistic interpretation of widely-used complexity measures may help link them to neurobiology.

Competing Interest Statement

KHP is currently an employee of Hoffmann-La Roche. JHK has consulting agreements (less than US\$5,000 per year) with the following: Aptinyx, Inc.; Atai Life Sciences; AstraZeneca Pharmaceuticals; Biogen, Idec, MA; Biomedisyn Corporation; Bionomics, Limited (Australia); Boehringer Ingelheim International; Cadent Therapeutics, Inc.; Clexio Bioscience, Ltd.; COMPASS Pathways, Limited, United Kingdom; Concert Pharmaceuticals, Inc.; Epiodyne, Inc.; EpiVario, Inc.; Greenwich Biosciences, Inc.; Heptares Therapeutics, Limited (UK); Janssen Research \& Development; Jazz Pharmaceuticals, Inc.; Otsuka America Pharmaceutical, Inc.; Perception Neuroscience Holdings, Inc.; Spring Care, Inc.; Sunovion Pharmaceuticals, Inc.; Takeda Industries; Taisho Pharmaceutical Co., Ltd. JHK serves on the scientific advisory boards of Biohaven Pharmaceuticals; BioXcel Therapeutics, Inc. (Clinical Advisory Board); Cadent Therapeutics, Inc. (Clinical Advisory Board); Cerevel Therapeutics, LLC; EpiVario, Inc.; Eisai, Inc.; Jazz Pharmaceuticals, Inc.; Lohocla Research Corporation; Novartis Pharmaceuticals Corporation; PsychoGenics, Inc.; Neumora Therapeutics, Inc.; Tempero Bio, Inc.; Terran Biosciences, Inc. JHK is on the board of directors of Freedom Biosciences, Inc. JHK has stock and/or stock options in Biohaven Pharmaceuticals; Sage Pharmaceuticals; Spring Care, Inc.; Biohaven Pharmaceuticals Medical Sciences; EpiVario, Inc.; Neumora Therapeutics, Inc.; Terran Biosciences, Inc.; Tempero Bio, Inc. JHK is editor of Biological Psychiatry with income greater than \$10,000. DL is a co-founder of Neurogazer Inc. AA and JDM are co-founders of Manifest Technologies, serve on the technical advisory board of Neumora Therapeutics, and are consultants for Gilgamesh Pharmaceuticals. ETB serves on the scientific advisory board of Sosei Heptares and as a consultant for GlaxoSmithKline.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 09, 2022.
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Spatial and temporal autocorrelation weave complexity in brain networks
Maxwell Shinn, Amber Hu, Laurel Turner, Stephanie Noble, Katrin H. Preller, Jie Lisa Ji, Flora Moujaes, Sophie Achard, Dustin Scheinost, R. Todd Constable, John H. Krystal, Franz X. Vollenweider, Daeyeol Lee, Alan Anticevic, Edward T. Bullmore, John D. Murray
bioRxiv 2021.06.01.446561; doi: https://doi.org/10.1101/2021.06.01.446561
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Spatial and temporal autocorrelation weave complexity in brain networks
Maxwell Shinn, Amber Hu, Laurel Turner, Stephanie Noble, Katrin H. Preller, Jie Lisa Ji, Flora Moujaes, Sophie Achard, Dustin Scheinost, R. Todd Constable, John H. Krystal, Franz X. Vollenweider, Daeyeol Lee, Alan Anticevic, Edward T. Bullmore, John D. Murray
bioRxiv 2021.06.01.446561; doi: https://doi.org/10.1101/2021.06.01.446561

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