Common functional networks in the mouse brain revealed by multi-centre resting-state fMRI analysis

Joanes Grandjean; Carola Canella; Cynthia Anckaerts; Gülebru Ayrancı; Salma Bougacha; Thomas Bienert; David Buehlmann; Ludovico Coletta; Daniel Gallino; Natalia Gass; Clément M Garin; Nachiket Abhay Nadkarni; Neele S Hübner; Meltem Karatas; Yuji Komaki; Silke Kreitz; Francesca Mandino; Anna E Mechling; Chika Sato; Katja Sauer; Disha Shah; Sandra Strobelt; Norio Takata; Isabel Wank; Tong Wu; Noriaki Yahata; Ling Yun Yeow; Yohan Yee; Ichio Aoki; M Mallar Chakravarty; Wei-Tang Chang; Marc Dhenain; Dominik von Elverfeldt; Laura-Adela Harsan; Andreas Hess; Tianzi Jiang; Georgios A Keliris; Jason P Lerch; Andreas Meyer-Lindenberg; Hideyuki Okano; Markus Rudin; Alexander Sartorius; Annemie Van der Linden; Marleen Verhoye; Wolfgang Weber-Fahr; Nicole Wenderoth; Valerio Zerbi; Alessandro Gozzi

doi:10.1016/j.neuroimage.2019.116278

Common functional networks in the mouse brain revealed by multi-centre resting-state fMRI analysis

Neuroimage. 2020 Jan 15:205:116278. doi: 10.1016/j.neuroimage.2019.116278. Epub 2019 Oct 12.

Authors

Joanes Grandjean¹, Carola Canella², Cynthia Anckaerts³, Gülebru Ayrancı⁴, Salma Bougacha⁵, Thomas Bienert⁶, David Buehlmann⁷, Ludovico Coletta², Daniel Gallino⁴, Natalia Gass⁸, Clément M Garin⁵, Nachiket Abhay Nadkarni⁵, Neele S Hübner⁶, Meltem Karatas⁹, Yuji Komaki¹⁰, Silke Kreitz¹¹, Francesca Mandino¹², Anna E Mechling⁶, Chika Sato¹³, Katja Sauer¹¹, Disha Shah¹⁴, Sandra Strobelt¹¹, Norio Takata¹⁵, Isabel Wank¹¹, Tong Wu¹⁶, Noriaki Yahata¹³, Ling Yun Yeow¹⁷, Yohan Yee¹⁸, Ichio Aoki¹³, M Mallar Chakravarty¹⁹, Wei-Tang Chang¹⁷, Marc Dhenain⁵, Dominik von Elverfeldt⁶, Laura-Adela Harsan²⁰, Andreas Hess¹¹, Tianzi Jiang²¹, Georgios A Keliris³, Jason P Lerch²², Andreas Meyer-Lindenberg²³, Hideyuki Okano²⁴, Markus Rudin²⁵, Alexander Sartorius⁸, Annemie Van der Linden³, Marleen Verhoye³, Wolfgang Weber-Fahr⁸, Nicole Wenderoth²⁶, Valerio Zerbi²⁶, Alessandro Gozzi²⁷

Affiliations

¹ Singapore Bioimaging Consortium, Agency for Science, Technology and Research, 11 Biopolis Way, 138667, Singapore. Electronic address: Joanes.Grandjean@radboudumc.nl.
² Functional Neuroimaging Laboratory, Istituto Italiano di Tecnologia, Centre for Neuroscience and Cognitive Systems @ UNITN, 38068, Rovereto, Italy; CIMeC, Centre for Mind/Brain Sciences, University of Trento, 38068, Rovereto, Italy.
³ Bio-Imaging Lab, University of Antwerp, CDE, Universiteitsplein 1, 2610, Antwerp, Belgium.
⁴ Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada.
⁵ Commissariat à l'Énergie Atomique et Aux Énergies Alternatives (CEA), Direction de la Recherche Fondamentale (DRF), Institut François Jacob, MIRCen, Fontenay-aux-roses, France; Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud, Université Paris-Saclay UMR 9199, Neurodegenerative Diseases Laboratory, Fontenay-aux-Roses, France.
⁶ Department of Radiology, Medical Physics, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Killianstr. 5a, 79106, Freiburg, Germany; BrainLinks-BrainTools Cluster of Excellence, University of Freiburg, Georges-Köhler-Allee 80, 79110, Freiburg, Germany.
⁷ Institute for Biomedical Engineering, University and ETH Zürich, Wolfgang-Pauli-Str. 27, 8093, Zürich, Switzerland.
⁸ Department of Neuroimaging, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, Germany.
⁹ Department of Radiology, Medical Physics, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Killianstr. 5a, 79106, Freiburg, Germany; The Engineering Science, Computer Science and Imaging Laboratory (ICube), Department of Biophysics and Nuclear Medicine, University of Strasbourg and University Hospital of Strasbourg, 67000, Strasbourg, France.
¹⁰ Central Institute for Experimental Animals (CIEA), 3-25-12, Tonomachi, Kawasaki, Kanagawa, 210-0821, Japan; Department of Physiology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan.
¹¹ Institute of Experimental and Clinical Pharmacology and Toxicology, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Fahrstraße 17, 91054, Erlangen, Germany.
¹² Singapore Bioimaging Consortium, Agency for Science, Technology and Research, 11 Biopolis Way, 138667, Singapore; Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.
¹³ Functional and Molecular Imaging Team, Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Anagawa 4-9-1, Inage, Chiba-city, Chiba, 263-8555, Japan.
¹⁴ Bio-Imaging Lab, University of Antwerp, CDE, Universiteitsplein 1, 2610, Antwerp, Belgium; Laboratory for the Research of Neurodegenerative Diseases, VIB Center for Brain and Disease Research, KU Leuven, O&N4 Herestraat 49 Box 602, 3000, Leuven, Belgium.
¹⁵ Central Institute for Experimental Animals (CIEA), 3-25-12, Tonomachi, Kawasaki, Kanagawa, 210-0821, Japan; Department of Neuropsychiatry, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan.
¹⁶ Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia; Centre for Medical Image Computing, Department of Computer Science, & Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK; Computational, Cognitive and Clinical Imaging Lab, Division of Brain Sciences, Department of Medicine, Imperial College London, W12 0NN, UK; UK DRI Centre for Care Research and Technology, Imperial College London, W12 0NN, UK.
¹⁷ Singapore Bioimaging Consortium, Agency for Science, Technology and Research, 11 Biopolis Way, 138667, Singapore.
¹⁸ Hospital for Sick Children and Department of Medical Biophysics, The University of Toronto, Toronto, Ontario, Canada.
¹⁹ Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada; Department of Psychiatry, McGill University, Montreal, Quebec, Canada; Department of Biological and Biomedical Engineering, McGill University, Montreal, Quebec, Canada.
²⁰ The Engineering Science, Computer Science and Imaging Laboratory (ICube), Department of Biophysics and Nuclear Medicine, University of Strasbourg and University Hospital of Strasbourg, 67000, Strasbourg, France.
²¹ Queensland Brain Institute, The University of Queensland, Brisbane, Queensland, Australia; Brainnetome Center & National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China.
²² Hospital for Sick Children and Department of Medical Biophysics, The University of Toronto, Toronto, Ontario, Canada; Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, OX3 9DU, UK.
²³ Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany.
²⁴ Department of Physiology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan; Laboratory for Marmoset Neural Architecture, RIKEN Brain Science Institute, Wako, Saitama, 351-0198, Japan.
²⁵ Institute for Biomedical Engineering, University and ETH Zürich, Wolfgang-Pauli-Str. 27, 8093, Zürich, Switzerland; Institute of Pharmacology and Toxicology, University of Zürich, Winterthurerstrasse 190, 8057, Zürich, Switzerland; Neuroscience Center Zürich, ETH Zürich and University of Zürich, Zürich, Switzerland.
²⁶ Neural Control of Movement Lab, Department of Health Sciences and Technology, ETH Zürich, Winterthurerstrasse 190, 8057, Zurich, Switzerland; Neuroscience Center Zürich, ETH Zürich and University of Zürich, Zürich, Switzerland.
²⁷ Functional Neuroimaging Laboratory, Istituto Italiano di Tecnologia, Centre for Neuroscience and Cognitive Systems @ UNITN, 38068, Rovereto, Italy.

Abstract

Preclinical applications of resting-state functional magnetic resonance imaging (rsfMRI) offer the possibility to non-invasively probe whole-brain network dynamics and to investigate the determinants of altered network signatures observed in human studies. Mouse rsfMRI has been increasingly adopted by numerous laboratories worldwide. Here we describe a multi-centre comparison of 17 mouse rsfMRI datasets via a common image processing and analysis pipeline. Despite prominent cross-laboratory differences in equipment and imaging procedures, we report the reproducible identification of several large-scale resting-state networks (RSN), including a mouse default-mode network, in the majority of datasets. A combination of factors was associated with enhanced reproducibility in functional connectivity parameter estimation, including animal handling procedures and equipment performance. RSN spatial specificity was enhanced in datasets acquired at higher field strength, with cryoprobes, in ventilated animals, and under medetomidine-isoflurane combination sedation. Our work describes a set of representative RSNs in the mouse brain and highlights key experimental parameters that can critically guide the design and analysis of future rodent rsfMRI investigations.

Keywords: Connectome; Default-mode network; Functional connectivity; ICA; Seed-based.

Publication types

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

MeSH terms

Animals
Brain / diagnostic imaging
Brain / physiology*
Connectome / methods*
Connectome / standards
Female
Image Processing, Computer-Assisted / methods*
Image Processing, Computer-Assisted / standards
Magnetic Resonance Imaging / methods*
Magnetic Resonance Imaging / standards
Male
Mice
Mice, Inbred C57BL
Nerve Net / diagnostic imaging
Nerve Net / physiology*
Reproducibility of Results

Grants and funding

802371/ERC_/European Research Council/International