Mitigating head motion artifact in functional connectivity MRI

Participant motion during functional magnetic resonance image (fMRI) acquisition produces spurious signal fluctuations that can confound measures of functional connectivity. Without mitigation, motion artifact can bias statistical inferences about relationships between connectivity and individual differences. To counteract motion artifact, this protocol describes the implementation of a validated, high-performance denoising strategy that combines a set of model features, including physiological signals, motion estimates, and mathematical expansions, to target both widespread and focal effects of subject movement. This protocol can be used to reduce motion-related variance to near zero in studies of functional connectivity, providing up to a 100-fold improvement over minimal-processing approaches in large datasets. Image denoising requires 40 min to 4 h of computing per image, depending on model specifications and data dimensionality. The protocol additionally includes instructions for assessing the performance of a denoising strategy. Associated software implements all denoising and diagnostic procedures, using a combination of established image-processing libraries and the eXtensible Connectivity Pipeline (XCP) software.Ciric et al. describe a protocol for the removal of motion artifacts from functional MRI data. They introduce a software package that implements common denoising protocols and provides tools for assessing the efficacy of denoising.

[1]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[2]  D. Bassett,et al.  Emergence of system roles in normative neurodevelopment , 2015, Proceedings of the National Academy of Sciences.

[3]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[4]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

[5]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[6]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[7]  Timothy O. Laumann,et al.  Evaluation of Denoising Strategies to Address Motion-Correlated Artifacts in Resting-State Functional Magnetic Resonance Imaging Data from the Human Connectome Project , 2016, Brain Connect..

[8]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[9]  Efstathios D. Gennatas,et al.  Linked Sex Differences in Cognition and Functional Connectivity in Youth. , 2015, Cerebral cortex.

[10]  Timothy O. Laumann,et al.  Sources and implications of whole-brain fMRI signals in humans , 2017, NeuroImage.

[11]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[12]  Ben D. Fulcher,et al.  An evaluation of the efficacy, reliability, and sensitivity of motion correction strategies for resting-state functional MRI , 2017, NeuroImage.

[13]  Yong He,et al.  Addressing head motion dependencies for small-world topologies in functional connectomics , 2013, Front. Hum. Neurosci..

[14]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[15]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[16]  Evan M. Gordon,et al.  Local-Global Parcellation of the Human Cerebral Cortex From Intrinsic Functional Connectivity MRI , 2017, bioRxiv.

[17]  Jonathan D. Power A simple but useful way to assess fMRI scan qualities , 2017, NeuroImage.

[18]  N. Lomb Least-squares frequency analysis of unequally spaced data , 1976 .

[19]  J. Kable,et al.  Common Dimensional Reward Deficits Across Mood and Psychotic Disorders: A Connectome-Wide Association Study. , 2017, The American journal of psychiatry.

[20]  Kevin Murphy,et al.  Removing motion and physiological artifacts from intrinsic BOLD fluctuations using short echo data , 2013, NeuroImage.

[21]  Patric Hagmann,et al.  Mapping the human connectome at multiple scales with diffusion spectrum MRI , 2012, Journal of Neuroscience Methods.

[22]  Joshua Carp,et al.  Optimizing the order of operations for movement scrubbing: Comment on Power et al. , 2013, NeuroImage.

[23]  Beatriz Luna,et al.  The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity , 2013, NeuroImage.

[24]  Timothy O. Laumann,et al.  Generation and Evaluation of a Cortical Area Parcellation from Resting-State Correlations. , 2016, Cerebral cortex.

[25]  Sherif M. Gaweesh,et al.  Characteristics and mitigation strategies for cell phone use while driving among young drivers in Qatar , 2018 .

[26]  Abraham Z. Snyder,et al.  Real-time motion analytics during brain MRI improve data quality and reduce costs , 2017, NeuroImage.

[27]  Arno Klein,et al.  Large-scale evaluation of ANTs and FreeSurfer cortical thickness measurements , 2014, NeuroImage.

[28]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[29]  Vince D. Calhoun,et al.  Save the Global: Global Signal Connectivity as a Tool for Studying Clinical Populations with Functional Magnetic Resonance Imaging , 2014, Brain Connect..

[30]  S. M. Steve SUSAN - a new approach to low level image processing , 1997 .

[31]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[32]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[33]  Satrajit S. Ghosh,et al.  FMRIPrep: a robust preprocessing pipeline for functional MRI , 2018, bioRxiv.

[34]  P. Mahadevan,et al.  An overview , 2007, Journal of Biosciences.

[35]  M. Dylan Tisdall,et al.  Quantitative assessment of structural image quality , 2018, NeuroImage.

[36]  Damien A. Fair,et al.  Behavioral interventions for reducing head motion during MRI scans in children , 2018, NeuroImage.

[37]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[38]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.

[39]  John Suckling,et al.  A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series , 2014, NeuroImage.

[40]  Danielle S Bassett,et al.  Motion artifact in studies of functional connectivity: Characteristics and mitigation strategies , 2019, Human brain mapping.

[41]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[42]  Maarten Mennes,et al.  Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI , 2015, NeuroImage.

[43]  Christos Davatzikos,et al.  Heterogeneous impact of motion on fundamental patterns of developmental changes in functional connectivity during youth , 2013, NeuroImage.

[44]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[45]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[46]  Jonathan D. Power,et al.  Recent progress and outstanding issues in motion correction in resting state fMRI , 2015, NeuroImage.

[47]  Noah D. Brenowitz,et al.  Integrated strategy for improving functional connectivity mapping using multiecho fMRI , 2013, Proceedings of the National Academy of Sciences.

[48]  Christos Davatzikos,et al.  Neuroimaging of the Philadelphia Neurodevelopmental Cohort , 2014, NeuroImage.

[49]  Hang Joon Jo,et al.  Effective Preprocessing Procedures Virtually Eliminate Distance-Dependent Motion Artifacts in Resting State FMRI , 2013, J. Appl. Math..

[50]  L. Kiemeney,et al.  Obesity, metabolic factors and risk of different histological types of lung cancer: A Mendelian randomization study , 2017, PloS one.

[51]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[52]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[53]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[54]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[55]  Satrajit S. Ghosh,et al.  The brain imaging data structure, a format for organizing and describing outputs of neuroimaging experiments , 2016, Scientific Data.

[56]  NeuroData,et al.  Towards Automated Analysis of Connectomes: The Configurable Pipeline for the Analysis of Connectomes , 2015 .

[57]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Bing Chen,et al.  An open science resource for establishing reliability and reproducibility in functional connectomics , 2014, Scientific Data.

[59]  Mary Beth Nebel,et al.  Reduction of motion-related artifacts in resting state fMRI using aCompCor , 2014, NeuroImage.

[60]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[61]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[62]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[63]  Jonathan D. Power,et al.  Temporal interpolation alters motion in fMRI scans: Magnitudes and consequences for artifact detection , 2017, PloS one.

[64]  Y. Zang,et al.  Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI , 2007, Brain and Development.

[65]  Soroosh Afyouni,et al.  Insight and Inference for DVARS , 2017 .

[66]  Yingli Lu,et al.  Regional homogeneity approach to fMRI data analysis , 2004, NeuroImage.

[67]  Kevin Murphy,et al.  Towards a consensus regarding global signal regression for resting state functional connectivity MRI , 2017, NeuroImage.

[68]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[69]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[70]  Li Qingyang,et al.  Towards Automated Analysis of Connectomes: The Configurable Pipeline for the Analysis of Connectomes (C-PAC) , 2013 .

[71]  Abraham Z. Snyder,et al.  Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to Carp , 2013, NeuroImage.

[72]  Fred Tam,et al.  Retrospective coregistration of functional magnetic resonance imaging data using external monitoring , 2005, Magnetic resonance in medicine.

[73]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

[74]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[75]  Dost Öngür,et al.  Anticorrelations in resting state networks without global signal regression , 2012, NeuroImage.

[76]  Michael W. Cole,et al.  Altered global brain signal in schizophrenia , 2014, Proceedings of the National Academy of Sciences.

[77]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[78]  Jonathan D. Power,et al.  Ridding fMRI data of motion-related influences: Removal of signals with distinct spatial and physical bases in multiecho data , 2018, Proceedings of the National Academy of Sciences.

[79]  Thomas E. Nichols Notes on Creating a Standardized Version of DVARS , 2017, 1704.01469.

[80]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[81]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[82]  Christos Davatzikos,et al.  GraSP: Geodesic Graph-based Segmentation with Shape Priors for the functional parcellation of the cortex , 2015, NeuroImage.

[83]  Timothy O. Laumann,et al.  On Global fMRI Signals and Simulations , 2017, Trends in Cognitive Sciences.

[84]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[85]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[86]  Simon J Graham,et al.  A robust method for suppressing motion-induced coil sensitivity variations during prospective correction of head motion in fMRI. , 2016, Magnetic resonance imaging.

[87]  L. Lemieux,et al.  Modelling large motion events in fMRI studies of patients with epilepsy. , 2007, Magnetic resonance imaging.

[88]  Jordan M. Malof,et al.  Distributed solar photovoltaic array location and extent dataset for remote sensing object identification , 2016, Scientific Data.

[89]  Richard F. Betzel,et al.  Linked dimensions of psychopathology and connectivity in functional brain networks , 2017, bioRxiv.

[90]  D. Hu,et al.  Neurobiological basis of head motion in brain imaging , 2014, Proceedings of the National Academy of Sciences.

[91]  D. Carone,et al.  Impact of automated ICA-based denoising of fMRI data in acute stroke patients , 2017, NeuroImage: Clinical.

[92]  Christos Davatzikos,et al.  Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity , 2017, NeuroImage.