Evaluating the sensitivity of functional connectivity measures to motion artifact in resting-state fMRI data

Functional connectivity (FC) networks are typically inferred from resting-state fMRI data using the Pearson correlation between BOLD time series from pairs of brain regions. However, alternative methods of estimating functional connectivity have not been systematically tested for their sensitivity or robustness to head motion artifact. Here, we evaluate the sensitivity of eight different functional connectivity measures to motion artifact using resting-state data from the Human Connectome Project. We report that FC estimated using full correlation has a relatively high residual distance-dependent relationship with motion compared to partial correlation, coherence, and information theory-based measures, even after implementing rigorous methods for motion artifact mitigation. This disadvantage of full correlation, however, may be offset by higher test-retest reliability, fingerprinting accuracy, and system identifiability. FC estimated by partial correlation offers the best of both worlds, with low sensitivity to motion artifact and intermediate system identifiability, with the caveat of low test-retest reliability and fingerprinting accuracy. We highlight spatial differences in the sub-networks affected by motion with different FC metrics. Further, we report that intra-network edges in the default mode and retrosplenial temporal sub-networks are highly correlated with motion in all FC methods. Our findings indicate that the method of estimating functional connectivity is an important consideration in resting-state fMRI studies and must be chosen carefully based on the parameters of the study.

[1]  Edward T. Bullmore,et al.  A simple view of the brain through a frequency-specific functional connectivity measure , 2008, NeuroImage.

[2]  Kristin A. Linn,et al.  The extent and drivers of gender imbalance in neuroscience reference lists , 2020, Nature Neuroscience.

[3]  Tristan A. Chaplin,et al.  Cortical circuits for integration of self-motion and visual-motion signals , 2019, Current Opinion in Neurobiology.

[4]  Dustin Scheinost,et al.  A decade of test-retest reliability of functional connectivity: A systematic review and meta-analysis , 2019, NeuroImage.

[5]  Jasmine Hect,et al.  Hubs in the human fetal brain network , 2018, Developmental Cognitive Neuroscience.

[6]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[7]  D. Freedman,et al.  On the histogram as a density estimator:L2 theory , 1981 .

[8]  Edward T. Bullmore,et al.  Low-dimensional morphospace of topological motifs in human fMRI brain networks , 2018, Network Neuroscience.

[9]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[10]  Wei Gao,et al.  Frontal parietal control network regulates the anti‐correlated default and dorsal attention networks , 2012, Human brain mapping.

[11]  E. Bullmore,et al.  Wavelets and functional magnetic resonance imaging of the human brain , 2004, NeuroImage.

[12]  Leonardo A. Molina,et al.  Vision and Locomotion Combine to Drive Path Integration Sequences in Mouse Retrosplenial Cortex , 2020, Current Biology.

[13]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[14]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[15]  M E J Newman,et al.  Modularity and community structure in networks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[17]  Joydeep Ghosh,et al.  Cluster Ensembles --- A Knowledge Reuse Framework for Combining Multiple Partitions , 2002, J. Mach. Learn. Res..

[18]  V. Traag,et al.  Community detection in networks with positive and negative links. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  S. Mitchell,et al.  Gendered Citation Patterns in International Relations Journals , 2013 .

[20]  C. Grady,et al.  Age differences in the functional interactions among the default, frontoparietal control, and dorsal attention networks , 2016, Neurobiology of Aging.

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

[22]  Ursula A. Tooley,et al.  Associations between Neighborhood SES and Functional Brain Network Development , 2018, Cerebral cortex.

[23]  Aslak Grinsted,et al.  Nonlinear Processes in Geophysics Application of the Cross Wavelet Transform and Wavelet Coherence to Geophysical Time Series , 2022 .

[24]  Edward T Bullmore,et al.  A Network Neuroscience Approach to Typical and Atypical Brain Development. , 2018, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[25]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[26]  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.

[27]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[28]  Koene R. A. Van Dijk,et al.  Frequency-Dependent Relationship Between Resting-State Functional Magnetic Resonance Imaging Signal Power and Head Motion Is Localized Within Distributed Association Networks , 2013, Brain Connect..

[29]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

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

[31]  Barbara F. Walter,et al.  The Gender Citation Gap in International Relations , 2013, International Organization.

[32]  Danielle S. Bassett,et al.  Multimodal network dynamics underpinning working memory , 2020, Nature Communications.

[33]  Richard F. Betzel,et al.  Modular Brain Networks. , 2016, Annual review of psychology.

[34]  E. Bullmore,et al.  Annual Research Review: Growth connectomics – the organization and reorganization of brain networks during normal and abnormal development , 2014, Journal of child psychology and psychiatry, and allied disciplines.

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

[36]  Jeffrey S Anderson,et al.  Network anticorrelations, global regression, and phase‐shifted soft tissue correction , 2011, Human brain mapping.

[37]  Danielle S. Bassett,et al.  Structural, geometric and genetic factors predict interregional brain connectivity patterns probed by electrocorticography , 2019, Nature Biomedical Engineering.

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

[39]  Jenifer Juranek,et al.  Children’s head motion during fMRI tasks is heritable and stable over time , 2017, Developmental Cognitive Neuroscience.

[40]  Lee M. Miller,et al.  Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data , 2004, NeuroImage.

[41]  Jonathan D. Power,et al.  Distinctions among real and apparent respiratory motions in human fMRI data , 2019, NeuroImage.

[42]  Neven Caplar,et al.  Quantitative evaluation of gender bias in astronomical publications from citation counts , 2016, Nature Astronomy.

[43]  B T Thomas Yeo,et al.  Towards a Universal Taxonomy of Macro-scale Functional Human Brain Networks , 2019, Brain Topography.

[44]  Elizabeth Jefferies,et al.  Individual variation in intentionality in the mind-wandering state is reflected in the integration of the default-mode, fronto-parietal, and limbic networks , 2017, NeuroImage.

[45]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

[46]  Steven Skiena,et al.  Name-ethnicity classification from open sources , 2009, KDD.

[47]  Bryant Duda,et al.  Distinct functional and structural neural underpinnings of working memory , 2018, NeuroImage.

[48]  Nicole Abaid,et al.  Comparing brain connectivity metrics: a didactic tutorial with a toy model and experimental data , 2018, Journal of neural engineering.

[49]  César Caballero-Gaudes,et al.  Methods for cleaning the BOLD fMRI signal , 2016, NeuroImage.

[50]  Anders M. Dale,et al.  Correction of respiratory artifacts in MRI head motion estimates , 2018, bioRxiv.

[51]  J. Rapoport,et al.  Simple models of human brain functional networks , 2012, Proceedings of the National Academy of Sciences.

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

[53]  Michelle L. Dion,et al.  Gendered Citation Patterns across Political Science and Social Science Methodology Fields , 2018, Political Analysis.

[54]  Gaurav Sood,et al.  Predicting Race and Ethnicity From the Sequence of Characters in a Name , 2018, 1805.02109.

[55]  Emery N. Brown,et al.  Model-based physiological noise removal in fast fMRI , 2020, NeuroImage.

[56]  Takanori Kochiyama,et al.  Causal relationship between effective connectivity within the default mode network and mind-wandering regulation and facilitation , 2016, NeuroImage.

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

[58]  R. Buckner,et al.  The brain’s default network: updated anatomy, physiology and evolving insights , 2019, Nature Reviews Neuroscience.

[59]  Pablo Jensen,et al.  Analysis of community structure in networks of correlated data. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[61]  Mark W. Woolrich,et al.  Optimising network modelling methods for fMRI , 2019, NeuroImage.

[62]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[63]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[64]  Karl J. Friston,et al.  A systematic framework for functional connectivity measures , 2014, Front. Neurosci..

[65]  A. Villringer,et al.  Weight loss reduces head motion: Revisiting a major confound in neuroimaging , 2020, Human brain mapping.

[66]  Lukas F Fischer,et al.  Representation of visual landmarks in retrosplenial cortex , 2019, bioRxiv.

[67]  Denise C. Park,et al.  Decreased segregation of brain systems across the healthy adult lifespan , 2014, Proceedings of the National Academy of Sciences.

[68]  Olaf Sporns,et al.  Weight-conserving characterization of complex functional brain networks , 2011, NeuroImage.

[69]  Santo Fortunato,et al.  Community detection in graphs , 2009, ArXiv.

[70]  E. Bullmore,et al.  Undirected graphs of frequency-dependent functional connectivity in whole brain networks , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[71]  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..

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

[73]  Timothy O. Laumann,et al.  Functional Brain Networks Are Dominated by Stable Group and Individual Factors, Not Cognitive or Daily Variation , 2018, Neuron.

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

[75]  B T Thomas Yeo,et al.  The modular and integrative functional architecture of the human brain , 2015, Proceedings of the National Academy of Sciences.

[76]  Peter B. Jones,et al.  Gene transcription profiles associated with inter-modular hubs and connection distance in human functional magnetic resonance imaging networks , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[77]  Peter B. Jones,et al.  373. Adolescence is Associated with Genomically Patterned Consolidation of the Hubs of the Human Brain Connectome , 2016, Biological Psychiatry.

[78]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

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

[80]  Steen Moeller,et al.  ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging , 2014, NeuroImage.

[81]  Alain de Cheveigné,et al.  Filters: When, Why, and How (Not) to Use Them , 2019, Neuron.

[82]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

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

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

[85]  Danielle S. Bassett,et al.  Choosing Wavelet Methods, Filters, and Lengths for Functional Brain Network Construction , 2015, PloS one.

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

[87]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[88]  Troy W. Margrie,et al.  A Circuit for Integration of Head- and Visual-Motion Signals in Layer 6 of Mouse Primary Visual Cortex , 2018, Neuron.

[89]  Danielle S Bassett,et al.  Mitigating head motion artifact in functional connectivity MRI , 2018, Nature Protocols.

[90]  Moriah E. Thomason,et al.  Development of Brain Networks In Utero: Relevance for Common Neural Disorders , 2020, Biological Psychiatry.

[91]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[92]  Wesley K. Thompson,et al.  MATLAB toolbox for functional connectivity , 2009, NeuroImage.

[93]  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.

[94]  Jasmine L. Hect,et al.  Sex differences in functional connectivity during fetal brain development , 2019, Developmental Cognitive Neuroscience.

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

[96]  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.