Measurement reliability for individual differences in multilayer network dynamics: Cautions and considerations

Multilayer network models have been proposed as an effective means of capturing the dynamic configuration of distributed neural circuits and quantitatively describing how communities vary over time. Beyond general insights into brain function, a growing number of studies have begun to employ these methods for the study of individua differences. However, test–retest reliabilities for multilayer network measures have yet to be fully quantified or optimized, potentially limiting their utility for individual difference studies. Here, we systematically evaluated the impact of multilayer community detection algorithms, selection of network parameters, scan duration, and task condition on test–retest reliabilities of multilayer network measures (i.e., flexibility, integration, and recruitment). A key finding was that the default method used for community detection by the popular generalized Louvain algorithm can generate erroneous results. Although available, an updated algorithm addressing this issue is yet to be broadly adopted in the neuroimaging literature. Beyond the algorithm, the present work identified parameter selection as a key determinant of test–retest reliability; however, optimization of these parameters and expected reliabilities appeared to be dataset-specific. Once parameters were optimized, consistent with findings from the static functional connectivity literature, scan duration was a much stronger determinant of reliability than scan condition. When the parameters were optimized and scan duration was sufficient, both passive (i.e., resting state, Inscapes, and movie) and active (i.e., flanker) tasks were reliable, although reliability in the movie watching condition was significantly higher than in the other three tasks. The minimal data requirement for achieving reliable measures for the movie watching condition was 20 min, and 30 min for the other three tasks. Our results caution the field against the use of default parameters without optimization based on the specific datasets to be employed – a process likely to be limited for most due to the lack of test–retest samples to enable parameter optimization.

[1]  Mary E. Meyerand,et al.  The effect of scan length on the reliability of resting-state fMRI connectivity estimates , 2013, NeuroImage.

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

[3]  Jano Moreira de Souza,et al.  Identifying Workgroups in Brazilian Scientific Social Networks , 2011, J. Univers. Comput. Sci..

[4]  Jiang Qiu,et al.  Verbal Creativity Is Correlated With the Dynamic Reconfiguration of Brain Networks in the Resting State , 2019, Front. Psychol..

[5]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[6]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[7]  Ahmad R. Hariri,et al.  General functional connectivity: Shared features of resting-state and task fMRI drive reliable and heritable individual differences in functional brain networks , 2018, NeuroImage.

[8]  Xi-Nian Zuo,et al.  Assessing Variations in Areal Organization for the Intrinsic Brain: From Fingerprints to Reliability , 2016, bioRxiv.

[9]  Amin Karbasi,et al.  There is no single functional atlas even for a single individual: Functional parcel definitions change with task , 2019, NeuroImage.

[10]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[11]  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.

[12]  Danielle S. Bassett,et al.  Functional Network Dynamics of the Language System , 2016, Cerebral cortex.

[13]  Mason A. Porter,et al.  Multilayer networks , 2013, J. Complex Networks.

[14]  Simone Kühn,et al.  Author Correction: Dynamic reconfiguration of functional brain networks during working memory training , 2020, Nature Communications.

[15]  Danielle S. Bassett,et al.  Dynamic flexibility in striatal-cortical circuits supports reinforcement learning , 2016 .

[16]  Dustin Scheinost,et al.  Considering factors affecting the connectome-based identification process: Comment on Waller et al. , 2018, NeuroImage.

[17]  Selin Aviyente,et al.  Tensor Based Temporal and Multilayer Community Detection for Studying Brain Dynamics During Resting State fMRI , 2019, IEEE Transactions on Biomedical Engineering.

[18]  Kun Bi,et al.  Early identification of bipolar from unipolar depression before manic episode: Evidence from dynamic rfMRI , 2019, Bipolar disorders.

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

[20]  X. Zuo,et al.  Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective , 2014, Neuroscience & Biobehavioral Reviews.

[21]  Kun Bi,et al.  Abnormal dynamic community structure of the salience network in depression , 2017, Journal of magnetic resonance imaging : JMRI.

[22]  Li Yao,et al.  The dynamic characteristics of the anterior cingulate cortex in resting-state fMRI of patients with depression. , 2018, Journal of affective disorders.

[23]  Carey E. Priebe,et al.  Eliminating accidental deviations to minimize generalization error: applications in connectomics and genomics , 2019, bioRxiv.

[24]  Jano Moreira de Souza,et al.  Mining and Analyzing Multirelational Social Networks , 2009, 2009 International Conference on Computational Science and Engineering.

[25]  Danielle S Bassett,et al.  Learning-induced autonomy of sensorimotor systems , 2014, Nature Neuroscience.

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

[27]  Jessica F. Cantlon,et al.  Neural Activity during Natural Viewing of Sesame Street Statistically Predicts Test Scores in Early Childhood , 2013, PLoS biology.

[28]  Evan M. Gordon,et al.  The community structure of functional brain networks exhibits scale-specific patterns of inter- and intra-subject variability , 2019, NeuroImage.

[29]  Xintao Hu,et al.  Test-retest reliability of functional connectivity networks during naturalistic fMRI paradigms , 2016, bioRxiv.

[30]  Yufeng Zang,et al.  Functional brain hubs and their test–retest reliability: A multiband resting-state functional MRI study , 2013, NeuroImage.

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

[32]  Jean M. Vettel,et al.  Time-evolving dynamics in brain networks forecast responses to health messaging , 2018, Network Neuroscience.

[33]  Z. Wang,et al.  The structure and dynamics of multilayer networks , 2014, Physics Reports.

[34]  Vince D. Calhoun,et al.  Questions and controversies in the study of time-varying functional connectivity in resting fMRI , 2020, Network Neuroscience.

[35]  O. Sporns Structure and function of complex brain networks , 2013, Dialogues in clinical neuroscience.

[36]  Amin Karbasi,et al.  Individualized functional networks reconfigure with cognitive state , 2020, NeuroImage.

[37]  D. Bassett,et al.  Dynamic reconfiguration of frontal brain networks during executive cognition in humans , 2015, Proceedings of the National Academy of Sciences.

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

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

[40]  Gaël Varoquaux,et al.  Benchmarking functional connectome-based predictive models for resting-state fMRI , 2019, NeuroImage.

[41]  Simon B. Eickhoff,et al.  Towards clinical applications of movie fMRI , 2020, NeuroImage.

[42]  Wei Gao,et al.  Task‐related modulation of functional connectivity variability and its behavioral correlations , 2015, Human brain mapping.

[43]  Jimeng Sun,et al.  MetaFac: community discovery via relational hypergraph factorization , 2009, KDD.

[44]  Danielle S Bassett,et al.  Evaluation of confound regression strategies for the mitigation of micromovement artifact in studies of dynamic resting-state functional connectivity and multilayer network modularity , 2019, Network Neuroscience.

[45]  Daniel S. Margulies,et al.  Common intrinsic connectivity states among posteromedial cortex subdivisions: Insights from analysis of temporal dynamics , 2014, NeuroImage.

[46]  Katherine L. Bottenhorn,et al.  Cooperating yet distinct brain networks engaged during naturalistic paradigms: A meta-analysis of functional MRI results , 2017, bioRxiv.

[47]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[48]  Qian Cui,et al.  Resting state functional network switching rate is differently altered in bipolar disorder and major depressive disorder , 2020, Human brain mapping.

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

[50]  Tom Michoel,et al.  Alignment and integration of complex networks by hypergraph-based spectral clustering , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  Patric Hagmann,et al.  Dynamic spatiotemporal patterns of brain connectivity reorganize across development , 2020, Network Neuroscience.

[52]  Pauline L. Baniqued,et al.  Aging Brain from a Network Science Perspective: Something to Be Positive About? , 2013, PloS one.

[53]  Kaixiang Zhuang,et al.  Brain flexibility associated with need for cognition contributes to creative achievement. , 2019, Psychophysiology.

[54]  Chaogan Yan,et al.  Concordance Among Indices of Intrinsic Brain Function: Insights from Inter-Individual Variation and Temporal Dynamics , 2016, bioRxiv.

[55]  Scott T. Grafton,et al.  Differential Recruitment of the Sensorimotor Putamen and Frontoparietal Cortex during Motor Chunking in Humans , 2012, Neuron.

[56]  R. Poldrack,et al.  Temporal metastates are associated with differential patterns of time-resolved connectivity, network topology, and attention , 2016, Proceedings of the National Academy of Sciences.

[57]  Benjamin H. Good,et al.  Performance of modularity maximization in practical contexts. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  Dustin Scheinost,et al.  Influences on the Test–Retest Reliability of Functional Connectivity MRI and its Relationship with Behavioral Utility , 2017, Cerebral cortex.

[59]  D. Bassett,et al.  Impact of childhood adversity on network reconfiguration dynamics during working memory in hypogonadal women , 2020, Psychoneuroendocrinology.

[60]  Brian Caffo,et al.  Comparing test-retest reliability of dynamic functional connectivity methods , 2017, NeuroImage.

[61]  Mason A. Porter,et al.  Robust Detection of Dynamic Community Structure in Networks , 2012, Chaos.

[62]  Simone Kühn,et al.  Dynamic reconfiguration of functional brain networks during working memory training , 2020, Nature Communications.

[63]  Mason A. Porter,et al.  Community Detection in Temporal Multilayer Networks, with an Application to Correlation Networks , 2014, Multiscale Model. Simul..

[64]  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.

[65]  Sharon L. Thompson-Schill,et al.  A Functional Cartography of Cognitive Systems , 2015, PLoS Comput. Biol..

[66]  Dane Taylor,et al.  Post-Processing Partitions to Identify Domains of Modularity Optimization , 2017, Algorithms.

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

[68]  Danielle S Bassett,et al.  Cohesive network reconfiguration accompanies extended training , 2017, Human brain mapping.

[69]  Xi-Nian Zuo,et al.  Harnessing reliability for neuroscience research , 2019, Nature Human Behaviour.

[70]  Lena S. Geiger,et al.  Dynamic brain network reconfiguration as a potential schizophrenia genetic risk mechanism modulated by NMDA receptor function , 2016, Proceedings of the National Academy of Sciences.

[71]  Simon B Eickhoff,et al.  Cooperating yet distinct brain networks engaged during naturalistic paradigms: A meta-analysis of functional MRI results , 2018, Network Neuroscience.

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

[73]  Jano Moreira de Souza,et al.  Modeling, Mining and Analysis of Multi-Relational Scientific Social Network , 2012, J. Univers. Comput. Sci..

[74]  Ahmad R. Hariri,et al.  What is the Test-Retest Reliability of Common Task-fMRI Measures? New Empirical Evidence and a Meta-Analysis , 2019, Biological Psychiatry.

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

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

[77]  Linda Geerligs,et al.  State and Trait Components of Functional Connectivity: Individual Differences Vary with Mental State , 2015, The Journal of Neuroscience.

[78]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[79]  Mason A. Porter,et al.  Task-Based Core-Periphery Organization of Human Brain Dynamics , 2012, PLoS Comput. Biol..

[80]  Danielle S. Bassett,et al.  Beyond modularity: Fine-scale mechanisms and rules for brain network reconfiguration , 2017, NeuroImage.

[81]  Linda Geerligs,et al.  Assessing dynamic functional connectivity in heterogeneous samples , 2017, NeuroImage.

[82]  Scott T Grafton,et al.  Improving resolution of dynamic communities in human brain networks through targeted node removal , 2017, PloS one.

[83]  Cheng Li,et al.  Adjusting batch effects in microarray expression data using empirical Bayes methods. , 2007, Biostatistics.

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

[85]  Danielle S. Bassett,et al.  Positive affect, surprise, and fatigue are correlates of network flexibility , 2017, Scientific Reports.

[86]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[87]  Danielle S Bassett,et al.  Understanding the Emergence of Neuropsychiatric Disorders With Network Neuroscience. , 2018, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[88]  M. Weissman,et al.  Statistical harmonization corrects site effects in functional connectivity measurements from multi‐site fMRI data , 2018, Human brain mapping.

[89]  Qiongling Li,et al.  Dynamic reconfiguration of the functional brain network after musical training in young adults , 2019, Brain Structure and Function.

[90]  Kimberly J. Schlesinger,et al.  Age-dependent changes in task-based modular organization of the human brain , 2017, NeuroImage.

[91]  V. Calhoun,et al.  Changing brain connectivity dynamics: From early childhood to adulthood , 2018, Human brain mapping.

[92]  Danielle S Bassett,et al.  Flexible Coordinator and Switcher Hubs for Adaptive Task Control , 2020, The Journal of Neuroscience.

[93]  Zhao Yang,et al.  A Comparative Analysis of Community Detection Algorithms on Artificial Networks , 2016, Scientific Reports.

[94]  Olaf Sporns,et al.  Functional brain modules reconfigure at multiple scales across the human lifespan , 2015, 1510.08045.

[95]  Gerardo Chowell,et al.  Null Models for Community Detection in Spatially-Embedded, Temporal Networks , 2014, bioRxiv.

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

[97]  Thomas E. Nichols,et al.  Scanning the horizon: towards transparent and reproducible neuroimaging research , 2016, Nature Reviews Neuroscience.

[98]  A. Walden,et al.  Wavelet Methods for Time Series Analysis , 2000 .

[99]  D. Bassett,et al.  Repetitive negative thinking in daily life and functional connectivity among default mode, fronto-parietal, and salience networks , 2019, Translational Psychiatry.

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

[101]  Danielle S Bassett,et al.  Detection of functional brain network reconfiguration during task-driven cognitive states , 2016, NeuroImage.

[102]  Danielle S Bassett,et al.  Dynamic Flexibility in Striatal-Cortical Circuits Supports Reinforcement Learning , 2017, The Journal of Neuroscience.

[103]  Danielle S Bassett,et al.  Disrupted dynamic network reconfiguration of the language system in temporal lobe epilepsy , 2018, Brain : a journal of neurology.

[104]  Michael Breakspear,et al.  Naturalistic Stimuli in Neuroscience: Critically Acclaimed , 2019, Trends in Cognitive Sciences.

[105]  Danielle S. Bassett,et al.  Brain state expression and transitions are related to complex executive cognition in normative neurodevelopment , 2018, NeuroImage.

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

[107]  Tamara Vanderwal,et al.  Inscapes: A movie paradigm to improve compliance in functional magnetic resonance imaging , 2015, NeuroImage.

[108]  Satrajit S. Ghosh,et al.  The Healthy Brain Network Serial Scanning Initiative: a resource for evaluating inter-individual differences and their reliabilities across scan conditions and sessions , 2016, bioRxiv.

[109]  Danielle S. Bassett,et al.  Flexible Coordinator and Switcher Hubs for Adaptive Task Control , 2019, The Journal of Neuroscience.

[110]  B. Lehmanna,et al.  Assessing dynamic functional connectivity in heterogeneous samples , 2017 .

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

[112]  Kun Bi,et al.  Dynamic community structure in major depressive disorder: A resting-state MEG study , 2019, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[113]  Evan M. Gordon,et al.  Functional System and Areal Organization of a Highly Sampled Individual Human Brain , 2015, Neuron.

[114]  Danielle S Bassett,et al.  Multi-scale detection of hierarchical community architecture in structural and functional brain networks , 2017, PloS one.

[115]  Jonathan Young,et al.  Resting state fMRI based multilayer network configuration in patients with schizophrenia , 2020, NeuroImage: Clinical.

[116]  F. Castellanos,et al.  Movies in the magnet: Naturalistic paradigms in developmental functional neuroimaging , 2018, Developmental Cognitive Neuroscience.

[117]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[118]  Jukka-Pekka Onnela,et al.  Community Structure in Time-Dependent, Multiscale, and Multiplex Networks , 2009, Science.

[119]  Thomas E. Nichols,et al.  Best practices in data analysis and sharing in neuroimaging using MRI , 2017, Nature Neuroscience.

[120]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[121]  Li Wang,et al.  Predicting escitalopram monotherapy response in depression: The role of anterior cingulate cortex , 2019, Human brain mapping.

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

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

[124]  Jean-Loup Guillaume,et al.  Local leaders in random networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[125]  Nora D. Volkow,et al.  Temporal Evolution of Brain Functional Connectivity Metrics: Could 7 Min of Rest be Enough? , 2016, Cerebral cortex.

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

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

[128]  Andrew Zalesky,et al.  Multilayer network switching rate predicts brain performance , 2018, Proceedings of the National Academy of Sciences.

[129]  D. Yurgelun-Todd,et al.  Reproducibility of Single-Subject Functional Connectivity Measurements , 2011, American Journal of Neuroradiology.

[130]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[131]  Dimitri Van De Ville,et al.  On spurious and real fluctuations of dynamic functional connectivity during rest , 2015, NeuroImage.

[132]  Russell T. Shinohara,et al.  Harmonization of cortical thickness measurements across scanners and sites , 2017, NeuroImage.

[133]  R. Cameron Craddock,et al.  Individual differences in functional connectivity during naturalistic viewing conditions , 2016, NeuroImage.