Assessment of the effect of data length on the reliability of resting-state fNIRS connectivity measures and graph metrics

Abstract The reliability assessment of connectivity measures and graph metrics is crucial for characterizing topological properties of resting-state brain networks that are intrinsic to the functioning of the brain and not biased by variability across subjects and data lengths. In this study, we investigated the effect of data length on the reliability and stability of four functional connectivity measures, Pearson’s Correlation (PC), percentage-Bend Correlation (BC), Mutual Information (MI) and Partial Correlation (PtC), and twelve graph theoretical metrics derived from resting state functional near-infrared spectroscopy (rsfNIRS) data using data lengths ranging from 0.5 to 4.5 min. We analyzed rsfNIRS data collected in two separate sessions from 13 healthy adult subjects using an optical probe covering the whole brain. Our results showed that PC and BC stabilized with data lengths longer than 1–2.5 min depending on concentration signals. The stabilization for MI occurred with medium to long-range data lengths (more than 2.5 min). PtC showed stability only for data lengths shorter than 2.5 min. The reliability of the majority of the PC, BC and MI-derived network metrics improved significantly by data lengths of at least 1.5 to 2.5 min, depending on functional connectivity (FC) measures and concentration signals. For the PC and BC and MI-based networks, degree, global efficiency, characteristic path length, clustering coefficient and transitivity, graph radius and diameter exhibited high reliability. For these networks, the betweenness, modularity and vulnerability metrics showed moderate to high reliability with increasing data length for oxyhemoglobin (HbO), deoxyhemoglobin (HbR) and/or total-hemoglobin (HbT) signals. The participation coefficient, however, showed no specific pattern of changes or improvement with increasing data length. The hierarchy measure also showed variable reliability trends with increasing data length. The PtC-derived network metrics exhibited moderate to high reliability only with short-range data lengths shorter than 2 min for HbO, HbR and/or HbT. Our results show that data length can significantly affect the results of the FC analysis as well as the topological properties of weighted functional brain networks. This suggests that caution should be taken when comparing results from studies on functional network organization when FC analysis is performed with different data lengths.

[1]  Elham Barzegaran,et al.  Functional connectivity analysis in EEG source space: The choice of method , 2017, PloS one.

[2]  J. Lurito,et al.  Correlations in Low-Frequency BOLD Fluctuations Reflect Cortico-Cortical Connections , 2000, NeuroImage.

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

[4]  Anders M. Dale,et al.  Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy , 2004, NeuroImage.

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

[6]  Ardalan Aarabi,et al.  Characterization and correction of the false-discovery rates in resting state connectivity using functional near-infrared spectroscopy , 2017, Journal of biomedical optics.

[7]  C. Stam,et al.  The effect of epoch length on estimated EEG functional connectivity and brain network organisation , 2016, Journal of neural engineering.

[8]  Fraser,et al.  Independent coordinates for strange attractors from mutual information. , 1986, Physical review. A, General physics.

[9]  John C Gore,et al.  Assessing functional connectivity in the human brain by fMRI. , 2007, Magnetic resonance imaging.

[10]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[11]  Alan C. Evans,et al.  Uncovering Intrinsic Modular Organization of Spontaneous Brain Activity in Humans , 2009, PloS one.

[12]  E. Okada,et al.  Monte Carlo prediction of near-infrared light propagation in realistic adult and neonatal head models. , 2003, Applied optics.

[13]  J. Maldjian,et al.  Effect of resting-state functional MR imaging duration on stability of graph theory metrics of brain network connectivity. , 2011, Radiology.

[14]  Fabrice Wallois,et al.  Effect of confounding variables on hemodynamic response function estimation using averaging and deconvolution analysis: An event-related NIRS study , 2017, NeuroImage.

[15]  L. da F. Costa,et al.  Characterization of complex networks: A survey of measurements , 2005, cond-mat/0505185.

[16]  O. Sporns Networks of the Brain , 2010 .

[17]  R. Mesquita,et al.  Resting state connectivity patterns with near-infrared spectroscopy data of the whole head. , 2016, Biomedical optics express.

[18]  Yoko Hoshi,et al.  Functional near-infrared spectroscopy: current status and future prospects. , 2007, Journal of biomedical optics.

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

[20]  Massimo Marchiori,et al.  Vulnerability and protection of infrastructure networks. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  Jonas Richiardi,et al.  Graph analysis of functional brain networks: practical issues in translational neuroscience , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Han Zhang,et al.  Is resting-state functional connectivity revealed by functional near-infrared spectroscopy test-retest reliable? , 2011, Journal of biomedical optics.

[23]  G. Taga,et al.  Development of Global Cortical Networks in Early Infancy , 2010, The Journal of Neuroscience.

[24]  Rodrigo Quian Quiroga,et al.  Nonlinear multivariate analysis of neurophysiological signals , 2005, Progress in Neurobiology.

[25]  K. Kaski,et al.  Intensity and coherence of motifs in weighted complex networks. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[26]  Guillaume A. Rousselet,et al.  Robust Correlation Analyses: False Positive and Power Validation Using a New Open Source Matlab Toolbox , 2012, Front. Psychology.

[27]  Shinichi Nakagawa,et al.  Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists , 2010, Biological reviews of the Cambridge Philosophical Society.

[28]  Yong He,et al.  Effects of Different Correlation Metrics and Preprocessing Factors on Small-World Brain Functional Networks: A Resting-State Functional MRI Study , 2012, PloS one.

[29]  Fabrice Wallois,et al.  Functional Brain Dysfunction in Patients with Benign Childhood Epilepsy as Revealed by Graph Theory , 2015, PloS one.

[30]  Han Zhang,et al.  Test–retest assessment of independent component analysis-derived resting-state functional connectivity based on functional near-infrared spectroscopy , 2011, NeuroImage.

[31]  Quan Zhang,et al.  Adaptive filtering to reduce global interference in non-invasive NIRS measures of brain activation: How well and when does it work? , 2009, NeuroImage.

[32]  Abraham Z. Snyder,et al.  Resting-state functional connectivity in the human brain revealed with diffuse optical tomography , 2009, NeuroImage.

[33]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[35]  Guillaume A. Rousselet,et al.  Improving standards in brain-behavior correlation analyses , 2012, Front. Hum. Neurosci..

[36]  A. Vespignani,et al.  The architecture of complex weighted networks. , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Yufeng Zang,et al.  Functional connectivity as revealed by independent component analysis of resting-state fNIRS measurements , 2010, NeuroImage.

[38]  Adam J. Schwarz,et al.  Negative edges and soft thresholding in complex network analysis of resting state functional connectivity data , 2011, NeuroImage.

[39]  Assia Jaillard,et al.  Reliability of graph analysis of resting state fMRI using test-retest dataset from the Human Connectome Project , 2016, NeuroImage.

[40]  G. Fagiolo Clustering in complex directed networks. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

[43]  David A. Boas,et al.  Improved recovery of the hemodynamic response in diffuse optical imaging using short optode separations and state-space modeling , 2011, NeuroImage.

[44]  A. Aarabi,et al.  EEG Resting State Functional Connectivity Analysis in Children with Benign Epilepsy with Centrotemporal Spikes , 2016, Front. Neurosci..

[45]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Oliver Grimm,et al.  Test–retest reliability of fMRI-based graph theoretical properties during working memory, emotion processing, and resting state , 2014, NeuroImage.

[47]  Yong He,et al.  Test-Retest Reliability of Graph Metrics in Functional Brain Networks: A Resting-State fNIRS Study , 2013, PloS one.

[48]  Maurizio Corbetta,et al.  Functional connectivity in resting-state fMRI: Is linear correlation sufficient? , 2011, NeuroImage.

[49]  B. Biswal,et al.  Simultaneous assessment of flow and BOLD signals in resting‐state functional connectivity maps , 1997, NMR in biomedicine.

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

[51]  Aram Galstyan,et al.  Efficient Estimation of Mutual Information for Strongly Dependent Variables , 2014, AISTATS.

[52]  Yong He,et al.  Revealing Topological Organization of Human Brain Functional Networks with Resting-State Functional near Infrared Spectroscopy , 2012, PloS one.

[53]  Ardalan Aarabi,et al.  Characterization of the relative contributions from systemic physiological noise to whole-brain resting-state functional near-infrared spectroscopy data using single-channel independent component analysis , 2016, Neurophotonics.

[54]  Antonio Napolitano,et al.  Test-retest reliability of graph metrics of resting state MRI functional brain networks: A review , 2015, Journal of Neuroscience Methods.

[55]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[56]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[57]  Chaozhe Zhu,et al.  Use of fNIRS to assess resting state functional connectivity , 2010, Journal of Neuroscience Methods.

[58]  Ann-Christine Ehlis,et al.  Event-related functional near-infrared spectroscopy (fNIRS): Are the measurements reliable? , 2006, NeuroImage.

[59]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[60]  I. Miyai,et al.  Removal of the skin blood flow artifact in functional near-infrared spectroscopic imaging data through independent component analysis. , 2007, Journal of biomedical optics.

[61]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[62]  J. D. Kruschwitz,et al.  GraphVar: A user-friendly toolbox for comprehensive graph analyses of functional brain connectivity , 2015, Journal of Neuroscience Methods.

[63]  Dustin Scheinost,et al.  The (in)stability of functional brain network measures across thresholds , 2015, NeuroImage.

[64]  T. Schreiber,et al.  Surrogate time series , 1999, chao-dyn/9909037.

[65]  Scott T. Grafton,et al.  Structural foundations of resting-state and task-based functional connectivity in the human brain , 2013, Proceedings of the National Academy of Sciences.

[66]  D. Boas,et al.  HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. , 2009, Applied optics.

[67]  Paul J. Laurienti,et al.  Neuroinformatics Original Research Article Materials and Methods Study Participants , 2022 .

[68]  Hanli Liu,et al.  Dynamic functional connectivity revealed by resting-state functional near-infrared spectroscopy. , 2015, Biomedical optics express.

[69]  K. McGraw,et al.  Forming inferences about some intraclass correlation coefficients. , 1996 .

[70]  D. Delpy,et al.  Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. , 1995, Physics in medicine and biology.

[71]  Mahdi Jalili,et al.  Constructing brain functional networks from EEG: partial and unpartial correlations. , 2011, Journal of integrative neuroscience.

[72]  David A Boas,et al.  Eigenvector-based spatial filtering for reduction of physiological interference in diffuse optical imaging. , 2005, Journal of biomedical optics.

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

[74]  Ashish Raj,et al.  Statistics of Weighted Brain Networks Reveal Hierarchical Organization and Gaussian Degree Distribution , 2012, PloS one.

[75]  Paul J. Laurienti,et al.  A New Measure of Centrality for Brain Networks , 2010, PloS one.

[76]  Edward T. Bullmore,et al.  Reproducibility of graph metrics of human brain functional networks , 2009, NeuroImage.

[77]  Theo Gasser,et al.  Assessing intrarater, interrater and test–retest reliability of continuous measurements , 2002, Statistics in medicine.

[78]  D. Boas,et al.  Resting state functional connectivity of the whole head with near-infrared spectroscopy , 2010, Biomedical optics express.

[79]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

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

[81]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[82]  Mark H. Johnson,et al.  Test–retest reliability of functional near infrared spectroscopy in infants , 2014, Neurophotonics.

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

[84]  A. Kleinschmidt,et al.  Simultaneous Recording of Cerebral Blood Oxygenation Changes during Human Brain Activation by Magnetic Resonance Imaging and Near-Infrared Spectroscopy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[85]  E. Gratton,et al.  Near-infrared study of fluctuations in cerebral hemodynamics during rest and motor stimulation: temporal analysis and spatial mapping. , 2000, Medical physics.

[86]  Andreas Heinz,et al.  Test–retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures , 2012, NeuroImage.

[87]  Michael B. Miller,et al.  How reliable are the results from functional magnetic resonance imaging? , 2010, Annals of the New York Academy of Sciences.

[88]  Guang-Zhong Yang,et al.  Assessment of the cerebral cortex during motor task behaviours in adults: A systematic review of functional near infrared spectroscopy (fNIRS) studies , 2011, NeuroImage.

[89]  Klaus Hahn,et al.  A new method to measure complexity in binary or weighted networks and applications to functional connectivity in the human brain , 2016, BMC Bioinformatics.

[90]  Bharat B. Biswal,et al.  Effect of Resting-State fNIRS Scanning Duration on Functional Brain Connectivity and Graph Theory Metrics of Brain Network , 2017, Front. Neurosci..

[91]  Yong He,et al.  Graph Theoretical Analysis of Functional Brain Networks: Test-Retest Evaluation on Short- and Long-Term Resting-State Functional MRI Data , 2011, PloS one.

[92]  B. Slack,et al.  The Geography of Transport Systems , 2006 .

[93]  M. Rosenblatt Remarks on Some Nonparametric Estimates of a Density Function , 1956 .

[94]  R. Wilcox The percentage bend correlation coefficient , 1994 .