Test–retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures

Characterizing the brain connectome using neuroimaging data and measures derived from graph theory emerged as a new approach that has been applied to brain maturation, cognitive function and neuropsychiatric disorders. For a broad application of this method especially for clinical populations and longitudinal studies, the reliability of this approach and its robustness to confounding factors need to be explored. Here we investigated test-retest reliability of graph metrics of functional networks derived from functional magnetic resonance imaging (fMRI) recorded in 33 healthy subjects during rest. We constructed undirected networks based on the Anatomic-Automatic-Labeling (AAL) atlas template and calculated several commonly used measures from the field of graph theory, focusing on the influence of different strategies for confound correction. For each subject, method and session we computed the following graph metrics: clustering coefficient, characteristic path length, local and global efficiency, assortativity, modularity, hierarchy and the small-worldness scalar. Reliability of each graph metric was assessed using the intraclass correlation coefficient (ICC). Overall ICCs ranged from low to high (0 to 0.763) depending on the method and metric. Methodologically, the use of a broader frequency band (0.008-0.15 Hz) yielded highest reliability indices (mean ICC=0.484), followed by the use of global regression (mean ICC=0.399). In general, the second order metrics (small-worldness, hierarchy, assortativity) studied here, tended to be more robust than first order metrics. In conclusion, our study provides methodological recommendations which allow the computation of sufficiently robust markers of network organization using graph metrics derived from fMRI data at rest.

[1]  Daniel L. Rubin,et al.  Network Analysis of Intrinsic Functional Brain Connectivity in Alzheimer's Disease , 2008, PLoS Comput. Biol..

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

[3]  C. Stam,et al.  Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis , 2006, Neuroscience Letters.

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

[5]  S. Rombouts,et al.  Hierarchical functional modularity in the resting‐state human brain , 2009, Human brain mapping.

[6]  Randy L. Gollub,et al.  Test–retest study of fMRI signal change evoked by electroacupuncture stimulation , 2007, NeuroImage.

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

[8]  R. Müller,et al.  A critical discussion of intraclass correlation coefficients. , 1994, Statistics in medicine.

[9]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

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

[11]  Dimitri Van De Ville,et al.  Impact of transient emotions on functional connectivity during subsequent resting state: A wavelet correlation approach , 2011, NeuroImage.

[12]  E. Bullmore,et al.  Hierarchical Organization of Human Cortical Networks in Health and Schizophrenia , 2008, The Journal of Neuroscience.

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

[14]  C. Stam,et al.  The influence of ageing on complex brain networks: A graph theoretical analysis , 2009, Human brain mapping.

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

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

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

[18]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[19]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[20]  Judith K Sluiter,et al.  Test-retest reliability of heart rate variability and respiration rate at rest and during light physical activity in normal subjects. , 2007, Archives of medical research.

[21]  S. Cichon,et al.  Neural Mechanisms of a Genome-Wide Supported Psychosis Variant , 2009, Science.

[22]  Peter Kirsch,et al.  Brain function in carriers of a genome-wide supported bipolar disorder variant. , 2010, Archives of general psychiatry.

[23]  Eugenio Rodriguez,et al.  Neural synchrony and the development of cortical networks , 2010, Trends in Cognitive Sciences.

[24]  E. Bullmore,et al.  Neurophysiological architecture of functional magnetic resonance images of human brain. , 2005, Cerebral cortex.

[25]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

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

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

[28]  Matthijs Vink,et al.  Cardiorespiratory effects on default‐mode network activity as measured with fMRI , 2009, Human brain mapping.

[29]  Edward T. Bullmore,et al.  Disrupted Modularity and Local Connectivity of Brain Functional Networks in Childhood-Onset Schizophrenia , 2010, Front. Syst. Neurosci..

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

[31]  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.

[32]  Lourens J. Waldorp,et al.  Effective connectivity of fMRI data using ancestral graph theory: Dealing with missing regions , 2011, NeuroImage.

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

[34]  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.

[35]  Paul J. Laurienti,et al.  Reproducibility of Graph Metrics in fMRI Networks , 2010, Front. Neuroinform..

[36]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[37]  J. Fleiss The design and analysis of clinical experiments , 1987 .

[38]  Yong He,et al.  Hemisphere- and gender-related differences in small-world brain networks: A resting-state functional MRI study , 2011, NeuroImage.

[39]  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.

[40]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

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

[42]  Walter Paulus,et al.  Introducing graph theory to track for neuroplastic alterations in the resting human brain: A transcranial direct current stimulation study , 2011, NeuroImage.

[43]  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.

[44]  Yong He,et al.  Disrupted small-world networks in schizophrenia. , 2008, Brain : a journal of neurology.

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

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

[47]  Alan C. Evans,et al.  Age- and Gender-Related Differences in the Cortical Anatomical Network , 2009, The Journal of Neuroscience.

[48]  D. Cicchetti,et al.  Developing criteria for establishing interrater reliability of specific items: applications to assessment of adaptive behavior. , 1981, American journal of mental deficiency.

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

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

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

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

[53]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[54]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[55]  D. Cicchetti Methodological Commentary The Precision of Reliability and Validity Estimates Re-Visited: Distinguishing Between Clinical and Statistical Significance of Sample Size Requirements , 2001 .

[56]  Edward T. Bullmore,et al.  Network Scaling Effects in Graph Analytic Studies of Human Resting-State fMRI Data , 2010, Front. Syst. Neurosci..

[57]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[58]  Albert-László Barabási,et al.  Hierarchical organization in complex networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[59]  Paul J. Laurienti,et al.  Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data , 2010, NeuroImage.

[60]  C. Stam,et al.  Small‐world properties of nonlinear brain activity in schizophrenia , 2009, Human brain mapping.

[61]  M E J Newman Assortative mixing in networks. , 2002, Physical review letters.

[62]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.