Reproducibility and Robustness of Graph Measures of the Associative-Semantic Network

Graph analysis is a promising tool to quantify brain connectivity. However, an essential requirement is that the graph measures are reproducible and robust. We have studied the reproducibility and robustness of various graph measures in group based and in individual binary and weighted networks derived from a task fMRI experiment during explicit associative-semantic processing of words and pictures. The nodes of the network were defined using an independent study and the connectivity was based on the partial correlation of the time series between any pair of nodes. The results showed that in case of binary networks, global graph measures exhibit a good reproducibility and robustness for networks which are not too sparse and these figures of merit depend on the graph measure and on the density of the network. Furthermore, group based binary networks should be derived from groups of sufficient size and the lower the density the more subjects are required to obtain robust values. Local graph measures are very variable in terms of reproducibility and should be interpreted with care. For weighted networks, we found good reproducibility (average test-retest variability <5% and ICC values >0.4) when using subject specific networks and this will allow us to relate network properties to individual subject information.

[1]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[2]  Mark E. Bastin,et al.  Test–retest reliability of structural brain networks from diffusion MRI , 2014, NeuroImage.

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

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

[5]  W. Schneider,et al.  Selective Retrieval of Abstract Semantic Knowledge in Left Prefrontal Cortex , 2007, The Journal of Neuroscience.

[6]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[7]  Michael I. Miller,et al.  Atlas-based analysis of resting-state functional connectivity: Evaluation for reproducibility and multi-modal anatomy–function correlation studies , 2012, NeuroImage.

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

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

[10]  Jason R. Tregellas,et al.  Nicotine increases brain functional network efficiency , 2012, NeuroImage.

[11]  Claudio Altafini,et al.  Comparing association network algorithms for reverse engineering of large-scale gene regulatory networks: synthetic versus real data , 2007, Bioinform..

[12]  Patrick Dupont,et al.  Right Hemisphere Recruitment During Language Processing in Frontotemporal Lobar Degeneration and Alzheimer’s Disease , 2011, Journal of Molecular Neuroscience.

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

[14]  Paul J. Laurienti,et al.  Consistency of Network Modules in Resting-State fMRI Connectome Data , 2012, PloS one.

[15]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[16]  R. Kahn,et al.  Aberrant Frontal and Temporal Complex Network Structure in Schizophrenia: A Graph Theoretical Analysis , 2010, The Journal of Neuroscience.

[17]  Yong He,et al.  Age-related changes in topological patterns of large-scale brain functional networks during memory encoding and recognition , 2010, NeuroImage.

[18]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[19]  E. Bullmore,et al.  Reconciling abnormalities of brain network structure and function in schizophrenia , 2015, Current Opinion in Neurobiology.

[20]  Jie Tian,et al.  The trade-off between wiring cost and network topology in white matter structural networks in health and migraine , 2013, Experimental Neurology.

[21]  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.

[22]  B. Avants,et al.  Reproducibility of functional network metrics and network structure: A comparison of task-related BOLD, resting ASL with BOLD contrast, and resting cerebral blood flow , 2013, Cognitive, affective & behavioral neuroscience.

[23]  Jacobus F. A. Jansen,et al.  The effect and reproducibility of different clinical DTI gradient sets on small world brain connectivity measures , 2010, NeuroImage.

[24]  Patrick Dupont,et al.  Motor learning-induced changes in functional brain connectivity as revealed by means of graph-theoretical network analysis , 2012, NeuroImage.

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

[26]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[27]  Timothy P. L. Roberts,et al.  Test-Retest Reliability of Computational Network Measurements Derived from the Structural Connectome of the Human Brain , 2013, Brain Connect..

[28]  Marcus Kaiser,et al.  Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems , 2006, PLoS Comput. Biol..

[29]  P. Dupont,et al.  Abeta amyloid deposition in the language system and how the brain responds. , 2007, Brain : a journal of neurology.

[30]  Vince D. Calhoun,et al.  Modulations of functional connectivity in the healthy and schizophrenia groups during task and rest , 2012, NeuroImage.

[31]  D. Willshaw,et al.  Cerebral Cortex doi:10.1093/cercor/bhr221 Cerebral Cortex Advance Access published September 21, 2011 Similarity-Based Extraction of Individual Networks from Gray Matter MRI Scans , 2022 .

[32]  Yong He,et al.  Resting-State Functional Brain Connectivity : Lessons from Functional Near-Infrared Spectroscopy , 2022 .

[33]  Patrick Dupont,et al.  The associative-semantic network for words and pictures: Effective connectivity and graph analysis , 2013, Brain and Language.

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

[35]  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.

[36]  Zhong Xue,et al.  Network‐based analysis reveals stronger local diffusion‐based connectivity and different correlations with oral language skills in brains of children with high functioning autism spectrum disorders , 2014, Human brain mapping.

[37]  Brian A. Nosek,et al.  Power failure: why small sample size undermines the reliability of neuroscience , 2013, Nature Reviews Neuroscience.

[38]  Alan C. Evans,et al.  Structural Insights into Aberrant Topological Patterns of Large-Scale Cortical Networks in Alzheimer's Disease , 2008, The Journal of Neuroscience.

[39]  E. Reiman,et al.  Polymorphism of brain derived neurotrophic factor influences β amyloid load in cognitively intact apolipoprotein E ε4 carriers , 2013, NeuroImage: Clinical.

[40]  J. Finn A General Model for Multivariate Analysis , 1978 .

[41]  Danielle S. Bassett,et al.  Conserved and variable architecture of human white matter connectivity , 2011, NeuroImage.

[42]  Wei Liao,et al.  Mapping the Voxel-Wise Effective Connectome in Resting State fMRI , 2013, PloS one.

[43]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

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

[45]  J. B. Demb,et al.  Semantic Repetition Priming for Verbal and Pictorial Knowledge: A Functional MRI Study of Left Inferior Prefrontal Cortex , 1997, Journal of Cognitive Neuroscience.

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

[47]  Fumiko Hoeft,et al.  Topological properties of large-scale structural brain networks in children with familial risk for reading difficulties , 2013, NeuroImage.

[48]  Yong He,et al.  Disrupted Functional Brain Connectome in Individuals at Risk for Alzheimer's Disease , 2013, Biological Psychiatry.

[49]  M. L. Lambon Ralph,et al.  The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus , 2010, Cerebral cortex.

[50]  C. Stam,et al.  Small-world networks and disturbed functional connectivity in schizophrenia , 2006, Schizophrenia Research.

[51]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[52]  Jonathan D. Power,et al.  Parcellation in left lateral parietal cortex is similar in adults and children. , 2012, Cerebral cortex.

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

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

[55]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[56]  Sayan Mukherjee,et al.  A comparative study of covariance selection models for the inference of gene regulatory networks , 2013, J. Biomed. Informatics.

[57]  Paul J. Laurienti,et al.  Assessing the consistency of community structure in complex networks , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

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

[60]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[61]  Paul J. Laurienti,et al.  An exploration of graph metric reproducibility in complex brain networks , 2013, Front. Neurosci..

[62]  Andreas Daffertshofer,et al.  Comparing Brain Networks of Different Size and Connectivity Density Using Graph Theory , 2010, PloS one.

[63]  Lin Shi,et al.  Abnormal Organization of White Matter Network in Patients with No Dementia after Ischemic Stroke , 2013, PloS one.

[64]  Edward T. Bullmore,et al.  On the use of correlation as a measure of network connectivity , 2012, NeuroImage.

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

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

[67]  Cathy J. Price,et al.  Explaining Left Lateralization for Words in the Ventral Occipitotemporal Cortex , 2011, The Journal of Neuroscience.

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

[69]  Xiaoping Hu,et al.  Quantitative assessment of a framework for creating anatomical brain networks via global tractography , 2012, NeuroImage.

[70]  P. Dupont,et al.  Word reading and posterior temporal dysfunction in amnestic mild cognitive impairment. , 2006, Cerebral cortex.

[71]  Patrick Dupont,et al.  The amodal system for conscious word and picture identification in the absence of a semantic task , 2010, NeuroImage.