Persistent homology‐based functional connectivity and its association with cognitive ability: Life‐span study

Brain-segregation attributes in resting-state functional networks have been widely investigated to understand cognition and cognitive aging using various approaches [e.g., average connectivity within/between networks and brain system segregation (BSS)]. While these approaches have assumed that resting-state functional networks operate in a modular structure, a complementary perspective assumes that a core-periphery or rich club structure accounts for brain functions where the hubs are tightly interconnected to each other to allow for integrated processing. In this article, we apply a novel method, persistent homology (PH), to develop an alternative to standard functional connectivity by quantifying the pattern of information during the integrated processing. We also investigate whether PH-based functional connectivity explains cognitive performance and compare the amount of variability in explaining cognitive performance for three sets of independent variables: (1) PH-based functional connectivity, (2) graph theory-based measures, and (3) BSS. Resting-state functional connectivity data were extracted from 279 healthy participants, and cognitive ability scores were generated in four domains (fluid reasoning, episodic memory, vocabulary, and processing speed). The results first highlight the pattern of brain-information flow over whole brain regions (i.e., integrated processing) accounts for more variance of cognitive abilities than other methods. The results also show that fluid reasoning and vocabulary performance significantly decrease as the strength of the additional information flow on functional connectivity with the shortest path increases. While PH has been applied to functional connectivity analysis in recent studies, our results demonstrate potential utility of PH-based functional connectivity in understanding cognitive function.

[1]  N. Dosenbach,et al.  Precision dynamical mapping using topological data analysis reveals a hub-like transition state at rest , 2022, Nature Communications.

[2]  A. Hillebrand,et al.  Minimum spanning tree analysis of brain networks: A systematic review of network size effects, sensitivity for neuropsychiatric pathology, and disorder specificity , 2022, Network Neuroscience.

[3]  Y. Stern,et al.  The role of neural flexibility in cognitive aging , 2021, NeuroImage.

[4]  Shengxiang Xia,et al.  Analysis of Brain Functional Connectivity Neural Circuits in Children With Autism Based on Persistent Homology , 2021, Frontiers in Human Neuroscience.

[5]  Y. Stern,et al.  A framework for identification of a resting-bold connectome associated with cognitive reserve , 2021, NeuroImage.

[6]  Frédéric Chazal,et al.  An Introduction to Topological Data Analysis: Fundamental and Practical Aspects for Data Scientists , 2017, Frontiers in Artificial Intelligence.

[7]  G. Alexander,et al.  The Role of Resting-State Network Functional Connectivity in Cognitive Aging , 2020, Frontiers in Aging Neuroscience.

[8]  Jie Xiang,et al.  EEG Functional Connectivity Underlying Emotional Valance and Arousal Using Minimum Spanning Trees , 2020, Frontiers in Neuroscience.

[9]  Y. Stern,et al.  The Effect of Aging on Resting State Connectivity of Predefined Networks in the Brain , 2019, Front. Aging Neurosci..

[10]  I. Voineagu,et al.  Persistent homology analysis of brain transcriptome data in autism , 2019, Journal of the Royal Society Interface.

[11]  Danielle S. Bassett,et al.  Unifying the Notions of Modularity and Core–Periphery Structure in Functional Brain Networks during Youth , 2019, Cerebral cortex.

[12]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[13]  Roberto Gasparotti,et al.  Brain Connectivity and Information-Flow Breakdown Revealed by a Minimum Spanning Tree-Based Analysis of MRI Data in Behavioral Variant Frontotemporal Dementia , 2019, Front. Neurosci..

[14]  Yalin Wang,et al.  A concise and persistent feature to study brain resting‐state network dynamics: Findings from the Alzheimer's Disease Neuroimaging Initiative , 2018, Human brain mapping.

[15]  Mariette Yvinec,et al.  Geometric and Topological Inference , 2018 .

[16]  Qolamreza R. Razlighi,et al.  A task-invariant cognitive reserve network , 2018, NeuroImage.

[17]  O. Sporns,et al.  Towards a new approach to reveal dynamical organization of the brain using topological data analysis , 2018, Nature Communications.

[18]  Andrew Zalesky,et al.  Minimum spanning tree analysis of the human connectome , 2018, Human brain mapping.

[19]  J. Kim,et al.  Disrupted Resting State Network of Fibromyalgia in Theta frequency , 2018, Scientific Reports.

[20]  Angelo Bifone,et al.  Graph Analysis and Modularity of Brain Functional Connectivity Networks: Searching for the Optimal Threshold , 2017, Front. Neurosci..

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

[22]  Danielle S. Bassett,et al.  Classification of weighted networks through mesoscale homological features , 2015, J. Complex Networks.

[23]  Arjan Hillebrand,et al.  Different functional connectivity and network topology in behavioral variant of frontotemporal dementia and Alzheimer's disease: an EEG study , 2016, Neurobiology of Aging.

[24]  Krzysztof J. Gorgolewski,et al.  The Dynamics of Functional Brain Networks: Integrated Network States during Cognitive Task Performance , 2015, Neuron.

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

[26]  T. Salthouse,et al.  Breadth and age-dependency of relations between cortical thickness and cognition , 2015, Neurobiology of Aging.

[27]  Danielle S. Bassett,et al.  Cognitive Network Neuroscience , 2015, Journal of Cognitive Neuroscience.

[28]  Qolamreza R. Razlighi,et al.  The Reference Ability Neural Network Study: Motivation, design, and initial feasibility analyses , 2014, NeuroImage.

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

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

[31]  C J Stam,et al.  The trees and the forest: Characterization of complex brain networks with minimum spanning trees. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[32]  Cornelis J. Stam,et al.  Functional brain network analysis using minimum spanning trees in Multiple Sclerosis: An MEG source-space study , 2014, NeuroImage.

[33]  Y. Stern,et al.  Unilateral disruptions in the default network with aging in native space , 2013, Brain and behavior.

[34]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[35]  Joshua Carp,et al.  Optimizing the order of operations for movement scrubbing: Comment on Power et al. , 2013, NeuroImage.

[36]  Olaf Sporns,et al.  Network attributes for segregation and integration in the human brain , 2013, Current Opinion in Neurobiology.

[37]  Cornelis J. Stam,et al.  Growing Trees in Child Brains: Graph Theoretical Analysis of Electroencephalography-Derived Minimum Spanning Tree in 5- and 7-Year-Old Children Reflects Brain Maturation , 2013, Brain Connect..

[38]  O. Sporns,et al.  High-cost, high-capacity backbone for global brain communication , 2012, Proceedings of the National Academy of Sciences.

[39]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

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

[41]  H. Buschke,et al.  Evaluating storage, retention and retrieval in disordered memory and learning , 2011, Neurology.

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

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

[44]  John Skvoretz,et al.  Node centrality in weighted networks: Generalizing degree and shortest paths , 2010, Soc. Networks.

[45]  Y. Stern,et al.  Cognitive reserve , 2009, Neuropsychologia.

[46]  Marián Boguñá,et al.  Extracting the multiscale backbone of complex weighted networks , 2009, Proceedings of the National Academy of Sciences.

[47]  R. Ghrist Barcodes: The persistent topology of data , 2007 .

[48]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[49]  Afra Zomorodian,et al.  Computing Persistent Homology , 2004, SCG '04.

[50]  M. Sliwinski,et al.  Development and validation of a model for estimating premorbid verbal intelligence in the elderly. , 1991, Journal of clinical and experimental neuropsychology.