Modular slowing of resting-state dynamic functional connectivity as a marker of cognitive dysfunction induced by sleep deprivation

Dynamic Functional Connectivity (dFC) in the resting state (rs) is considered as a correlate of cognitive processing. Describing dFC as a flow across morphing connectivity configurations, our notion of dFC speed quantifies the rate at which FC networks evolve in time. Here we probe the hypothesis that variations of rs dFC speed and cognitive performance are selectively interrelated within specific functional subnetworks. In particular, we focus on Sleep Deprivation (SD) as a reversible model of cognitive dysfunction. We found that whole-brain level (global) dFC speed significantly slows down after 24h of SD. However, the reduction in global dFC speed does not correlate with variations of cognitive performance in individual tasks, which are subtle and highly heterogeneous. On the contrary, we found strong correlations between performance variations in individual tasks -including Rapid Visual Processing (RVP, assessing sustained visual attention)- and dFC speed quantified at the level of functional sub-networks of interest. Providing a compromise between classic static FC (no time) and global dFC (no space), modular dFC speed analyses allow quantifying a different speed of dFC reconfiguration independently for sub-networks overseeing different tasks. Importantly, we found that RVP performance robustly correlates with the modular dFC speed of a characteristic frontoparietal module.

[1]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[2]  G. Tononi,et al.  BOLD signatures of sleep , 2019, bioRxiv.

[3]  J. Matias Palva,et al.  Infra-slow fluctuations in electrophysiological recordings, blood-oxygenation-level-dependent signals, and psychophysical time series , 2012, NeuroImage.

[4]  Dimitri Van De Ville,et al.  The dynamic functional connectome: State-of-the-art and perspectives , 2017, NeuroImage.

[5]  Sam R. Miller,et al.  Effects of donepezil on cognitive performance after sleep deprivation , 2011, Human psychopharmacology.

[6]  M. Walker,et al.  The human emotional brain without sleep — a prefrontal amygdala disconnect , 2007, Current Biology.

[7]  G. Vandewalle,et al.  Local modulation of human brain responses by circadian rhythmicity and sleep debt , 2016, Science.

[8]  C. Frith,et al.  A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory , 1996, Neuropsychologia.

[9]  Peter A. Bandettini,et al.  Task-based dynamic functional connectivity: Recent findings and open questions , 2017, NeuroImage.

[10]  Chenhao Wang,et al.  Dynamic functional connectivity and its behavioral correlates beyond vigilance , 2018, NeuroImage.

[11]  Enzo Tagliazucchi,et al.  Dynamic functional connectivity and brain metastability during altered states of consciousness , 2017, NeuroImage.

[12]  Jeffrey Cummings,et al.  Advances in designs for Alzheimer's disease clinical trials. , 2012, American journal of neurodegenerative disease.

[13]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

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

[15]  P. Rossini,et al.  Brain Networks are Independently Modulated by Donepezil, Sleep, and Sleep Deprivation , 2017, Brain Topography.

[16]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[18]  Joaquín Goñi,et al.  Mapping the functional connectome traits of levels of consciousness , 2016, NeuroImage.

[19]  Geoffrey E. Hinton,et al.  Visualizing Data using t-SNE , 2008 .

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

[21]  D. Dinges,et al.  Neurocognitive Consequences of Sleep Deprivation , 2005, Seminars in neurology.

[22]  Thomas Boudou,et al.  Dynamic Functional Connectivity between order and randomness and its evolution across the human adult lifespan , 2020, NeuroImage.

[23]  Danielle S. Bassett,et al.  From Maps to Multi-dimensional Network Mechanisms of Mental Disorders , 2018, Neuron.

[24]  Michael J. Hove,et al.  Dynamic Brain Network Correlates of Spontaneous Fluctuations in Attention , 2016, Cerebral cortex.

[25]  A. Pack,et al.  Heritability of performance deficit accumulation during acute sleep deprivation in twins. , 2012, Sleep.

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

[27]  Julian Lim,et al.  Dynamic functional connectivity markers of objective trait mindfulness , 2018, NeuroImage.

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

[29]  David Bartrés-Faz,et al.  Structural and Functional Imaging Correlates of Cognitive and Brain Reserve Hypotheses in Healthy and Pathological Aging , 2011, Brain Topography.

[30]  Xiaoping Hu,et al.  Behavioral Relevance of the Dynamics of the Functional Brain Connectome , 2014, Brain Connect..

[31]  Andrea Brovelli,et al.  Dynamic Reconfiguration of Visuomotor-Related Functional Connectivity Networks , 2017, The Journal of Neuroscience.

[32]  Viktor K. Jirsa,et al.  Symmetry Breaking in Space-Time Hierarchies Shapes Brain Dynamics and Behavior , 2017, Neuron.

[33]  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.

[34]  Gustavo Deco,et al.  Functional connectivity dynamics: Modeling the switching behavior of the resting state , 2015, NeuroImage.

[35]  V. Calhoun,et al.  The Chronnectome: Time-Varying Connectivity Networks as the Next Frontier in fMRI Data Discovery , 2014, Neuron.

[36]  A. Kirova,et al.  Working Memory and Executive Function Decline across Normal Aging, Mild Cognitive Impairment, and Alzheimer's Disease , 2015, BioMed research international.

[37]  R. Passingham The frontal lobes and voluntary action , 1993 .

[38]  Sean L. Hill,et al.  The Sleep Slow Oscillation as a Traveling Wave , 2004, The Journal of Neuroscience.

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

[40]  Mark W. Woolrich,et al.  Spectrally resolved fast transient brain states in electrophysiological data , 2016, NeuroImage.

[41]  Stuart M Fogel,et al.  Functional connectivity dynamics slow with descent from wakefulness to sleep , 2019, PloS one.

[42]  Akhilesh Pandey,et al.  Homer1a drives homeostatic scaling-down of excitatory synapses during sleep , 2017, Science.

[43]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[44]  S. Havlin,et al.  Detecting long-range correlations with detrended fluctuation analysis , 2001, cond-mat/0102214.

[45]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[46]  Marc Timme,et al.  Dynamic information routing in complex networks , 2015, Nature Communications.

[47]  Chin-Hui Lee,et al.  Evaluation of sliding window correlation performance for characterizing dynamic functional connectivity and brain states , 2016, NeuroImage.

[48]  B. T. Thomas Yeo,et al.  Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation , 2015, NeuroImage.

[49]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[50]  John D E Gabrieli,et al.  Resting in peace or noise: Scanner background noise suppresses default‐mode network , 2008, Human brain mapping.

[51]  Leonardo L. Gollo,et al.  Time-resolved resting-state brain networks , 2014, Proceedings of the National Academy of Sciences.

[52]  J. Kelso,et al.  Coordination Dynamics in Cognitive Neuroscience , 2016, Front. Neurosci..

[53]  Andreas Daffertshofer,et al.  Dynamic Functional Connectivity between order and randomness and its evolution across the human adult lifespan , 2020, NeuroImage.

[54]  E. Stein,et al.  Multiple Neuronal Networks Mediate Sustained Attention , 2003, Journal of Cognitive Neuroscience.

[55]  B. T. Thomas Yeo,et al.  Interpreting temporal fluctuations in resting-state functional connectivity MRI , 2017, NeuroImage.

[56]  J. Fuster Network memory , 1997, Trends in Neurosciences.

[57]  R. Petersen,et al.  Aging, mild cognitive impairment, and Alzheimer's disease. , 2000, Neurologic clinics.

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

[59]  J. Cummings,et al.  The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment , 2005, Journal of the American Geriatrics Society.

[60]  S. Doran,et al.  Sustained attention performance during sleep deprivation: evidence of state instability. , 2001, Archives italiennes de biologie.

[61]  Xiping Liu,et al.  Dynamic Repertoire of Intrinsic Brain States Is Reduced in Propofol-Induced Unconsciousness , 2015, Brain Connect..

[62]  Lars T. Westlye,et al.  The brain functional connectome is robustly altered by lack of sleep , 2016, NeuroImage.

[63]  Lisa Y. M. Chuah,et al.  Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition , 2008, Current opinion in neurology.

[64]  I. Heuser,et al.  Acetylcholinesterase inhibitors and memantine for neuroenhancement in healthy individuals: a systematic review. , 2010, Pharmacological research.

[65]  Michael Breakspear,et al.  Towards a statistical test for functional connectivity dynamics , 2015, NeuroImage.

[66]  Stephen M Smith,et al.  Fast transient networks in spontaneous human brain activity , 2014, eLife.

[67]  J. Morton,et al.  Tracking the Brain's Functional Coupling Dynamics over Development , 2015, The Journal of Neuroscience.

[68]  M. Walker,et al.  The sleep-deprived human brain , 2017, Nature Reviews Neuroscience.

[69]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[70]  Peter Fransson,et al.  Bursty properties revealed in large-scale brain networks with a point-based method for dynamic functional connectivity , 2016, Scientific Reports.

[71]  Yaakov Stern,et al.  Cognitive Reserve: Implications for Assessment and Intervention , 2013, Folia Phoniatrica et Logopaedica.

[72]  Danielle S Bassett,et al.  Cross-linked structure of network evolution. , 2013, Chaos.

[73]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[74]  Jari Saramäki,et al.  Temporal Networks , 2011, Encyclopedia of Social Network Analysis and Mining.

[75]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

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

[77]  S. File,et al.  Cognitive effects of modafinil in student volunteers may depend on IQ , 2005, Pharmacology Biochemistry and Behavior.

[78]  Tor D. Wager,et al.  The neuroscience of placebo effects: connecting context, learning and health , 2015, Nature Reviews Neuroscience.

[79]  Jessica R. Cohen The behavioral and cognitive relevance of time-varying, dynamic changes in functional connectivity , 2017, NeuroImage.

[80]  Yaakov Stern,et al.  An approach to studying the neural correlates of reserve , 2017, Brain Imaging and Behavior.

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

[82]  Juan Zhou,et al.  Spontaneous eyelid closures link vigilance fluctuation with fMRI dynamic connectivity states , 2016, Proceedings of the National Academy of Sciences.

[83]  P MALABIA,et al.  [Dynamic brain]. , 1956, Medicina espanola.

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

[85]  Gustavo Deco,et al.  Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI? , 2016, NeuroImage.

[86]  Olaf Sporns,et al.  Edge-centric functional network representations of human cerebral cortex reveal overlapping system-level architecture , 2019, Nature Neuroscience.

[87]  Vince D. Calhoun,et al.  Mutually temporally independent connectivity patterns: A new framework to study the dynamics of brain connectivity at rest with application to explain group difference based on gender , 2015, NeuroImage.

[88]  Fernando Maestú,et al.  Functional brain networks reveal the existence of cognitive reserve and the interplay between network topology and dynamics , 2017, Scientific Reports.

[89]  O. Blin,et al.  An Alzheimer Disease Challenge Model: 24-Hour Sleep Deprivation in Healthy Volunteers, Impact on Working Memory, and Reversal Effect of Pharmacological Intervention , 2020, Journal of clinical psychopharmacology.

[90]  P. Schlattmann,et al.  Modafinil and methylphenidate for neuroenhancement in healthy individuals: A systematic review. , 2010, Pharmacological research.

[91]  C. Moorehead All rights reserved , 1997 .