Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture

Functional coupling across distributed brain regions varies across task contexts, yet there are stable features. To better understand the range and central tendencies of network configurations, coupling patterns were explored using functional MRI (fMRI) across 14 distinct continuously performed task states ranging from passive fixation to increasingly demanding classification tasks. Mean global correlation profiles across the cortex ranged from 0.69 to 0.82 between task states. Network configurations from both passive fixation and classification tasks similarly predicted task coactivation patterns estimated from meta-analysis of the literature. Thus, even across markedly different task states, central tendencies dominate the coupling configurations. Beyond these shared components, distinct task states displayed significant differences in coupling patterns in response to their varied demands. One possibility is that anatomical connectivity provides constraints that act as attractors pulling network configurations towards a limited number of robust states. Reconfigurable coupling modes emerge as significant modifications to a core functional architecture.

[1]  H. Nusbaum,et al.  Task-dependent organization of brain regions active during rest , 2009, Proceedings of the National Academy of Sciences.

[2]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[3]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[4]  A. Zalesky,et al.  Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection , 2012, Proceedings of the National Academy of Sciences.

[5]  Lila Davachi,et al.  Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory , 2013, Proceedings of the National Academy of Sciences.

[6]  B T Thomas Yeo,et al.  Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. , 2014, JAMA psychiatry.

[7]  R. Henson,et al.  Awake reactivation predicts memory in humans , 2013, Proceedings of the National Academy of Sciences.

[8]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[9]  Nicholas A. Ketz,et al.  Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences , 2010, Neuron.

[10]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[11]  M. Greicius,et al.  Decoding subject-driven cognitive states with whole-brain connectivity patterns. , 2012, Cerebral cortex.

[12]  John H. Gilmore,et al.  The dynamic reorganization of the default-mode network during a visual classification task , 2013, Front. Syst. Neurosci..

[13]  B. T. Thomas Yeo,et al.  Estimates of segregation and overlap of functional connectivity networks in the human cerebral cortex , 2014, NeuroImage.

[14]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[15]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[16]  Edward T. Bullmore,et al.  Neuroinformatics Original Research Article , 2022 .

[17]  Jonathan D. Power,et al.  A Parcellation Scheme for Human Left Lateral Parietal Cortex , 2010, Neuron.

[18]  Jennifer A. Mangels,et al.  Neocortical Connectivity during Episodic Memory Formation , 2006, PLoS biology.

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

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

[21]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[22]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[23]  R. Buckner,et al.  Cerebellar asymmetry and its relation to cerebral asymmetry estimated by intrinsic functional connectivity. , 2013, Journal of neurophysiology.

[24]  T. Milner,et al.  Functionally Specific Changes in Resting-State Sensorimotor Networks after Motor Learning , 2011, The Journal of Neuroscience.

[25]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[26]  D. Schacter,et al.  Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. , 2010, Cerebral cortex.

[27]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

[28]  B. Stein,et al.  The Merging of the Senses , 1993 .

[29]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[30]  J. Duyn,et al.  Time-varying functional network information extracted from brief instances of spontaneous brain activity , 2013, Proceedings of the National Academy of Sciences.

[31]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[32]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[33]  Peter J Hellyer,et al.  The Control of Global Brain Dynamics: Opposing Actions of Frontoparietal Control and Default Mode Networks on Attention , 2014, The Journal of Neuroscience.

[34]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[35]  M. Kerszberg,et al.  A Neuronal Model of a Global Workspace in Effortful Cognitive Tasks , 2001 .

[36]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

[37]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Engel,et al.  Intrinsic Coupling Modes: Multiscale Interactions in Ongoing Brain Activity , 2013, Neuron.

[39]  Andreas Kleinschmidt,et al.  Spontaneous local variations in ongoing neural activity bias perceptual decisions , 2008, Proceedings of the National Academy of Sciences.

[40]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[41]  Edwin M. Robertson,et al.  The Resting Human Brain and Motor Learning , 2009, Current Biology.

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

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

[44]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[45]  Dimitri Van De Ville,et al.  Decoding brain states from fMRI connectivity graphs , 2011, NeuroImage.

[46]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

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

[48]  Xi-Nian Zuo,et al.  Reliable intrinsic connectivity networks: Test–retest evaluation using ICA and dual regression approach , 2010, NeuroImage.

[49]  B. T. Thomas Yeo,et al.  The Organization of Local and Distant Functional Connectivity in the Human Brain , 2010, PLoS Comput. Biol..

[50]  Edward T. Bullmore,et al.  Human Brain Functional Network Changes Associated with Enhanced and Impaired Attentional Task Performance , 2013, The Journal of Neuroscience.

[51]  Polina Golland,et al.  Discovering structure in the space of fMRI selectivity profiles , 2010, NeuroImage.

[52]  Michelle Hampson,et al.  Changes in functional connectivity of human MT/V5 with visual motion input , 2004, Neuroreport.

[53]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[54]  A. McIntosh,et al.  Functional Connectivity of the Medial Temporal Lobe Relates to Learning and Awareness , 2003, The Journal of Neuroscience.

[55]  André J. W. van der Kouwe,et al.  Brain morphometry with multiecho MPRAGE , 2008, NeuroImage.

[56]  C. Kelly,et al.  The extrinsic and intrinsic functional architectures of the human brain are not equivalent. , 2013, Cerebral cortex.

[57]  David A. Leopold,et al.  Ongoing physiological processes in the cerebral cortex , 2012, NeuroImage.

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

[59]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[60]  Gustavo Deco,et al.  Resting brains never rest: computational insights into potential cognitive architectures , 2013, Trends in Neurosciences.

[61]  R. Buckner,et al.  Evidence for the Default Network's Role in Spontaneous Cognition , 2010 .

[62]  Thomas E. Nichols,et al.  Functional connectomics from resting-state fMRI , 2013, Trends in Cognitive Sciences.

[63]  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.

[64]  M. Corbetta,et al.  Individual variability in functional connectivity predicts performance of a perceptual task , 2012, Proceedings of the National Academy of Sciences.

[65]  Dominik Heider,et al.  Impact of Working Memory Load on fMRI Resting State Pattern in Subsequent Resting Phases , 2009, PloS one.

[66]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

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

[69]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[70]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[71]  Marvin M Chun,et al.  Category-selective background connectivity in ventral visual cortex. , 2012, Cerebral cortex.

[72]  Cedric E. Ginestet,et al.  Cognitive relevance of the community structure of the human brain functional coactivation network , 2013, Proceedings of the National Academy of Sciences.

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

[74]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[76]  Karl J. Friston,et al.  Functional ontologies for cognition: The systematic definition of structure and function , 2005, Cognitive neuropsychology.

[77]  N. Volkow,et al.  Association between functional connectivity hubs and brain networks. , 2011, Cerebral cortex.

[78]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[79]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[80]  J. W. Belliveau,et al.  Functional Brain Mapping Using Magnetic Resonance Imaging , 1991, Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society Volume 13: 1991.

[81]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[82]  Edward E. Smith,et al.  A parametric study of prefrontal cortex involvement in human working memory , 1996, NeuroImage.

[83]  Amanda Elton,et al.  Divergent task-dependent functional connectivity of executive control and salience networks , 2014, Cortex.

[84]  G. Deco,et al.  Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors , 2012, The Journal of Neuroscience.