The dynamic reorganization of the default-mode network during a visual classification task

The default-mode network has been reported to possess highly versatile and even contrasting functions but the underlying functioning mechanism remains elusive. In this study, we adopt a dynamic view of the default-mode network structure and hypothesize that it could potentially contribute to different functions through dynamic reorganization of its functional interaction pattern within and across network boundaries depending on the ongoing cognitive demands. With four experimental states and functional connectivity magnetic resonance imaging, we show that the default-mode network is characterized by within-network desynchronization and outside-network integration during the transition from resting state to an external visual classification task. Such default-mode network dynamics are task demand-dependent and return to their original status during the transition back to resting. More importantly, the degree of within-network desynchronization correlates with reaction time while the level of outside-network integration indexes task performance accuracy. Overall, the documented dynamic reorganization of the default-mode network and the significant behavioral correlations provide new insights into our understanding of this complex network and emphasize a dynamic view in future studies of its functioning mechanism.

[1]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[2]  Dante Mantini,et al.  Emerging Roles of the Brain’s Default Network , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[3]  E. Stein,et al.  Cingulate activation increases dynamically with response speed under stimulus unpredictability. , 2007, Cerebral cortex.

[4]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Inhibitory Control in High Functioning Autism: Decreased Activation and Underconnectivity in Inhibition Networks Inhibitory Control in High-functioning Autism: Decreased Activation and Underconnectivity in Inhibition Networks , 2022 .

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

[6]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[7]  M. Greicius,et al.  Persistent default‐mode network connectivity during light sedation , 2008, Human brain mapping.

[8]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[9]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[10]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[11]  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.

[12]  Dinggang Shen,et al.  Cerebral Cortex doi:10.1093/cercor/bhs043 Cerebral Cortex Advance Access published February 24, 2012 The Synchronization within and Interaction between the Default and Dorsal Attention Networks in Early Infancy , 2022 .

[13]  P. Fransson How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations , 2006, Neuropsychologia.

[14]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[15]  Cleofé Peña-Gómez,et al.  Brain connectivity during resting state and subsequent working memory task predicts behavioural performance , 2012, Cortex.

[16]  C. Frith,et al.  Comment on "Wandering Minds: The Default Network and Stimulus-Independent Thought" , 2007, Science.

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

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

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

[20]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[21]  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.

[22]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[23]  Marnie E. Shaw,et al.  Default network connectivity during a working memory task , 2011, Human brain mapping.

[24]  D. Schacter,et al.  Remembering the past to imagine the future: the prospective brain , 2007, Nature Reviews Neuroscience.

[25]  Susan A. Sadek,et al.  Atypical neural self-representation in autism. , 2010, Brain : a journal of neurology.

[26]  Wei Gao,et al.  Frontal parietal control network regulates the anti‐correlated default and dorsal attention networks , 2012, Human brain mapping.

[27]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[28]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[29]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[30]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[31]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[32]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[33]  Jessica R. Andrews-Hanna,et al.  The Brain’s Default Network and Its Adaptive Role in Internal Mentation , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[34]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

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

[36]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[37]  Mark T. Waters,et al.  This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.Thislicensedoesnot permit commercial exploitation or the creation of derivative works without sp , 2009 .

[38]  K. R. Ridderinkhof,et al.  Conscious perception of errors and its relation to the anterior insula , 2010, Brain Structure and Function.

[39]  E. Ross The Organization of Will , 1916, American Journal of Sociology.

[40]  H. Critchley,et al.  Neural Activity Relating to Generation and Representation of Galvanic Skin Conductance Responses: A Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[41]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[42]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[43]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[45]  C. Frith,et al.  Performance-related activity in medial rostral prefrontal cortex (area 10) during low-demand tasks. , 2006, Journal of experimental psychology. Human perception and performance.

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

[47]  Hongkeun Kim,et al.  A dual-subsystem model of the brain's default network: Self-referential processing, memory retrieval processes, and autobiographical memory retrieval , 2012, NeuroImage.

[48]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[49]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[50]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[51]  Dinggang Shen,et al.  Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects , 2009, Proceedings of the National Academy of Sciences.

[52]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[53]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[54]  D. Caplan,et al.  Cognition, emotion and the cerebellum. , 2006, Brain : a journal of neurology.

[55]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  D. Schacter,et al.  The cognitive neuroscience of constructive memory: remembering the past and imagining the future , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  Marc Jeannerod,et al.  Modulating the experience of agency: a positron emission tomography study , 2003, NeuroImage.

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

[59]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[60]  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.

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

[62]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[63]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

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

[65]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[66]  Blaise deB Frederick,et al.  Cerebellar Vermis Involvement in Cocaine-Related Behaviors , 2006, Neuropsychopharmacology.

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

[68]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[69]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

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

[71]  Daniel L. Schacter,et al.  Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition , 2010, NeuroImage.

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