Anticorrelation between default and dorsal attention networks varies across default subsystems and cognitive states

Anticorrelation between the default network (DN) and dorsal attention network (DAN) is thought to be an intrinsic aspect of functional brain organization reflecting competing functions. However, the stability of anticorrelations across distinct DN subsystems, different contexts, and time, remains unexplored. Here we examine DN-DAN functional connectivity across six different cognitive states. We show that:(i) the DAN is anticorrelated with the DN core subsystem, but not with the two DN subsystems involved in mentalizing and mnemonic functions, respectively; (ii) DN-DAN interactions vary significantly across cognitive states; (iii) DN-DAN connectivity fluctuates across time between periods of anticorrelation and periods of positive correlation; and (iv) coupling between the frontoparietal control network (FPCN) and DAN predicts variation in the strength of DN-DAN anticorrelation across time. These findings reveal substantial variability in DN-DAN interactions, suggesting that these networks are not strictly competitive, and that the FPCN may act to modulate their anticorrelation strength.

[1]  C. Honey,et al.  Mapping human brain networks with cortico-cortical evoked potentials , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

[3]  Marie Schaer,et al.  Degrees of separation: A quantitative neuroimaging meta-analysis investigating self-specificity and shared neural activation between self- and other-reflection , 2012, Neuroscience & Biobehavioral Reviews.

[4]  Danielle S. Bassett,et al.  Brain Network Adaptability across Task States , 2014, PLoS Comput. Biol..

[5]  John D. E. Gabrieli,et al.  Selective Development of Anticorrelated Networks in the Intrinsic Functional Organization of the Human Brain , 2014, Journal of Cognitive Neuroscience.

[6]  Daniel S. Margulies,et al.  A Correspondence between Individual Differences in the Brain's Intrinsic Functional Architecture and the Content and Form of Self-Generated Thoughts , 2014, PloS one.

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

[8]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[9]  J. Duncan.  The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[10]  Jonathan Smallwood,et al.  The balanced mind: the variability of task-unrelated thoughts predicts error monitoring , 2013, Front. Hum. Neurosci..

[11]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

[12]  S. Petersen,et al.  Brain Networks and Cognitive Architectures , 2015, Neuron.

[13]  Matthew L. Dixon,et al.  A framework for understanding the relationship between externally and internally directed cognition , 2014, Neuropsychologia.

[14]  Sterling C. Johnson,et al.  Relevance to self: A brief review and framework of neural systems underlying appraisal , 2007, Neuroscience & Biobehavioral Reviews.

[15]  Bernard Ng,et al.  Identification of Mood-Relevant Brain Connections Using a Continuous, Subject-Driven Rumination Paradigm. , 2016, Cerebral cortex.

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

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

[18]  B. T. Thomas Yeo,et al.  Cerebral functional connectivity periodically (de)synchronizes with anatomical constraints , 2015, Brain Structure and Function.

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

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

[21]  N. Farb,et al.  Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference. , 2007, Social cognitive and affective neuroscience.

[22]  R. N. Spreng,et al.  Attenuated anticorrelation between the default and dorsal attention networks with aging: evidence from task and rest , 2016, Neurobiology of Aging.

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

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

[25]  A. Nobre,et al.  Orienting Attention Based on Long-Term Memory Experience , 2006, Neuron.

[26]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

[27]  Y. Saalmann,et al.  Functional and structural architecture of the human dorsal frontoparietal attention network , 2013, Proceedings of the National Academy of Sciences.

[28]  Scott R Sponheim,et al.  Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition , 2013, Nature Neuroscience.

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

[30]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

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

[32]  R. Jewkes,et al.  Perceptions and Experiences of Research Participants on Gender-Based Violence Community Based Survey: Implications for Ethical Guidelines , 2012, PloS one.

[33]  Paula Tavares,et al.  Paying attention to social meaning: an FMRI study. , 2008, Cerebral cortex.

[34]  A. Damasio,et al.  Neural correlates of different self domains , 2015, Brain and behavior.

[35]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[36]  M. Chun,et al.  Interactions between attention and memory , 2007, Current Opinion in Neurobiology.

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

[38]  Todd W. Thompson,et al.  Resting-state anticorrelations between medial and lateral prefrontal cortex: Association with working memory, aging, and individual differences , 2014, Cortex.

[39]  Kevin N. Ochsner,et al.  A Meta-analysis of Functional Neuroimaging Studies of Self- and Other Judgments Reveals a Spatial Gradient for Mentalizing in Medial Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

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

[41]  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.

[42]  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.

[43]  B T Thomas Yeo,et al.  Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Wen-Ming Luh,et al.  Goal-Congruent Default Network Activity Facilitates Cognitive Control , 2014, The Journal of Neuroscience.

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

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

[47]  Linda Geerligs,et al.  State and Trait Components of Functional Connectivity: Individual Differences Vary with Mental State , 2015, The Journal of Neuroscience.

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

[49]  M. Hasselmo,et al.  High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. , 2004, Progress in brain research.

[50]  R. Buckner,et al.  Parcellating Cortical Functional Networks in Individuals , 2015, Nature Neuroscience.

[51]  K. Christoff,et al.  Undirected thought: Neural determinants and correlates , 2012, Brain Research.

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

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

[54]  Daniel L. Schacter,et al.  Intrinsic Architecture Underlying the Relations among the Default, Dorsal Attention, and Frontoparietal Control Networks of the Human Brain , 2013, Journal of Cognitive Neuroscience.

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

[56]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[57]  Bernard Mazoyer,et al.  Patterns of hemodynamic low-frequency oscillations in the brain are modulated by the nature of free thought during rest , 2012, NeuroImage.

[58]  Dost Öngür,et al.  Anticorrelations in resting state networks without global signal regression , 2012, NeuroImage.

[59]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[60]  S. Baron-Cohen,et al.  The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

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

[62]  Kevin S. Brown,et al.  Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought , 2012, Brain Research.

[63]  R. Malach,et al.  Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems , 2008, Neuropsychologia.

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

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

[66]  Matthew L. Dixon,et al.  The lateral prefrontal cortex and complex value-based learning and decision making , 2014, Neuroscience & Biobehavioral Reviews.

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

[68]  E. Thompson,et al.  Specifying the self for cognitive neuroscience , 2011, Trends in Cognitive Sciences.

[69]  S. Gallagher.  Philosophical conceptions of the self: implications for cognitive science , 2000, Trends in Cognitive Sciences.

[70]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[71]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[72]  Elliot T. Berkman,et al.  Evidence for social working memory from a parametric functional MRI study , 2012, Proceedings of the National Academy of Sciences.

[73]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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

[75]  Matthew L. Dixon,et al.  The Decision to Engage Cognitive Control Is Driven by Expected Reward-Value: Neural and Behavioral Evidence , 2012, PloS one.

[76]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[77]  Zachary C. Irving,et al.  Mind-wandering as spontaneous thought: a dynamic framework , 2016, Nature Reviews Neuroscience.

[78]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[79]  E. Thompson,et al.  The Kantian brain: brain dynamics from a neurophenomenological perspective , 2015, Current Opinion in Neurobiology.

[80]  R. N. Spreng,et al.  The default network and self‐generated thought: component processes, dynamic control, and clinical relevance , 2014, Annals of the New York Academy of Sciences.

[81]  Marc Joliot,et al.  The resting state questionnaire: An introspective questionnaire for evaluation of inner experience during the conscious resting state , 2010, Brain Research Bulletin.

[82]  Rebecca M. Todd,et al.  Dynamics of neural recruitment surrounding the spontaneous arising of thoughts in experienced mindfulness practitioners , 2016, NeuroImage.

[83]  C. Pennartz,et al.  The Hippocampus Is Coupled with the Default Network during Memory Retrieval but Not during Memory Encoding , 2011, PloS one.

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

[85]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[86]  Michael W. Cole,et al.  The Behavioral Relevance of Task Information in Human Prefrontal Cortex. , 2016, Cerebral cortex.

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

[88]  C. Grady,et al.  Age differences in the functional interactions among the default, frontoparietal control, and dorsal attention networks , 2016, Neurobiology of Aging.

[89]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[90]  R. Poldrack,et al.  Temporal metastates are associated with differential patterns of time-resolved connectivity, network topology, and attention , 2016, Proceedings of the National Academy of Sciences.

[91]  S. Kastner,et al.  From Behavior to Neural Dynamics: An Integrated Theory of Attention , 2015, Neuron.

[92]  Erik D. Reichle,et al.  Meta-awareness, perceptual decoupling and the wandering mind , 2011, Trends in Cognitive Sciences.

[93]  Danielle S. Bassett,et al.  Structurally-Constrained Relationships between Cognitive States in the Human Brain , 2014, PLoS Comput. Biol..

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

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

[96]  J. Haxby,et al.  The representation of self and person knowledge in the medial prefrontal cortex. , 2012, Wiley interdisciplinary reviews. Cognitive science.

[97]  R. Nathan Spreng,et al.  The wandering brain: Meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes , 2015, NeuroImage.

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

[99]  Laura C. Buchanan,et al.  Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns , 2015, Proceedings of the National Academy of Sciences.

[100]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[101]  P. Fransson.  Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

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

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

[104]  Earl K Miller,et al.  Cortical circuits for the control of attention , 2012, Current Opinion in Neurobiology.

[105]  Rafael Malach,et al.  Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. , 2007, Cerebral cortex.

[106]  R. Marois,et al.  Capacity limits of information processing in the brain , 2005, Trends in Cognitive Sciences.