Divergent task-dependent functional connectivity of executive control and salience networks

BACKGROUND Previous studies have demonstrated task-dependent functional interactions of a frontal-parietal control system with the competing dorsal attention (DA) and default mode networks (DM). However, evidence suggests that the frontal-parietal control system is functionally heterogeneous, consisting of two distinct sub-networks that demonstrate dissociable intrinsic functional connectivity (FC) patterns: a frontal-parietal "executive control network" (CON) and a cingulo-opercular "salience network" (SAL). In this study, we aimed to test the hypothesis that CON and SAL would show dissociable task-dependent changes in connectivity with regard to the competing DA and DM when switching from rest to external task performance. METHODS Nineteen healthy adults underwent four functional MRI scans: two during rest and two while performing a global-local selective attention task. Seed-based FC defined the CON and SAL. Connectivity changes between task and rest states were assessed by analysis of variance. The relationship of task-dependent changes in connectivity for each of these networks with behavioral measures was also characterized. RESULTS CON and SAL demonstrated distinct stable and task-dependent regional connectivity. Whereas CON primarily increased FC with visual cortex regions associated with the DA during task performance versus rest, the SAL increased coupling with regions belonging to the DM. Greater dissociation between CON and SAL and between regions with which they coupled during task was associated with better task accuracy. CONCLUSIONS The divergent task-dependent dynamics of CON and SAL connectivity with the anti-correlated DA and DM support distinct functional roles of these two "control" networks.

[1]  Robert Desimone,et al.  Feature-Based Attention in the Frontal Eye Field and Area V4 during Visual Search , 2011, Neuron.

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

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

[4]  Jin Fan,et al.  Effective Connectivity of the Fronto-parietal Network during Attentional Control , 2010, Journal of Cognitive Neuroscience.

[5]  Leslie G. Ungerleider,et al.  The prefrontal cortex and the executive control of attention , 2008, Experimental Brain Research.

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

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

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

[9]  F. Xavier Castellanos,et al.  Large-scale brain systems in ADHD: beyond the prefrontal–striatal model , 2012, Trends in Cognitive Sciences.

[10]  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.

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

[12]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[13]  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.

[14]  Gregory V. Simpson,et al.  Evidence for Anterior Cingulate Cortex Involvement in Monitoring Preparatory Attentional Set , 2002, NeuroImage.

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

[16]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

[17]  L. M. Warner,et al.  The Neural Mechanisms for Minimizing Cross-Modal Distraction , 2004, The Journal of Neuroscience.

[18]  Dwight J. Kravitz,et al.  Attentional control: Temporal relationships within the fronto-parietal network , 2012, Neuropsychologia.

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

[20]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

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

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

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

[24]  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.

[25]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[26]  R. Passingham,et al.  Motivation to do well enhances responses to errors and self-monitoring. , 2009, Cerebral cortex.

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

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

[29]  Mark D'Esposito,et al.  The salience network causally influences default mode network activity during moral reasoning. , 2013, Brain : a journal of neurology.

[30]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[31]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

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

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

[35]  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.

[36]  L. Yao,et al.  Top-Down Regulation of Default Mode Activity in Spatial Visual Attention , 2013, The Journal of Neuroscience.

[37]  André Aleman,et al.  Activation of Anterior Insula during Self-Reflection , 2009, PloS one.

[38]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[39]  M. Corbetta,et al.  Functional network dysfunction in anxiety and anxiety disorders , 2012, Trends in Neurosciences.

[40]  Carrie L. Masten,et al.  Neural correlates of direct and reflected self-appraisals in adolescents and adults: when social perspective-taking informs self-perception. , 2009, Child development.

[41]  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.

[42]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

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

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

[45]  Michael W. Cole,et al.  The role of default network deactivation in cognition and disease , 2012, Trends in Cognitive Sciences.

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

[47]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[48]  Jeffrey M. Zacks,et al.  Rapid Self-Paced Event-Related Functional MRI: Feasibility and Implications of Stimulus- versus Response-Locked Timing , 2001, NeuroImage.

[49]  H. Critchley.  Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

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

[51]  Thomas E. Nichols,et al.  Switching attention and resolving interference: fMRI measures of executive functions , 2003, Neuropsychologia.

[52]  John D. Carew,et al.  Independent component analysis applied to self-paced functional MR imaging paradigms , 2005, NeuroImage.