Resting-State Coupling between Core Regions within the Central-Executive and Salience Networks Contributes to Working Memory Performance

Previous studies investigated the distinct roles played by different cognitive regions and suggested that the patterns of connectivity of these regions are associated with working memory (WM). However, the specific causal mechanism through which the neuronal circuits that involve these brain regions contribute to WM is still unclear. Here, in a large sample of healthy young adults, we first identified the core WM regions by linking WM accuracy to resting-state functional connectivity with the bilateral dorsolateral prefrontal cortex (dLPFC; a principal region in the central-executive network, CEN). Then a spectral dynamic causal modeling (spDCM) analysis was performed to quantify the effective connectivity between these regions. Finally, the effective connectivity was correlated with WM accuracy to characterize the relationship between these connections and WM performance. We found that the functional connections between the bilateral dLPFC and the dorsal anterior cingulate cortex (dACC) and between the right dLPFC and the left orbital fronto-insular cortex (FIC) were correlated with WM accuracy. Furthermore, the effective connectivity from the dACC to the bilateral dLPFC and from the right dLPFC to the left FIC could predict individual differences in WM. Because the dACC and FIC are core regions of the salience network (SN), we inferred that the inter- and causal-connectivity between core regions within the CEN and SN is functionally relevant for WM performance. In summary, the current study identified the dLPFC-related resting-state effective connectivity underlying WM and suggests that individual differences in cognitive ability could be characterized by resting-state effective connectivity.

[1]  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.

[2]  F. Collette,et al.  Brain imaging of the central executive component of working memory , 2002, Neuroscience & Biobehavioral Reviews.

[3]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[4]  A. Baddeley The episodic buffer: a new component of working memory? , 2000, Trends in Cognitive Sciences.

[5]  Jun Li,et al.  Brain spontaneous functional connectivity and intelligence , 2008, NeuroImage.

[6]  Helen Barbas,et al.  Anterior Cingulate Synapses in Prefrontal Areas 10 and 46 Suggest Differential Influence in Cognitive Control , 2010, The Journal of Neuroscience.

[7]  Michelle Hampson,et al.  Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. , 2010, Magnetic resonance imaging.

[8]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[9]  Kaustubh Supekar,et al.  Dynamic Reconfiguration of Structural and Functional Connectivity Across Core Neurocognitive Brain Networks with Development , 2011, The Journal of Neuroscience.

[10]  Bharat B. Biswal,et al.  Identifying the default mode network structure using dynamic causal modeling on resting-state functional magnetic resonance imaging , 2014, NeuroImage.

[11]  M. Casanova,et al.  Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans , 2008, Neuroscience Letters.

[12]  Heike Schmidt,et al.  No gender differences in brain activation during the N‐back task: An fMRI study in healthy individuals , 2009, Human brain mapping.

[13]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[14]  Bertrand Audoin,et al.  Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis , 2005, NeuroImage.

[15]  A. Anastasi Individual differences. , 2020, Annual review of psychology.

[16]  R. Engle,et al.  The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: An individual-differences perspective , 2002, Psychonomic bulletin & review.

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

[18]  Karl J. Friston Dynamic causal modeling and Granger causality Comments on: The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution , 2011, NeuroImage.

[19]  Hesheng Liu,et al.  Functional Connectivity Architecture of the Human Brain , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[21]  L. F. Barrett,et al.  Individual differences in working memory capacity and dual-process theories of the mind. , 2004, Psychological bulletin.

[22]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[23]  D. Norman,et al.  Attention to action: Willed and automatic control , 1980 .

[24]  A. Baddeley Working Memory: The Interface between Memory and Cognition , 1992, Journal of Cognitive Neuroscience.

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

[26]  Karl J. Friston,et al.  Remote Effects of Hippocampal Sclerosis on Effective Connectivity during Working Memory Encoding: A Case of Connectional Diaschisis? , 2012, Cerebral cortex.

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

[28]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

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

[30]  Angela R. Laird,et al.  Modelling neural correlates of working memory: A coordinate-based meta-analysis , 2012, NeuroImage.

[31]  Walter Schneider,et al.  Controlled & automatic processing: behavior, theory, and biological mechanisms , 2003, Cogn. Sci..

[32]  Karl J. Friston Causal Modelling and Brain Connectivity in Functional Magnetic Resonance Imaging , 2009, PLoS biology.

[33]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[34]  Jen-Chuen Hsieh,et al.  Cortico-striatal disconnection within the cingulo-opercular network in schizophrenia revealed by intrinsic functional connectivity analysis: A resting fMRI study , 2012, NeuroImage.

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

[36]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[37]  R. Engle,et al.  Individual differences in working memory capacity and what they tell us about controlled attention, general fluid intelligence, and functions of the prefrontal cortex. , 1999 .

[38]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[39]  Karl Magnus Petersson,et al.  Interaction between a verbal working memory network and the medial temporal lobe , 2006, NeuroImage.

[40]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[41]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[42]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[43]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[44]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[45]  P. Liddle,et al.  Neural Primacy of the Salience Processing System in Schizophrenia , 2013, Neuron.

[46]  D. Stuss,et al.  Cognitive neuroscience. , 1993, Current opinion in neurobiology.

[47]  Hidenao Fukuyama,et al.  Functional roles of the cingulo-frontal network in performance on working memory , 2004, NeuroImage.

[48]  Karl J. Friston,et al.  Modelling functional integration: a comparison of structural equation and dynamic causal models , 2004, NeuroImage.

[49]  Evan M. Gordon,et al.  Resting-state striato-frontal functional connectivity is sensitive to DAT1 genotype and predicts executive function. , 2015, Cerebral cortex.

[50]  Evan M Gordon,et al.  Using spatial multiple regression to identify intrinsic connectivity networks involved in working memory performance , 2012, Human brain mapping.

[51]  Adeel Razi,et al.  A DCM for resting state fMRI , 2014, NeuroImage.

[52]  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.

[53]  Angela R. Laird,et al.  Comparison of structural covariance with functional connectivity approaches exemplified by an investigation of the left anterior insula , 2014, NeuroImage.

[54]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[55]  B. Biswal,et al.  Correspondence of executive function related functional and anatomical alterations in aging brain , 2014, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[56]  B. J. Casey,et al.  Activation of the prefrontal cortex in a nonspatial working memory task with functional MRI , 1994, Human brain mapping.

[57]  Hidenao Fukuyama,et al.  The neural basis of executive function in working memory: an fMRI study based on individual differences , 2004, NeuroImage.

[58]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[59]  Maria V. Sanchez-Vives,et al.  Hyperpolarization-activated graded persistent activity in the prefrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[60]  R. Gur,et al.  Working memory deficit as a core neuropsychological dysfunction in schizophrenia. , 2003, The American journal of psychiatry.

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

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

[63]  Y. Zang,et al.  Intrinsic resting‐state activity predicts working memory brain activation and behavioral performance , 2013, Human brain mapping.

[64]  R. Cheloha,et al.  The of a Development , 2004 .

[65]  R. Poldrack Can cognitive processes be inferred from neuroimaging data? , 2006, Trends in Cognitive Sciences.

[66]  Donald A. Norman,et al.  Attention to Action , 1986 .

[67]  M. Posner,et al.  The Development of Executive Attention: Contributions to the Emergence of Self-Regulation , 2005, Developmental neuropsychology.

[68]  Andreas Schulze-Bonhage,et al.  Remote effects of hippocampal damage on default network connectivity in the human brain , 2009, Journal of Neurology.

[69]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[70]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[71]  Karl J. Friston,et al.  Resting state functional MRI in Parkinson’s disease: the impact of deep brain stimulation on ‘effective’ connectivity , 2014, Brain : a journal of neurology.

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

[73]  Adeel Razi,et al.  Construct validation of a DCM for resting state fMRI , 2015, NeuroImage.

[74]  J. Allman,et al.  Dendritic architecture of the von Economo neurons , 2006, Neuroscience.

[75]  S. Hogg-Johnson,et al.  A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[76]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[77]  Yuan Zhou,et al.  Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI , 2007, Neuroscience Letters.

[78]  K. R. Ridderinkhof,et al.  Probability effects in the stop-signal paradigm: The insula and the significance of failed inhibition , 2006, Brain Research.