Definition and characterization of an extended multiple-demand network

ABSTRACT Neuroimaging evidence suggests that executive functions (EF) depend on brain regions that are not closely tied to specific cognitive demands but rather to a wide range of behaviors. A multiple‐demand (MD) system has been proposed, consisting of regions showing conjoint activation across multiple demands. Additionally, a number of studies defining networks specific to certain cognitive tasks suggest that the MD system may be composed of a number of sub‐networks each subserving specific roles within the system. We here provide a robust definition of an extended MDN (eMDN) based on task‐dependent and task‐independent functional connectivity analyses seeded from regions previously shown to be convergently recruited across neuroimaging studies probing working memory, attention and inhibition, i.e., the proposed key components of EF. Additionally, we investigated potential sub‐networks within the eMDN based on their connectional and functional similarities. We propose an eMDN network consisting of a core whose integrity should be crucial to performance of most operations that are considered higher cognitive or EF. This then recruits additional areas depending on specific demands. HighlightsA neurobiological substrate for executive processes is proposed.Proposed network consists of a core, crucial to performance of executive functions.Core network in turn recruits other brain regions depending on specific demands.Hierarchical clustering grouped regions into three cliques each with specific roles.

[1]  Duke Tanaka,et al.  Thalamic projections of the dorsomedial prefrontal cortex in the rhesus monkey (Macaca mulatta) , 1976, Brain Research.

[2]  Margot J. Taylor,et al.  The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia , 2013, Human brain mapping.

[3]  M. Raichle,et al.  On the existence of a generalized non-specific task-dependent network , 2015, Front. Hum. Neurosci..

[4]  Danilo Bzdok,et al.  The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data , 2011, BMC Research Notes.

[5]  Steen Moeller,et al.  ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging , 2014, NeuroImage.

[6]  Koji Jimura,et al.  Sub-centimeter scale functional organization in human inferior frontal gyrus , 2009, NeuroImage.

[7]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

[8]  J. Steven Reznick,et al.  Early Development of Executive Function: A Problem-Solving Framework , 1997 .

[9]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[10]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[11]  Tianzi Jiang,et al.  The Right Dorsal Premotor Mosaic: Organization, Functions, and Connectivity , 2016, Cerebral cortex.

[12]  A. Aron,et al.  Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex , 2010, Proceedings of the National Academy of Sciences.

[13]  K. Zilles,et al.  Differentiated parietal connectivity of frontal regions for “what” and “where” memory , 2012, Brain Structure and Function.

[14]  T. A. Kelley,et al.  Cortical mechanisms for shifting and holding visuospatial attention. , 2008, Cerebral cortex.

[15]  Marc A Sommer,et al.  The role of the thalamus in motor control , 2003, Current Opinion in Neurobiology.

[16]  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.

[17]  Angela R. Laird,et al.  Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation , 2011, NeuroImage.

[18]  R. Guillery,et al.  Thalamic Relay Functions and Their Role in Corticocortical Communication Generalizations from the Visual System , 2002, Neuron.

[19]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[20]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[21]  Angela R. Laird,et al.  Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation , 2016, NeuroImage.

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

[23]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[24]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[25]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[26]  G. Fink,et al.  Dorsal and Ventral Attention Systems : Distinct Neural Circuits but Collaborative Roles , 2013 .

[27]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[28]  Y. Miyashita,et al.  Preparation to Inhibit a Response Complements Response Inhibition during Performance of a Stop-Signal Task , 2009, The Journal of Neuroscience.

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

[30]  A. Jensen,et al.  The g factor , 1996, Nature.

[31]  Angela R. Laird,et al.  Definition and characterization of an extended social-affective default network , 2014, Brain Structure and Function.

[32]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[33]  S. Eickhoff,et al.  Interindividual differences in cognitive flexibility: influence of gray matter volume, functional connectivity and trait impulsivity , 2014, Brain Structure and Function.

[34]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

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

[36]  Carol A. Seger,et al.  The Basal Ganglia in Human Learning , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[37]  Rebecca Elliott,et al.  Executive functions and their disorders. , 2003, British medical bulletin.

[38]  Simon B. Eickhoff,et al.  Psychosocial versus physiological stress — Meta-analyses on deactivations and activations of the neural correlates of stress reactions , 2015, NeuroImage.

[39]  P. Strick,et al.  Cerebellar output channels. , 1997, International review of neurobiology.

[40]  P. Fox,et al.  Mapping context and content: the BrainMap model , 2002, Nature Reviews Neuroscience.

[41]  Thierry Bal,et al.  Sensory gating mechanisms of the thalamus , 1994, Current Opinion in Neurobiology.

[42]  Takao K. Hensch,et al.  Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation , 2014, Neuron.

[43]  E. Irle,et al.  Cortical and subcortical afferent connections of the primate's temporal pole: A study of rhesus monkeys, squirrel monkeys, and marmosets , 1985, The Journal of comparative neurology.

[44]  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.

[45]  Kimberly L. Ray,et al.  Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions , 2012, Cognitive, affective & behavioral neuroscience.

[46]  Lumy Sawaki,et al.  The contribution of the putamen to sensory aspects of pain: insights from structural connectivity and brain lesions. , 2011, Brain : a journal of neurology.

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

[48]  Margaret D. King,et al.  The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry , 2012, Front. Neurosci..

[49]  J. Duncan The Structure of Cognition: Attentional Episodes in Mind and Brain , 2013, Neuron.

[50]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[51]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[52]  Ikuko Mukai,et al.  A role of right middle frontal gyrus in reorienting of attention: a case study , 2015, Front. Syst. Neurosci..

[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]  C. Bellone,et al.  ON A ROLE , 1996 .

[55]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[56]  Simon B. Eickhoff,et al.  Multimodal connectivity of motor learning-related dorsal premotor cortex , 2015, NeuroImage.

[57]  P. Fox,et al.  Dysregulated left inferior parietal activity in schizophrenia and depression: functional connectivity and characterization , 2013, Front. Hum. Neurosci..

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

[59]  D. Joel,et al.  The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated , 1994, Neuroscience.

[60]  Simon B Eickhoff,et al.  Meta-analysis in human neuroimaging: computational modeling of large-scale databases. , 2014, Annual review of neuroscience.

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

[62]  L. Tremblay,et al.  Motor control in basal ganglia circuits using fMRI and brain atlas approaches. , 2006, Cerebral cortex.

[63]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[64]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[65]  P. Schwartzkroin,et al.  Neural mechanisms. , 1994, Science.

[66]  S. Eickhoff,et al.  Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. , 2013, Psychological bulletin.

[67]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[68]  Angela R. Laird,et al.  Networks of task co-activations , 2013, NeuroImage.

[69]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[70]  P. Zelazo,et al.  Executive Function in Typical and Atypical Development , 2010 .

[71]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[72]  N. H. Timm Applied Multivariate Analysis , 2002 .

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

[74]  J. Alvarez,et al.  Executive Function and the Frontal Lobes: A Meta-Analytic Review , 2006, Neuropsychology Review.

[75]  Muriel D. Lezak,et al.  The Problem of Assessing Executive Functions , 1982 .

[76]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[77]  Ralph Weidner,et al.  Dynamic Coding of Events within the Inferior Frontal Gyrus in a Probabilistic Selective Attention Task , 2011, Journal of Cognitive Neuroscience.

[78]  S. Eickhoff,et al.  Neuroscience and Biobehavioral Reviews Three Key Regions for Supervisory Attentional Control: Evidence from Neuroimaging Meta-analyses , 2022 .

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

[80]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[81]  Adam G. Thomas,et al.  Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas in Monkey Frontal Cortex , 2014, Neuron.

[82]  Karl J. Friston,et al.  Cortical and subcortical localization of response to pain in man using positron emission tomography , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  P. Fox,et al.  Identification of a common neurobiological substrate for mental illness. , 2015, JAMA psychiatry.

[85]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[86]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[87]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.