A Domain-General Cognitive Core Defined in Multimodally Parcellated Human Cortex

Abstract Numerous brain imaging studies identified a domain-general or “multiple-demand” (MD) activation pattern accompanying many tasks and may play a core role in cognitive control. Though this finding is well established, the limited spatial localization provided by traditional imaging methods precluded a consensus regarding the precise anatomy, functional differentiation, and connectivity of the MD system. To address these limitations, we used data from 449 subjects from the Human Connectome Project, with the cortex of each individual parcellated using neurobiologically grounded multimodal MRI features. The conjunction of three cognitive contrasts reveals a core of 10 widely distributed MD parcels per hemisphere that are most strongly activated and functionally interconnected, surrounded by a penumbra of 17 additional areas. Outside cerebral cortex, MD activation is most prominent in the caudate and cerebellum. Comparison with canonical resting-state networks shows MD regions concentrated in the fronto-parietal network but also engaging three other networks. MD activations show modest relative task preferences accompanying strong co-recruitment. With distributed anatomical organization, mosaic functional preferences, and strong interconnectivity, we suggest MD regions are well positioned to integrate and assemble the diverse components of cognitive operations. Our precise delineation of MD regions provides a basis for refined analyses of their functions.

[1]  David Badre,et al.  Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms. , 2004, Cerebral cortex.

[2]  Xiao-Jing Wang,et al.  The importance of mixed selectivity in complex cognitive tasks , 2013, Nature.

[3]  John Duncan,et al.  Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex , 2010, Proceedings of the National Academy of Sciences.

[4]  Adrian M. Owen,et al.  Fractionating Human Intelligence , 2012, Neuron.

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

[6]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[7]  David Badre,et al.  Frontal Cortex and the Hierarchical Control of Behavior , 2018, Trends in Cognitive Sciences.

[8]  C. Chabris,et al.  Neural mechanisms of general fluid intelligence , 2003, Nature Neuroscience.

[9]  O. Sporns,et al.  Network neuroscience , 2017, Nature Neuroscience.

[10]  David Badre,et al.  Cognitive control, hierarchy, and the rostro–caudal organization of the frontal lobes , 2008, Trends in Cognitive Sciences.

[11]  B. Milner Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes , 1963 .

[12]  Peter Janssen,et al.  Functional MRI in Macaque Monkeys during Task Switching , 2018, The Journal of Neuroscience.

[13]  Nikola T. Markov,et al.  A Weighted and Directed Interareal Connectivity Matrix for Macaque Cerebral Cortex , 2012, Cerebral cortex.

[14]  Danielle S. Bassett,et al.  A mechanistic model of connector hubs, modularity and cognition , 2018, Nature Human Behaviour.

[15]  John Duncan,et al.  Executive function and fluid intelligence after frontal lobe lesions , 2009, Brain : a journal of neurology.

[16]  David C Van Essen,et al.  The impact of traditional neuroimaging methods on the spatial localization of cortical areas , 2018, Proceedings of the National Academy of Sciences.

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

[18]  Evan M. Gordon,et al.  Functional System and Areal Organization of a Highly Sampled Individual Human Brain , 2015, Neuron.

[19]  Yuji Naya,et al.  Contributions of primate prefrontal cortex and medial temporal lobe to temporal-order memory , 2017, Proceedings of the National Academy of Sciences.

[20]  D. Pandya,et al.  Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys , 1991, The Journal of comparative neurology.

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

[22]  N. Kanwisher,et al.  Common Neural Mechanisms for Response Selection and Perceptual Processing , 2003, Journal of Cognitive Neuroscience.

[23]  S. Haber,et al.  Estimates of Projection Overlap and Zones of Convergence within Frontal-Striatal Circuits , 2014, The Journal of Neuroscience.

[24]  O. Sporns Contributions and challenges for network models in cognitive neuroscience , 2014, Nature Neuroscience.

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

[26]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[27]  Stanislas Dehaene,et al.  Cortical circuits for mathematical knowledge: evidence for a major subdivision within the brain's semantic networks , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  Michael Petrides,et al.  Single subject analyses reveal consistent recruitment of frontal operculum in performance monitoring , 2016, NeuroImage.

[29]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[30]  John Duncan,et al.  Coding of Visual, Auditory, Rule, and Response Information in the Brain: 10 Years of Multivoxel Pattern Analysis , 2016, Journal of Cognitive Neuroscience.

[31]  F. Diderichsen,et al.  Cancer Stage, Comorbidity, and Socioeconomic Differences in the Effect of Cancer on Labour Market Participation: A Danish Register-Based Follow-Up Study , 2015, PloS one.

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

[33]  Andreea C. Bostan,et al.  Cerebellar networks with the cerebral cortex and basal ganglia , 2013, Trends in Cognitive Sciences.

[34]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[35]  Daniel J Mitchell,et al.  Task Encoding across the Multiple Demand Cortex Is Consistent with a Frontoparietal and Cingulo-Opercular Dual Networks Distinction , 2016, The Journal of Neuroscience.

[36]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

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

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

[39]  Narender Ramnani,et al.  Cerebellum and cognition: evidence for the encoding of higher order rules. , 2013, Cerebral cortex.

[40]  Xiao-Jing Wang,et al.  Internal Representation of Task Rules by Recurrent Dynamics: The Importance of the Diversity of Neural Responses , 2010, Front. Comput. Neurosci..

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

[42]  Stefano Fusi,et al.  Why neurons mix: high dimensionality for higher cognition , 2016, Current Opinion in Neurobiology.

[43]  E. Jefferies,et al.  Anterior temporal lobes mediate semantic representation: Mimicking semantic dementia by using rTMS in normal participants , 2007, Proceedings of the National Academy of Sciences.

[44]  Stephen M. Smith,et al.  Using temporal ICA to selectively remove global noise while preserving global signal in functional MRI data , 2017, NeuroImage.

[45]  Barbara G. Shinn-Cunningham,et al.  Short-Term Memory for Space and Time Flexibly Recruit Complementary Sensory-Biased Frontal Lobe Attention Networks , 2015, Neuron.

[46]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[47]  John Duncan,et al.  Fluid intelligence is supported by the multiple-demand system not the language system , 2018, Nature Human Behaviour.

[48]  John Duncan,et al.  Response of the multiple-demand network during simple stimulus discriminations , 2018, NeuroImage.

[49]  J. Duncan,et al.  Fluid intelligence after frontal lobe lesions , 1995, Neuropsychologia.

[50]  Christopher L. Asplund,et al.  Functional Specialization and Flexibility in Human Association Cortex. , 2016, Cerebral cortex.

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

[52]  K. Christoff,et al.  Prefrontal organization of cognitive control according to levels of abstraction , 2009, Brain Research.

[53]  M. Petrides,et al.  Dissociation within the Frontoparietal Network in Verbal Working Memory: A Parametric Functional Magnetic Resonance Imaging Study , 2010, The Journal of Neuroscience.

[54]  Evan M. Gordon,et al.  Three Distinct Sets of Connector Hubs Integrate Human Brain Function. , 2018, Cell reports.

[55]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[56]  John Duncan,et al.  Hierarchical coding for sequential task events in the monkey prefrontal cortex , 2008, Proceedings of the National Academy of Sciences.

[57]  Kristen A. Ford,et al.  BOLD fMRI activation for anti-saccades in nonhuman primates , 2009, NeuroImage.

[58]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[59]  Anjan Chatterjee,et al.  A bilateral frontoparietal network underlies visuospatial analogical reasoning , 2012, NeuroImage.

[60]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[61]  Stanislas Dehaene,et al.  Origins of the brain networks for advanced mathematics in expert mathematicians , 2016, Proceedings of the National Academy of Sciences.

[62]  Thomas E. Nichols,et al.  Functional connectomics from resting-state fMRI , 2013, Trends in Cognitive Sciences.

[63]  Sabine Kastner,et al.  Thalamic functions in distributed cognitive control , 2017, Nature Neuroscience.

[64]  Jonathan D. Power,et al.  Network measures predict neuropsychological outcome after brain injury , 2014, Proceedings of the National Academy of Sciences.

[65]  Jörn Diedrichsen,et al.  Surface-Based Display of Volume-Averaged Cerebellar Imaging Data , 2015, PloS one.

[66]  Jonathan D. Power,et al.  Evidence for Hubs in Human Functional Brain Networks , 2013, Neuron.

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

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

[69]  Krzysztof J. Gorgolewski,et al.  The Dynamics of Functional Brain Networks: Integrated Network States during Cognitive Task Performance , 2015, Neuron.

[70]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[71]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  Suzanne N. Haber,et al.  Convergence of prefrontal and parietal anatomical projections in a connectional hub in the striatum , 2017, NeuroImage.

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

[74]  Nancy Kanwisher,et al.  Functional specificity for high-level linguistic processing in the human brain , 2011, Proceedings of the National Academy of Sciences.

[75]  N. Sigala,et al.  Dynamic Coding for Cognitive Control in Prefrontal Cortex , 2013, Neuron.

[76]  Jörn Diedrichsen,et al.  Functional boundaries in the human cerebellum revealed by a multi-domain task battery , 2019, Nature Neuroscience.

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

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

[79]  John Duncan,et al.  Progressive Recruitment of the Frontoparietal Multiple-demand System with Increased Task Complexity, Time Pressure, and Reward , 2019, Journal of Cognitive Neuroscience.

[80]  Nancy Kanwisher,et al.  Language-Selective and Domain-General Regions Lie Side by Side within Broca’s Area , 2012, Current Biology.

[81]  Ricardo Pio Monti,et al.  Dissociating frontoparietal brain networks with neuroadaptive Bayesian optimization , 2017, Nature Communications.

[82]  Daniel J Mitchell,et al.  A Putative Multiple-Demand System in the Macaque Brain , 2016, The Journal of Neuroscience.

[83]  N. Kanwisher,et al.  A functional dissociation between language and multiple-demand systems revealed in patterns of BOLD signal fluctuations. , 2014, Journal of neurophysiology.

[84]  Mark Jenkinson,et al.  MSM: A new flexible framework for Multimodal Surface Matching , 2014, NeuroImage.

[85]  Stephen M. Smith,et al.  Classification of temporal ICA components for separating global noise from fMRI data: Reply to Power , 2019, NeuroImage.

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

[87]  S Dehaene,et al.  A neuronal model of a global workspace in effortful cognitive tasks. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[89]  Matthew F. Glasser,et al.  Trends and Properties of Human Cerebral Cortex: Correlations with Cortical Myelin Content Introduction and Review , 2022 .

[90]  Suk Won Han,et al.  Functional Fractionation of the Stimulus-Driven Attention Network , 2014, The Journal of Neuroscience.

[91]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[92]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[93]  John Q. Trojanowski,et al.  dorsolateral prefrontal cortex , 1999 .

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

[95]  A. Battersby Plans and the Structure of Behavior , 1968 .

[96]  Ben M. Crittenden,et al.  Task Difficulty Manipulation Reveals Multiple Demand Activity but no Frontal Lobe Hierarchy , 2012, Cerebral cortex.

[97]  Michael W. Cole,et al.  Mapping the human brain's cortical-subcortical functional network organization , 2018, NeuroImage.

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

[99]  Steen Moeller,et al.  Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project , 2013, NeuroImage.

[100]  Elizabeth Jefferies,et al.  Semantic Processing in the Anterior Temporal Lobes: A Meta-analysis of the Functional Neuroimaging Literature , 2010, Journal of Cognitive Neuroscience.

[101]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[102]  Richard Reviewer-Granger Unified Theories of Cognition , 1991, Journal of Cognitive Neuroscience.

[103]  J. Duncan,et al.  The multiple-demand system but not the language system supports fluid intelligence. , 2018, Nature human behaviour.

[104]  Steen Moeller,et al.  The Human Connectome Project's neuroimaging approach , 2016, Nature Neuroscience.

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

[106]  Daniel Rueckert,et al.  Multimodal surface matching with higher-order smoothness constraints , 2017, NeuroImage.

[107]  T. Powell,et al.  The cortico-striate projection in the monkey. , 1970, Brain : a journal of neurology.

[108]  Matthew F. Glasser,et al.  Parcellating Cerebral Cortex: How Invasive Animal Studies Inform Noninvasive Mapmaking in Humans , 2018, Neuron.

[109]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

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

[111]  A. Luria Higher Cortical Functions in Man , 1980, Springer US.

[112]  D Rudrauf,et al.  Distributed neural system for general intelligence revealed by lesion mapping , 2010, Proceedings of the National Academy of Sciences.

[113]  Kurt E. Weaver,et al.  Mapping anterior temporal lobe language areas with fMRI: A multicenter normative study , 2011, NeuroImage.

[114]  J. Duncan,et al.  Competitive brain activity in visual attention , 1997, Current Opinion in Neurobiology.