Is There “One” DLPFC in Cognitive Action Control? Evidence for Heterogeneity From Co-Activation-Based Parcellation

The dorsolateral prefrontal cortex (DLPFC) has consistently been implicated in cognitive control of motor behavior. There is, however, considerable variability in the exact location and extension of these activations across functional magnetic resonance imaging (fMRI) experiments. This poses the question of whether this variability reflects sampling error and spatial uncertainty in fMRI experiments or structural and functional heterogeneity of this region. This study shows that the right DLPFC as observed in 4 different experiments tapping executive action control may be subdivided into 2 distinct subregions-an anterior-ventral and a posterior-dorsal one -based on their whole-brain co-activation patterns across neuroimaging studies. Investigation of task-dependent and task-independent connectivity revealed both clusters to be involved in distinct neural networks. The posterior subregion showed increased connectivity with bilateral intraparietal sulci, whereas the anterior subregion showed increased connectivity with the anterior cingulate cortex. Functional characterization with quantitative forward and reverse inferences revealed the anterior network to be more strongly associated with attention and action inhibition processes, whereas the posterior network was more strongly related to action execution and working memory. The present data provide evidence that cognitive action control in the right DLPFC may rely on differentiable neural networks and cognitive functions.

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

[2]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

[3]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[4]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

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

[6]  K. Amunts,et al.  The human inferior parietal lobule in stereotaxic space , 2008, Brain Structure and Function.

[7]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[8]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[9]  S. Wise,et al.  Comparison of Strategy Signals in the Dorsolateral and Orbital Prefrontal Cortex , 2011, The Journal of Neuroscience.

[10]  C. Liston,et al.  Anterior Cingulate and Posterior Parietal Cortices Are Sensitive to Dissociable Forms of Conflict in a Task-Switching Paradigm , 2006, Neuron.

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

[12]  K. Zilles,et al.  Neural correlates of developing and adapting behavioral biases in speeded choice reactions--an fMRI study on predictive motor coding. , 2011, Cerebral cortex.

[13]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[14]  N. P. Bichot,et al.  A visual salience map in the primate frontal eye field. , 2005, Progress in brain research.

[15]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[16]  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.

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

[18]  Sang Won Seo,et al.  Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method , 2010, NeuroImage.

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

[20]  Jessica A. Turner,et al.  The Cognitive Paradigm Ontology: Design and Application , 2011, Neuroinformatics.

[21]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[22]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[23]  R. Poldrack Inferring Mental States from Neuroimaging Data: From Reverse Inference to Large-Scale Decoding , 2011, Neuron.

[24]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[25]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[26]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[27]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[29]  E. Hoshi Functional specialization within the dorsolateral prefrontal cortex: A review of anatomical and physiological studies of non-human primates , 2006, Neuroscience Research.

[30]  D. Pandya,et al.  Anatomic Organization of the Basilar Pontine Projections from Prefrontal Cortices in Rhesus Monkey , 1997, The Journal of Neuroscience.

[31]  J. Lurito,et al.  Correlations in Low-Frequency BOLD Fluctuations Reflect Cortico-Cortical Connections , 2000, NeuroImage.

[32]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[33]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[34]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[35]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[36]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

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

[38]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[39]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[40]  A. Schleicher,et al.  Ventral visual cortex in humans: Cytoarchitectonic mapping of two extrastriate areas , 2007, Human brain mapping.

[41]  H. Diener,et al.  On the neural basis of focused and divided attention. , 2005, Brain research. Cognitive brain research.

[42]  Jessica A. Turner,et al.  ALE Meta-Analysis Workflows Via the Brainmap Database: Progress Towards A Probabilistic Functional Brain Atlas , 2009, Front. Neuroinform..

[43]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[44]  Nadim Joni Shah,et al.  Prefrontal involvement in imitation learning of hand actions: Effects of practice and expertise , 2007, NeuroImage.

[45]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[46]  P. Fox,et al.  Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala , 2009, Human brain mapping.

[47]  M. D’Esposito,et al.  Is the rostro-caudal axis of the frontal lobe hierarchical? , 2009, Nature Reviews Neuroscience.

[48]  Mark V. Albert,et al.  Anticipation of conflict monitoring in the anterior cingulate cortex and the prefrontal cortex , 2007, Proceedings of the National Academy of Sciences.

[49]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[50]  Simon B Eickhoff,et al.  Modulating the processing of emotional stimuli by cognitive demand. , 2012, Social cognitive and affective neuroscience.

[51]  K. Amunts,et al.  Posterior Parietal Cortex: Multimodal Association Cortex , 2012 .

[52]  K. Amunts,et al.  Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. , 2008, Cerebral cortex.

[53]  Katsuyuki Sakai,et al.  The prefrontal cortex and working memory: physiology and brain imaging , 2004, Current Opinion in Neurobiology.

[54]  Tim Shallice,et al.  The Fractionation of Supervisory Control , 2004 .

[55]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[56]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

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

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

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

[60]  A. Schleicher,et al.  Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. , 2008, Cerebral cortex.

[61]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[62]  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.

[63]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[64]  David E. Booth,et al.  Applied Multivariate Analysis , 2003, Technometrics.

[65]  Joshua W. Brown,et al.  Learned Predictions of Error Likelihood in the Anterior Cingulate Cortex , 2005, Science.

[66]  K. Zilles,et al.  Laminar distribution and co-distribution of neurotransmitter receptors in early human visual cortex , 2007, Brain Structure and Function.

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

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

[69]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

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

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

[72]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[73]  Angela R Laird,et al.  Brainmap taxonomy of experimental design: Description and evaluation , 2005, Human brain mapping.

[74]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[75]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[76]  S. Eickhoff,et al.  Approaches for the Integrated Analysis of Structure, Function and Connectivity of the Human Brain , 2011, Clinical EEG and neuroscience.

[77]  J. Jonides,et al.  Interference resolution: Insights from a meta-analysis of neuroimaging tasks , 2007, Cognitive, affective & behavioral neuroscience.

[78]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[79]  P. Roland,et al.  Bilateral activation of fronto-parietal networks by incrementing demand in a working memory task. , 1997, Cerebral cortex.

[80]  Timothy Edward John Behrens,et al.  Anatomical and Functional Connectivity of Cytoarchitectonic Areas within the Human Parietal Operculum , 2010, The Journal of Neuroscience.

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

[82]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[83]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[84]  Vinod Venkatraman,et al.  A Parallel Functional Topography between Medial and Lateral Prefrontal Cortex: Evidence and Implications for Cognitive Control , 2011, The Journal of Neuroscience.

[85]  M. Rushworth,et al.  Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks. , 2012, Cerebral cortex.

[86]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[87]  J. Gottlieb From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[88]  Katrin Amunts,et al.  The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability , 2006, NeuroImage.

[89]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[90]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[91]  Simon B. Eickhoff,et al.  Effects of timing and movement uncertainty implicate the temporo-parietal junction in the prediction of forthcoming motor actions , 2009, NeuroImage.

[92]  J. Fell,et al.  Memory formation by neuronal synchronization , 2006, Brain Research Reviews.

[93]  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.

[94]  Shuhei Yamaguchi,et al.  The Key Locus of Common Response Inhibition Network for No-go and Stop Signals , 2008, Journal of Cognitive Neuroscience.

[95]  Simon B Eickhoff,et al.  Dissociating bottom-up and top-down processes in a manual stimulus-response compatibility task. , 2010, Journal of neurophysiology.

[96]  P. Hancock,et al.  Cerebral lateralization of vigilance: A function of task difficulty , 2010, Neuropsychologia.

[97]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[98]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[99]  Keiji Tanaka,et al.  Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex , 2009, Nature Reviews Neuroscience.

[100]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[101]  Walle J. H. Nauta,et al.  Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey , 1976, Brain Research.