The hierarchical organization of the lateral prefrontal cortex

Higher-level cognition depends on the lateral prefrontal cortex (LPFC), but its functional organization has remained elusive. An influential proposal is that the LPFC is organized hierarchically whereby progressively rostral areas of the LPFC process/represent increasingly abstract information facilitating efficient and flexible cognition. However, support for this theory has been limited. Here, human fMRI data revealed rostral/caudal gradients of abstraction in the LPFC. Dynamic causal modeling revealed asymmetrical LPFC interactions indicative of hierarchical processing. Contrary to dominant assumptions, the relative strength of efferent versus afferent connections positioned mid LPFC as the apex of the hierarchy. Furthermore, cognitive demands induced connectivity modulations towards mid LPFC consistent with a role in integrating information for control operations. Moreover, the strengths of these dynamics were related to trait-measured higher-level cognitive ability. Collectively, these results suggest that the LPFC is hierarchically organized with the mid LPFC positioned to synthesize abstract and concrete information to control behavior. DOI: http://dx.doi.org/10.7554/eLife.12112.001

[1]  Karl J. Friston,et al.  Large-scale neural models and dynamic causal modelling , 2006, NeuroImage.

[2]  R. Spinks The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe, 3rd ed. , 2000 .

[3]  Joshua W. Brown,et al.  Prefrontal cortex organization: dissociating effects of temporal abstraction, relational abstraction, and integration with FMRI. , 2014, Cerebral cortex.

[4]  T. Braver,et al.  Functional specializations in lateral prefrontal cortex associated with the integration and segregation of information in working memory. , 2006, Cerebral cortex.

[5]  A. Nobre,et al.  Top-down modulation: bridging selective attention and working memory , 2012, Trends in Cognitive Sciences.

[6]  Lizabeth M Romanski,et al.  Domain specificity in the primate prefrontal cortex , 2004, Cognitive, affective & behavioral neuroscience.

[7]  Mark D'Esposito,et al.  Influence of Motivation on Control Hierarchy in the Human Frontal Cortex , 2015, The Journal of Neuroscience.

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

[9]  Richard Levy,et al.  Testing the model of caudo-rostral organization of cognitive control in the human with frontal lesions , 2014, NeuroImage.

[10]  Etienne Koechlin,et al.  Divided Representation of Concurrent Goals in the Human Frontal Lobes , 2010, Science.

[11]  Mark D'Esposito,et al.  Focal Brain Lesions to Critical Locations Cause Widespread Disruption of the Modular Organization of the Brain , 2012, Journal of Cognitive Neuroscience.

[12]  Michael W. Cole,et al.  Global Connectivity of Prefrontal Cortex Predicts Cognitive Control and Intelligence , 2012, The Journal of Neuroscience.

[13]  David Badre,et al.  Functional Magnetic Resonance Imaging Evidence for a Hierarchical Organization of the Prefrontal Cortex , 2007, Journal of Cognitive Neuroscience.

[14]  Andrew R. Mitz,et al.  Prefrontal Cortex Activity Related to Abstract Response Strategies , 2005, Neuron.

[15]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[16]  John R. Anderson,et al.  The role of prefrontal cortex and posterior parietal cortex in task switching. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Egill Rostrup,et al.  Motion or activity: their role in intra- and inter-subject variation in fMRI , 2005, NeuroImage.

[18]  Karl J. Friston,et al.  Tractography-based priors for dynamic causal models , 2009, NeuroImage.

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

[20]  Peter Stiers,et al.  Mapping the hierarchical layout of the structural network of the macaque prefrontal cortex. , 2014, Cerebral cortex.

[21]  J. Fuster Anatomy of the Prefrontal Cortex , 2008 .

[22]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[23]  G. F. Tremblay,et al.  The Prefrontal Cortex , 1989, Neurology.

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

[25]  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.

[26]  F. Plum Handbook of Physiology. , 1960 .

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

[28]  Ari Weinstein,et al.  Model-based hierarchical reinforcement learning and human action control , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[30]  Joshua W. Brown,et al.  A meta-analysis of executive components of working memory. , 2013, Cerebral cortex.

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

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

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

[34]  Joshua W. Brown,et al.  Dissociable frontal-striatal and frontal-parietal networks involved in updating hierarchical contexts in working memory. , 2013, Cerebral cortex.

[35]  Alec Solway,et al.  Optimal Behavioral Hierarchy , 2014, PLoS Comput. Biol..

[36]  H. Spinnler The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[37]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

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

[39]  C. Segebarth,et al.  Identifying Neural Drivers with Functional MRI: An Electrophysiological Validation , 2008, PLoS biology.

[40]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[41]  E. Koechlin,et al.  Broca's Area and the Hierarchical Organization of Human Behavior , 2006, Neuron.

[42]  M. Brass,et al.  Neural Circuitry Underlying Rule Use in Humans and Nonhuman Primates , 2005, The Journal of Neuroscience.

[43]  B. Postle,et al.  The cognitive neuroscience of working memory. , 2007, Annual review of psychology.

[44]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[46]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

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

[49]  P. Goldman-Rakic Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory , 2011 .

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

[51]  Jonathan D. Cohen,et al.  The Function and Organization of Lateral Prefrontal Cortex: A Test of Competing Hypotheses , 2012, PloS one.

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

[53]  F. Lhermitte,et al.  Human autonomy and the frontal lobes. Part II: Patient behavior in complex and social situations: The “environmental dependency syndrome” , 1986, Annals of neurology.

[54]  T. Braver,et al.  Integration in Working Memory: A Magnetic Stimulation Study on the Role of Left Anterior Prefrontal Cortex , 2012, PloS one.

[55]  J. Ashburner,et al.  Multimodal Image Coregistration and Partitioning—A Unified Framework , 1997, NeuroImage.

[56]  Mark D'Esposito,et al.  The Rostro-Caudal Axis of Frontal Cortex Is Sensitive to the Domain of Stimulus Information. , 2015, Cerebral cortex.

[57]  Alfred Anwander,et al.  Functional Network Mirrored in the Prefrontal Cortex, Caudate Nucleus, and Thalamus: High-Resolution Functional Imaging and Structural Connectivity , 2014, The Journal of Neuroscience.

[58]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

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

[60]  G. D. Logan Task Switching , 2022 .

[61]  R. Engle,et al.  Is working memory capacity task dependent , 1989 .

[62]  Joshua W. Brown,et al.  Rostral–caudal gradients of abstraction revealed by multi-variate pattern analysis of working memory , 2012, NeuroImage.

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

[64]  Angela D Friederici,et al.  Two principles of organization in the prefrontal cortex are cognitive hierarchy and degree of automaticity , 2013, Nature Communications.

[65]  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.

[66]  J. Fuster Frontal lobes , 1993, Current Opinion in Neurobiology.

[67]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

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

[69]  Jeffrey W. Cooney,et al.  Hierarchical cognitive control deficits following damage to the human frontal lobe , 2009, Nature Neuroscience.

[70]  J. Fuster Prefrontal Cortex , 2018 .