Parsing the Roles of the Frontal Lobes and Basal Ganglia in Task Control Using Multivoxel Pattern Analysis

Cognitive control has traditionally been associated with pFC based on observations of deficits in patients with frontal lesions. However, evidence from patients with Parkinson disease indicates that subcortical regions also contribute to control under certain conditions. We scanned 17 healthy volunteers while they performed a task-switching paradigm that previously dissociated performance deficits arising from frontal lesions in comparison with Parkinson disease, as a function of the abstraction of the rules that are switched. From a multivoxel pattern analysis by Gaussian Process Classification, we then estimated the forward (generative) model to infer regional patterns of activity that predict Switch/Repeat behavior between rule conditions. At 1000 permutations, Switch/Repeat classification accuracy for concrete rules was significant in the BG, but at chance in the frontal lobe. The inverse pattern was obtained for abstract rules, whereby the conditions were successfully discriminated in the frontal lobe but not in the BG. This double dissociation highlights the difference between cortical and subcortical contributions to cognitive control and demonstrates the utility of multivariate approaches in investigations of functions that rely on distributed and overlapping neural substrates.

[1]  D Y von Cramon,et al.  Executive control functions in task switching: evidence from brain injured patients. , 1999, Journal of clinical and experimental neuropsychology.

[2]  John-Dylan Haynes,et al.  Distributed Representations of Rule Identity and Rule Order in Human Frontal Cortex and Striatum , 2012, The Journal of Neuroscience.

[3]  Lawrence H Snyder,et al.  Single Neurons in Posterior Parietal Cortex of Monkeys Encode Cognitive Set , 2004, Neuron.

[4]  Angie A. Kehagia,et al.  Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation , 2010, Current Opinion in Neurobiology.

[5]  M. Schmitter-Edgecombe,et al.  Costs of a predictable switch between simple cognitive tasks following severe closed-head injury. , 2006, Neuropsychology.

[6]  B. Gold,et al.  Common and Distinct Mechanisms of Cognitive Flexibility in Prefrontal Cortex , 2011, The Journal of Neuroscience.

[7]  T. Robbins,et al.  Dissociating executive mechanisms of task control following frontal lobe damage and Parkinson's disease. , 1998, Brain : a journal of neurology.

[8]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[9]  Richard N. Henson,et al.  CHAPTER 15 – Efficient Experimental Design for fMRI , 2007 .

[10]  Sten Grillner,et al.  Evolution of the basal ganglia: Dual‐output pathways conserved throughout vertebrate phylogeny , 2012, The Journal of comparative neurology.

[11]  Jonathan D. Cohen,et al.  Between-Task Competition and Cognitive Control in Task Switching , 2006, The Journal of Neuroscience.

[12]  Mariya V. Cherkasova,et al.  Schizophrenic subjects show deficient inhibition but intact task switching on saccadic tasks , 2002, Biological Psychiatry.

[13]  Carl E. Rasmussen,et al.  Gaussian processes for machine learning , 2005, Adaptive computation and machine learning.

[14]  Roshan Cools,et al.  Switching between abstract rules reflects disease severity but not dopaminergic status in Parkinson's disease , 2009, Neuropsychologia.

[15]  M. Brass,et al.  Decomposing Components of Task Preparation with Functional Magnetic Resonance Imaging , 2004, Journal of Cognitive Neuroscience.

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

[17]  M. Brass,et al.  Advance preparation and stimulus-induced interference in cued task switching: further insights from BOLD fMRI , 2005, Neuropsychologia.

[18]  J. R. Simon,et al.  Reactions toward the source of stimulation. , 1969, Journal of experimental psychology.

[19]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[20]  R. Passingham,et al.  Anatomical differences between the neocortex of man and other primates. , 1973, Brain, behavior and evolution.

[21]  Cameron S Carter,et al.  Cognitive control involved in overcoming prepotent response tendencies and switching between tasks. , 2005, Cerebral cortex.

[22]  Jörn Diedrichsen,et al.  Dissociating Task-set Selection from Task-set Inhibition in the Prefrontal Cortex , 2006, Journal of Cognitive Neuroscience.

[23]  F. Karayanidis,et al.  Switching between univalent task-sets in schizophrenia: ERP evidence of an anticipatory task-set reconfiguration deficit , 2006, Clinical Neurophysiology.

[24]  Trevor W. Robbins Functioning of frontostriatal anatomical "loops" in mechanisms of cognitive control , 2000 .

[25]  Trevor Hastie,et al.  The Elements of Statistical Learning , 2001 .

[26]  Steffen Moritz,et al.  Task Switching and Backward Inhibition in Obsessive-Compulsive Disorder , 2004, Journal of clinical and experimental neuropsychology.

[27]  D. C. Howell Statistical methods for psychology, 3rd ed. , 1992 .

[28]  G. Mangun,et al.  Brain regions activated by endogenous preparatory set shifting as revealed by fMRI , 2006, Cognitive, affective & behavioral neuroscience.

[29]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[30]  Louis Wehenkel,et al.  Decoding Semi-Constrained Brain Activity from fMRI Using Support Vector Machines and Gaussian Processes , 2012, PloS one.

[31]  Richard B. Ivry,et al.  The Human Striatum is Necessary for Responding to Changes in Stimulus Relevance , 2006, Journal of Cognitive Neuroscience.

[32]  Stefan Haufe,et al.  On the interpretation of weight vectors of linear models in multivariate neuroimaging , 2014, NeuroImage.

[33]  Martin A. Lindquist,et al.  Detection of time-varying signals in event-related fMRI designs , 2008, NeuroImage.

[34]  Christian C. Ruff,et al.  Short- and long-term changes in anterior cingulate activation during resolution of task-set competition , 2006, Brain Research.

[35]  M. Frank,et al.  Mechanisms of hierarchical reinforcement learning in corticostriatal circuits 1: computational analysis. , 2012, Cerebral cortex.

[36]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[37]  Thomas R. Knösche,et al.  Who Comes First? The Role of the Prefrontal and Parietal Cortex in Cognitive Control , 2005, Journal of Cognitive Neuroscience.

[38]  David Badre,et al.  Computational and neurobiological mechanisms underlying cognitive flexibility. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Darryl W. Schneider,et al.  Modeling task switching without switching tasks: a short-term priming account of explicitly cued performance. , 2005, Journal of experimental psychology. General.

[40]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[41]  T. Robbins,et al.  l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease , 2003, Neuropsychologia.

[42]  Angie A. Kehagia,et al.  Revisiting the effects of Parkinson's disease and frontal lobe lesions on task switching: the role of rule reconfiguration. , 2014, Journal of neuropsychology.

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

[44]  S. Yantis,et al.  A Domain-Independent Source of Cognitive Control for Task Sets: Shifting Spatial Attention and Switching Categorization Rules , 2009, The Journal of Neuroscience.

[45]  J. Haynes A Primer on Pattern-Based Approaches to fMRI: Principles, Pitfalls, and Perspectives , 2015, Neuron.

[46]  Anne G E Collins,et al.  Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. , 2014, Psychological review.

[47]  Thomas E. Hazy,et al.  Banishing the homunculus: Making working memory work , 2006, Neuroscience.

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

[49]  B. Gold,et al.  Domain general and domain preferential brain regions associated with different types of task switching: A Meta‐Analysis , 2012, Human brain mapping.

[50]  T. Robbins,et al.  Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. , 2001, Cerebral cortex.

[51]  Stephen Monsell,et al.  Task-Set Switching Deficits in Early-Stage Huntington's Disease: Implications for Basal Ganglia Function , 2003, Journal of Cognitive Neuroscience.

[52]  Matthew F. S. Rushworth,et al.  Components of Switching Intentional Set , 2002, Journal of Cognitive Neuroscience.

[53]  D. Stuss,et al.  The Frontal Lobes , 1986 .

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

[55]  S. Channon,et al.  Tourette's syndrome (TS): cognitive performance in adults with uncomplicated TS. , 2006, Neuropsychology.

[56]  J. Duncan,et al.  Adaptive Coding of Task-Relevant Information in Human Frontoparietal Cortex , 2011, The Journal of Neuroscience.

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

[58]  K. A. Hadland,et al.  Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. , 2002, Journal of neurophysiology.

[59]  Jonathan D. Wallis,et al.  A Comparison of Abstract Rules in the Prefrontal Cortex, Premotor Cortex, Inferior Temporal Cortex, and Striatum , 2006, Journal of Cognitive Neuroscience.

[60]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

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

[62]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[63]  E. Crone,et al.  Neural evidence for dissociable components of task-switching. , 2006, Cerebral cortex.

[64]  T. Robbins,et al.  A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. , 2004, Brain : a journal of neurology.

[65]  T. Robbins,et al.  Differential Responses in Human Striatum and Prefrontal Cortex to Changes in Object and Rule Relevance , 2004, The Journal of Neuroscience.

[66]  Arthur L. Benton,et al.  Differential behavioral effects in frontal lobe disease , 1968 .

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

[68]  E. Robinson Cybernetics, or Control and Communication in the Animal and the Machine , 1963 .

[69]  R. Reitan,et al.  A selective and critical review of neuropsychological deficits and the frontal lobes , 1994, Neuropsychology Review.

[70]  John-Dylan Haynes,et al.  Compositionality of rule representations in human prefrontal cortex. , 2012, Cerebral cortex.