Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control

A network of prefrontal and parietal regions has been implicated in executive control processes. However, the extent to which individual regions within this network are engaged in component control processes, such as inhibition of task-irrelevant stimulus attributes or shifting (switching) between attentional foci, remains controversial. Participants (N=17) underwent functional magnetic resonance imaging while performing a global-local task in which the global and local levels could facilitate or interfere with one another. Stimuli were presented in blocks in which participants either constantly shifted between the global and local levels, or consistently responded to one level only. Activations related to inhibition and shifting processes were observed in a large network of bilateral prefrontal, parietal, and basal ganglia regions. Region of interest analyses were used to classify each region within this network as being common to inhibition and shifting, or preferential to one component process. Several regions were classified as being preferential to inhibition, including regions within the dorsolateral and ventrolateral prefrontal cortex, the parietal lobes, and the temporal-parietal junction. A limited set of regions in the parietal lobes and left dorsolateral prefrontal cortex were classified as preferential to shifting. There was a very large set of regions displaying activation common to both inhibition and shifting processes, including regions within the dorsolateral prefrontal cortex, anterior cingulate, and basal ganglia. Several of these common regions were also involved during facilitation, suggesting that they are responsive to the number of task-salient channels of information, rather than purely to demands on control processes.

[1]  Leslie G. Ungerleider,et al.  The prefrontal cortex and the executive control of attention , 2008, Experimental Brain Research.

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

[3]  T. Robbins,et al.  Chemistry of the adaptive mind , 2004, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

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

[5]  D. Navon Forest before trees: The precedence of global features in visual perception , 1977, Cognitive Psychology.

[6]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[7]  Jonathan D. Cohen,et al.  Interference and Facilitation Effects during Selective Attention: An H2 15O PET Study of Stroop Task Performance , 1995, NeuroImage.

[8]  M. Brass,et al.  Voluntary Selection of Task Sets Revealed by Functional Magnetic Resonance Imaging , 2006 .

[9]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

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

[11]  Andrew B. Leber,et al.  Neural predictors of moment-to-moment fluctuations in cognitive flexibility , 2008, Proceedings of the National Academy of Sciences.

[12]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

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

[14]  Thomas E. Nichols,et al.  Toward a taxonomy of attention shifting: Individual differences in fMRI during multiple shift types , 2005, Cognitive, affective & behavioral neuroscience.

[15]  D. Linden,et al.  Processing conflicting information: Facilitation, interference, and functional connectivity , 2008, Neuropsychologia.

[16]  M. Petrides,et al.  Neural Bases of Set-Shifting Deficits in Parkinson's Disease , 2004, The Journal of Neuroscience.

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

[18]  Thomas E. Nichols,et al.  Switching attention and resolving interference: fMRI measures of executive functions , 2003, Neuropsychologia.

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

[20]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[22]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Robert Rogers,et al.  Top–Down Attentional Control in Parkinson's Disease: Salient Considerations , 2010, Journal of Cognitive Neuroscience.

[24]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[25]  M. Brass,et al.  Involvement of the inferior frontal junction in cognitive control: Meta‐analyses of switching and Stroop studies , 2005, Human brain mapping.

[26]  F. Collette,et al.  Brain imaging of the central executive component of working memory , 2002, Neuroscience & Biobehavioral Reviews.

[27]  Trey Hedden,et al.  Individual differences in executive processing predict susceptibility to interference in verbal working memory. , 2006, Neuropsychology.

[28]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[29]  Stefan Bode,et al.  Decoding sequential stages of task preparation in the human brain , 2009, NeuroImage.

[30]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[31]  Jonas Persson,et al.  Mapping interference resolution across task domains: A shared control process in left inferior frontal gyrus , 2009, Brain Research.

[32]  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.

[33]  Marcel Brass,et al.  Selection for Cognitive Control: A Functional Magnetic Resonance Imaging Study on the Selection of Task-Relevant Information , 2004, The Journal of Neuroscience.

[34]  T. Robbins Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[35]  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.

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

[37]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[38]  Leslie G. Ungerleider,et al.  Attentional control during the transient updating of cue information , 2009, Brain Research.

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

[40]  Jan Derrfuss,et al.  Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory , 2004, NeuroImage.

[41]  O. Monchi,et al.  Dopamine Depletion Impairs Frontostriatal Functional Connectivity during a Set-Shifting Task , 2008, The Journal of Neuroscience.

[42]  Susan M. Ravizza,et al.  Shifting set about task switching: Behavioral and neural evidence for distinct forms of cognitive flexibility , 2008, Neuropsychologia.

[43]  M. Banich Executive Function , 2009 .

[44]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[45]  T. Salthouse,et al.  Executive functioning as a potential mediator of age-related cognitive decline in normal adults. , 2003, Journal of experimental psychology. General.

[46]  K. Berman,et al.  Fractionating the neural substrate of cognitive control processes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[48]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[49]  M. Milham,et al.  Competition for priority in processing increases prefrontal cortex's involvement in top-down control: an event-related fMRI study of the stroop task. , 2003, Brain research. Cognitive brain research.

[50]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[51]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[52]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

[53]  A. Miyake,et al.  The relations among inhibition and interference control functions: a latent-variable analysis. , 2004, Journal of experimental psychology. General.

[54]  D. H Weissman,et al.  Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features , 2003, NeuroImage.

[55]  Robert T. Knight,et al.  Effects of frontal lobe damage on interference effects in working memory , 2002, Cognitive, affective & behavioral neuroscience.

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

[57]  M. Petrides,et al.  Cortical activity in Parkinson's disease during executive processing depends on striatal involvement. , 2006, Brain : a journal of neurology.

[58]  Steven Laureys,et al.  Exploring the unity and diversity of the neural substrates of executive functioning , 2005, Human brain mapping.

[59]  Birte U. Forstmann,et al.  Neural Mechanisms, Temporal Dynamics, and Individual Differences in Interference Control , 2008, Journal of Cognitive Neuroscience.