The neural mechanisms of semantic and response conflicts: An fMRI study of practice-related effects in the Stroop task

Previous studies have demonstrated that there are separate neural mechanisms underlying semantic and response conflicts in the Stroop task. However, the practice effects of these conflicts need to be elucidated and the possible involvements of common neural mechanisms are yet to be established. We employed functional magnetic resonance imaging (fMRI) in a 4-2 mapping practice-related Stroop task to determine the neural substrates under these conflicts. Results showed that different patterns of brain activations are associated with practice in the attentional networks (e.g., dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex (ACC), and posterior parietal cortex (PPC)) for both conflicts, response control regions (e.g., inferior frontal junction (IFJ), inferior frontal gyrus (IFG)/insula, and pre-supplementary motor areas (pre-SMA)) for semantic conflict, and posterior cortex for response conflict. We also found areas of common activation in the left hemisphere within the attentional networks, for the early practice stage in semantic conflict and the late stage in "pure" response conflict using conjunction analysis. The different practice effects indicate that there are distinct mechanisms underlying these two conflict types: semantic conflict practice effects are attributable to the automation of stimulus processing, conflict and response control; response conflict practice effects are attributable to the proportional increase of conflict-related cognitive resources. In addition, the areas of common activation suggest that the semantic conflict effect may contain a partial response conflict effect, particularly at the beginning of the task. These findings indicate that there are two kinds of response conflicts contained in the key-pressing Stroop task: the vocal-level (mainly in the early stage) and key-pressing (mainly in the late stage) response conflicts; thus, the use of the subtraction method for the exploration of semantic and response conflicts may need to be further examined.

[1]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[2]  Jelena Jovanovic,et al.  Anterior cingulate cortex and the Stroop task: neuropsychological evidence for topographic specificity , 2002, Neuropsychologia.

[3]  R. Andersen,et al.  Target Selection Signals for Arm Reaching in the Posterior Parietal Cortex , 2007, The Journal of Neuroscience.

[4]  Jin Fan,et al.  Effective Connectivity of the Fronto-parietal Network during Attentional Control , 2010, Journal of Cognitive Neuroscience.

[5]  Andrew Webb,et al.  Behavioral conflict, anterior cingulate cortex, and experiment duration: Implications of diverging data , 2004, Human brain mapping.

[6]  A. Aron The Neural Basis of Inhibition in Cognitive Control , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[7]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[8]  Jeounghoon Kim,et al.  Multiple cognitive control mechanisms associated with the nature of conflict , 2010, Neuroscience Letters.

[9]  John Jonides,et al.  How does practice makes perfect? , 2004, Nature Neuroscience.

[10]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[11]  R. Marois,et al.  Visual Short-Term Memory Load Suppresses Temporo-Parietal Junction Activity and Induces Inattentional Blindness , 2005, Psychological science.

[12]  Colin M. Macleod,et al.  Training and Stroop-like interference: evidence for a continuum of automaticity. , 1988, Journal of experimental psychology. Learning, memory, and cognition.

[13]  R. Cox,et al.  Event‐related fMRI contrast when using constant interstimulus interval: Theory and experiment , 2000, Magnetic resonance in medicine.

[14]  Xun Liu,et al.  Common and distinct neural substrates of attentional control in an integrated Simon and spatial Stroop task as assessed by event-related fMRI , 2004, NeuroImage.

[15]  E. Donchin,et al.  Optimizing the use of information: strategic control of activation of responses. , 1992, Journal of experimental psychology. General.

[16]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

[17]  M. P Milham,et al.  Practice-related effects demonstrate complementary roles of anterior cingulate and prefrontal cortices in attentional control , 2003, NeuroImage.

[18]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[19]  Eric H. Schumacher,et al.  Sustained involvement of a frontal–parietal network for spatial response selection with practice of a spatial choice–reaction task , 2005, Neuropsychologia.

[20]  Bruce D. McCandliss,et al.  Testing the Efficiency and Independence of Attentional Networks , 2002, Journal of Cognitive Neuroscience.

[21]  G. M. Redding,et al.  Stroop Effect: Interference and Facilitation with Verbal and Manual Responses , 1977, Perceptual and motor skills.

[22]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

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

[24]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[25]  Hidenao Fukuyama,et al.  Task-irrelevant memory load induces inattentional blindness without temporo-parietal suppression , 2010, Neuropsychologia.

[26]  C. Büchel,et al.  Functional Dissociation of Hippocampal Mechanism during Implicit Learning Based on the Domain of Associations , 2011, The Journal of Neuroscience.

[27]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[28]  C. Porcaro,et al.  Multimodal Functional Network Connectivity: An EEG-fMRI Fusion in Network Space , 2011, PloS one.

[29]  R. West,et al.  Sensitivity of medial frontal cortex to response and nonresponse conflict. , 2004, Psychophysiology.

[30]  J. Buhle,et al.  Typologies of attentional networks , 2006, Nature Reviews Neuroscience.

[31]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[32]  W. Rogers,et al.  Mechanisms underlying reduction in Stroop interference with practice for young and old adults. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

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

[34]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[35]  J. Lancaster,et al.  Using the talairach atlas with the MNI template , 2001, NeuroImage.

[36]  Mike Wendt,et al.  Disentangling Sequential Effects of Stimulus- and Response-related Conflict and Stimulus-Response Repetition using Brain Potentials , 2007, Journal of Cognitive Neuroscience.

[37]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[38]  Benjamin O. Turner,et al.  Cortical and basal ganglia contributions to habit learning and automaticity , 2010, Trends in Cognitive Sciences.

[39]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[40]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[41]  A. Aron From Reactive to Proactive and Selective Control: Developing a Richer Model for Stopping Inappropriate Responses , 2011, Biological Psychiatry.

[42]  Gary H. Glover,et al.  A Developmental fMRI Study of the Stroop Color-Word Task , 2002, NeuroImage.

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

[44]  Jan De Houwer,et al.  On the role of stimulus-response and stimulus-stimulus compatibility in the Stroop effect , 2003 .

[45]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[46]  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.

[47]  N. Cohen,et al.  The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. , 2001, Brain research. Cognitive brain research.

[48]  M. Banich,et al.  Functional dissociation of attentional selection within PFC: response and non-response related aspects of attentional selection as ascertained by fMRI. , 2006, Cerebral cortex.

[49]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[50]  Jeounghoon Kim,et al.  Conflict adjustment through domain-specific multiple cognitive control mechanisms , 2012, Brain Research.

[51]  G. Repovš The mode of response and the Stroop effect: A reaction time analysis , 2004 .

[52]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[53]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[54]  Deanna M. Barch,et al.  Improving Prefrontal Cortex Function in Schizophrenia Through Focused Training of Cognitive Control , 2009, Front. Hum. Neurosci..

[55]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[56]  N. Cohen,et al.  Attentional Control in the Aging Brain: Insights from an fMRI Study of the Stroop Task , 2002, Brain and Cognition.

[57]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

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

[60]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[61]  James L. McClelland,et al.  On the control of automatic processes: a parallel distributed processing account of the Stroop effect. , 1990, Psychological review.

[62]  Arthur F. Kramer,et al.  fMRI Studies of Stroop Tasks Reveal Unique Roles of Anterior and Posterior Brain Systems in Attentional Selection , 2000, Journal of Cognitive Neuroscience.

[63]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

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

[65]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[66]  J. Stroop Studies of interference in serial verbal reactions. , 1992 .

[67]  J. de Houwer On the role of stimulus-response and stimulus-stimulus compatibility in the Stroop effect. , 2003, Memory & cognition.

[68]  J R Simon,et al.  Processing auditory information: interference from an irrelevant cue. , 1969, The Journal of applied psychology.

[69]  I. THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[70]  Hakwan C. Lau,et al.  Dissociating response selection and conflict in the medial frontal surface , 2006, NeuroImage.

[71]  Cameron S. Carter,et al.  Separating semantic conflict and response conflict in the Stroop task: A functional MRI study , 2005, NeuroImage.

[72]  Edward E. Smith,et al.  Attention Enhances the Neural Processing of Relevant Features and Suppresses the Processing of Irrelevant Features in Humans: A Functional Magnetic Resonance Imaging Study of the Stroop Task , 2008, The Journal of Neuroscience.

[73]  Colin M. Macleod Training on integrated versus separated Stroop tasks: The progression of interference and facilitation , 1998, Memory & cognition.

[74]  E. Miller,et al.  THE PREFRONTAL CORTEX AND COGNITIVE CONTROL , 2000 .

[75]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

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

[77]  Cameron S Carter,et al.  Cognitive Control Deficits in Schizophrenia: Mechanisms and Meaning , 2011, Neuropsychopharmacology.

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

[79]  Carrick C. Williams,et al.  Stroop Interference, Practice, and Aging , 2003, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[80]  M. Husain,et al.  Control over Conflict during Movement Preparation: Role of Posterior Parietal Cortex , 2008, Neuron.

[81]  Dezhong Yao,et al.  fMRI functional networks for EEG source imaging , 2011, Human brain mapping.

[82]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.