Practice-related effects demonstrate complementary roles of anterior cingulate and prefrontal cortices in attentional control

The purpose of this study was to test the hypothesis that the dorsolateral prefrontal cortex (DLFPC), not the anterior cingulate cortex (ACC), plays the predominant role in implementing top-down attentional control. To do so, we used fMRI to examine practice-related changes in neural activity during a variant of the Stroop task. The results indicated that the DLPFC's activity decreased gradually as the need for control was reduced (as indexed by behavioral measures), while the ACC's activity dropped off rapidly. Such a pattern is consistent with the DLPFC taking a leading role in implementing top-down attentional control and the ACC being involved in other aspects of attentional control, such as response-related processes. In addition, with practice, there was a reduction in activity within cortical systems handling the processing of task-irrelevant information capable of interfering with task performance. This finding suggests that with practice the brain is capable of identifying and strategically inhibiting such processing.

[1]  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.

[2]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[4]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[5]  N. Cohen,et al.  Prefrontal regions play a predominant role in imposing an attentional 'set': evidence from fMRI. , 2000, Brain research. Cognitive brain research.

[6]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[9]  Alex Martin,et al.  Cortical Regions Associated with Perceiving, Naming, and Knowing about Colors , 1999, Journal of Cognitive Neuroscience.

[10]  Guido Gerig,et al.  Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images , 1998, Medical Image Anal..

[11]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[12]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

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

[14]  Jonathan D. Cohen,et al.  Anterior Cingulate Cortex, Conflict Monitoring, and Levels of Processing , 2001, NeuroImage.

[15]  S. Kornblum,et al.  Isolation of Specific Interference Processing in the Stroop Task: PET Activation Studies , 1997, NeuroImage.

[16]  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.

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

[18]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[20]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[21]  Leslie G. Ungerleider,et al.  Selective attention to face identity and color studied with f MRI , 1997, Human brain mapping.

[22]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[23]  M. Posner,et al.  Executive attention: Conflict, target detection, and cognitive control. , 1998 .

[24]  C. Frith A framework for studying the neural basis of attention , 2001, Neuropsychologia.

[25]  P T Fox,et al.  A Highly Accurate Method of Localizing Regions of Neuronal Activation in the Human Brain with Positron Emission Tomography , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[26]  M. Posner,et al.  Localization of cognitive operations in the human brain. , 1988, Science.

[27]  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.

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

[29]  Christian Casanova,et al.  Vision : from neurons to cognition , 2001 .

[30]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.

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

[32]  R. Parasuraman The attentive brain , 1998 .

[33]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

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

[36]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[37]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[39]  Jonathan E. Jennings,et al.  An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. , 1999, Cerebral cortex.

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

[41]  A. Anderson,et al.  An fMRI study of stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems , 1999, Biological Psychiatry.