Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function.

Functional differentiation of dorsal (dACC) and rostral (rACC) anterior cingulate cortex for cognitive and emotional function has received considerable indirect support. Using fMRI, parallel tasks, and within-subject analysis, the present study directly tested the proposed specialization of ACC subdivisions. A Task x Region interaction confirmed more dACC activation during color-word distractors and more rACC activation during emotion-word distractors. Activity in ACC subdivisions differentially predicted behavioral performance. Connectivity with prefrontal and limbic regions also supported distinct dACC and rACC roles. Findings provide direct evidence for differential engagement of ACC subdivisions in cognitive and emotional processing and for differential functional connectivity in the implementation of cognitive control and emotion regulation. Results point to an anatomical and functional continuum rather than segregated operations.

[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 Magnus Petersson,et al.  Context-dependent Deactivation of the Amygdala during Pain , 2004, Journal of Cognitive Neuroscience.

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

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

[5]  R. Simons,et al.  Error-related psychophysiology and negative affect , 2004, Brain and Cognition.

[6]  Anthony A Grace,et al.  Gating of information flow within the limbic system and the pathophysiology of schizophrenia , 2000, Brain Research Reviews.

[7]  Kim Kirsner,et al.  What Can we Infer from Double Dissociations? , 2003, Cortex.

[8]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[9]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[10]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[11]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[12]  Marie T. Banich,et al.  Neural Mechanisms of Cognitive Control: An Integrative Model of Stroop Task Performance and fMRI Data , 2006, Journal of Cognitive Neuroscience.

[13]  D. A. Medler,et al.  Functional localization and double dissociations: The relationship between internal structure and behavior , 2005, Brain and Cognition.

[14]  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.

[15]  Anna S. Engels,et al.  Specificity of regional brain activity in anxiety types during emotion processing , 2008, Brain and Cognition.

[16]  D. Algom,et al.  A rational look at the emotional stroop phenomenon: a generic slowdown, not a stroop effect. , 2004, Journal of experimental psychology. General.

[17]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[18]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[19]  G. A. Miller,et al.  Cognitive Deficits in Depression and Functional Specificity of Regional Brain Activity , 2007, Cognitive Therapy and Research.

[20]  Leanne M Williams,et al.  Amygdala–prefrontal dissociation of subliminal and supraliminal fear , 2006, Human brain mapping.

[21]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[22]  Andrew H. Kemp,et al.  Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems , 2005, NeuroImage.

[23]  Klaas Enno Stephan,et al.  On the role of general system theory for functional neuroimaging , 2004, Journal of anatomy.

[24]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

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

[26]  John M Hoffman,et al.  Ecstasy and Agony: Activation of the Human Amygdala in Positive and Negative Emotion , 2002, Psychological science.

[27]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[28]  K. Kiehl,et al.  Error processing and the rostral anterior cingulate: an event-related fMRI study. , 2000, Psychophysiology.

[29]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[30]  M. Petrides,et al.  Cortico-cortical connectivity of the human mid-dorsolateral frontal cortex and its modulation by repetitive transcranial magnetic stimulation: a combined TMS/PET study , 2000, NeuroImage.

[31]  G A Miller,et al.  How we think about cognition, emotion, and biology in psychopathology. , 1996, Psychophysiology.

[32]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

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

[34]  L. Pessoa To what extent are emotional visual stimuli processed without attention and awareness? , 2005, Current Opinion in Neurobiology.

[35]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[36]  Anna S. Engels,et al.  Specificity of regional brain activity in anxiety types during emotion processing. , 2007 .

[37]  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.

[38]  Erich O. Richter,et al.  Human Anterior Cingulate Cortex Neurons Encode Cognitive and Emotional Demands , 2005, The Journal of Neuroscience.

[39]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[40]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[41]  M. Raichle,et al.  Integration of emotion and cognition in the lateral prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[43]  M. Milham,et al.  Anterior cingulate cortex: An fMRI analysis of conflict specificity and functional differentiation , 2005, Human brain mapping.

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

[45]  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.

[46]  Marcus E. Raichle,et al.  Suppression of Regional Cerebral Blood during Emotional versus Higher Cognitive Implications for Interactions between Emotion and Cognition , 1998 .

[47]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[48]  T. Dalgleish Putting some feeling into it--the conceptual and empirical relationships between the classic and emotional Stroop tasks: comment on Algom, Chajut, and Lev (2004). , 2005, Journal of experimental psychology. General.

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

[50]  N. Frijda Emotions require cognitions, even if simple ones. , 1994 .

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

[52]  Wendy Heller,et al.  regional Brain Activity in Emotion: A Framework for Understanding Cognition in Depresion , 1997 .

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

[54]  Marie T Banich,et al.  Neural mechanisms of affective interference in schizotypy. , 2005, Journal of abnormal psychology.

[55]  G. A. Miller,et al.  Relationships of Distinct Affective Dimensions to Performance on an Emotional Stroop Task , 2003, Cognitive Therapy and Research.