Dissociable neural systems resolve conflict from emotional versus nonemotional distracters.

The human brain protects the processing of task-relevant stimuli from interference ("conflict") by task-irrelevant stimuli via attentional biasing mechanisms. The lateral prefrontal cortex has been implicated in resolving conflict between competing stimuli by selectively enhancing task-relevant stimulus representations in sensory cortices. Conversely, recent data suggest that conflict from emotional distracters may be resolved by an alternative route, wherein the rostral anterior cingulate cortex inhibits amygdalar responsiveness to task-irrelevant emotional stimuli. Here we tested the proposal of 2 dissociable, distracter-specific conflict resolution mechanisms, by acquiring functional magnetic resonance imaging data during resolution of conflict from either nonemotional or emotional distracters. The results revealed 2 distinct circuits: a lateral prefrontal "cognitive control" system that resolved nonemotional conflict and was associated with enhanced processing of task-relevant stimuli in sensory cortices, and a rostral anterior cingulate "emotional control" system that resolved emotional conflict and was associated with decreased amygdalar responses to emotional distracters. By contrast, activations related to both emotional and nonemotional conflict monitoring were observed in a common region of the dorsal anterior cingulate. These data suggest that the neuroanatomical networks recruited to overcome conflict vary systematically with the nature of the conflict, but that they may share a common conflict-detection mechanism.

[1]  P. Ekman.  Pictures of Facial Affect , 1976 .

[2]  C. MacLeod,et al.  Selective processing of threat cues in anxiety states. , 1985, Behaviour research and therapy.

[3]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

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

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

[6]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

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

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

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

[10]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[11]  T. Dalgleish,et al.  The emotional Stroop task and psychopathology. , 1996, Psychological bulletin.

[12]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[13]  Joseph E LeDoux.  The emotional brain , 1996 .

[14]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[15]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

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

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

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

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

[21]  E. Stern,et al.  Linguistic threat activates the human amygdala. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

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

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

[27]  J. Eastwood,et al.  Differential attentional guidance by unattended faces expressing positive and negative emotion , 2001, Perception & psychophysics.

[28]  A. Ohman,et al.  Emotion drives attention: detecting the snake in the grass. , 2001, Journal of experimental psychology. General.

[29]  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.

[30]  Alastair M. Hull,et al.  Neuroimaging findings in post-traumatic stress disorder , 2002, British Journal of Psychiatry.

[31]  R. Davidson,et al.  Depression: perspectives from affective neuroscience. , 2002, Annual review of psychology.

[32]  Anthony A Grace,et al.  Cellular Mechanisms of Infralimbic and Prelimbic Prefrontal Cortical Inhibition and Dopaminergic Modulation of Basolateral Amygdala Neurons In Vivo , 2002, The Journal of Neuroscience.

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

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

[35]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[36]  D. Paré,et al.  Stimulation of Medial Prefrontal Cortex Decreases the Responsiveness of Central Amygdala Output Neurons , 2003, The Journal of Neuroscience.

[37]  E. Awh,et al.  Conflict adaptation effects in the absence of executive control , 2003, Nature Neuroscience.

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

[39]  B. Hommel,et al.  A feature-integration account of sequential effects in the Simon task , 2004, Psychological research.

[40]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

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

[42]  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.

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

[44]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[45]  Tobias Egner,et al.  The neural correlates and functional integration of cognitive control in a Stroop task , 2005, NeuroImage.

[46]  S. Rauch,et al.  A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. , 2005, Archives of general psychiatry.

[47]  Colin Camerer,et al.  Neural Systems Responding to Degrees of Uncertainty in Human Decision-Making , 2005, Science.

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

[49]  A. Lozano,et al.  Deep Brain Stimulation for Treatment-Resistant Depression , 2005, Neuron.

[50]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

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

[52]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[53]  Raymond J. Dolan,et al.  Neural Correlates of Self-distraction from Anxiety and a Process Model of Cognitive Emotion Regulation , 2006, Journal of Cognitive Neuroscience.

[54]  W. Notebaert,et al.  Top-down and bottom-up sequential modulations of congruency effects , 2006, Psychonomic bulletin & review.

[55]  Tobias Egner,et al.  Cerebral Cortex doi:10.1093/cercor/bhi129 Mistaking a House for a Face: Neural Correlates of Misperception in Healthy Humans , 2005 .

[56]  Marie T Banich,et al.  Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function. , 2007, Psychophysiology.

[57]  Tobias Egner,et al.  Separate conflict-specific cognitive control mechanisms in the human brain , 2007, NeuroImage.

[58]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

[59]  A. Etkin,et al.  Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. , 2007, The American journal of psychiatry.