Brain Systems Mediating Cognitive Interference by Emotional Distraction

Flexible behavior depends on our ability to cope with distracting stimuli that can interfere with the attainment of goals. Emotional distracters can be particularly disruptive to goal-oriented behavior, but the neural systems through which these detrimental effects are mediated are not known. We used event-related functional magnetic resonance imaging to investigate the effect of emotional and nonemotional distracters on a delayed-response working memory (WM) task. As expected, this task evoked robust activity during the delay period in typical WM regions (dorsolateral prefrontal cortex and lateral parietal cortex). Presentation of emotional distracters during the delay interval evoked strong activity in typical emotional processing regions (amygdala and ventrolateral prefrontal cortex) while simultaneously evoking relative deactivation of the WM regions and impairing WM performance. These results provide the first direct evidence that the detrimental effect of emotional distracters on ongoing cognitive processes entails the interaction between a dorsal neural system associated with “cold” executive processing and a ventral system associated with “hot” emotional processing.

[1]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[2]  A. MacLeod,et al.  Associations between phenomenal and objective aspects of concentration problems in depressed patients. , 1988, British journal of psychology.

[3]  K. Fiedler,et al.  Affect Cognition and Social Behavior: New Evidence and Integrative Attempts , 1991 .

[4]  H. Ellis,et al.  Irrelevant thoughts, emotional mood states, and cognitive task performance , 1991, Memory & cognition.

[5]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Karl J. Friston,et al.  Dorsolateral prefrontal cortex dysfunction in the major psychoses; symptom or disease specificity? , 1993, Journal of neurology, neurosurgery, and psychiatry.

[7]  M. Bradley,et al.  Looking at pictures: affective, facial, visceral, and behavioral reactions. , 1993, Psychophysiology.

[8]  Sven-Åke Christianson,et al.  The Handbook of Emotion and Memory : Research and Theory , 1994 .

[9]  R. Davidson.  Cerebral asymmetry, emotion, and affective style. , 1995 .

[10]  R G Robinson,et al.  Lesion location and poststroke depression. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[11]  M. Oaksford,et al.  Mood, reasoning, and central executive processes. , 1996 .

[12]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[13]  H. Mayberg.  Limbic-cortical dysregulation: a proposed model of depression. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[14]  J. Fuster.  Network memory , 1997, Trends in Neurosciences.

[15]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[16]  L. Obler,et al.  Right hemisphere emotional perception: evidence across multiple channels. , 1998, Neuropsychology.

[17]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[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]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[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]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[22]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[23]  Arthur P. Shimamura,et al.  The role of the prefrontal cortex in dynamic filtering , 2000, Psychobiology.

[24]  Leslie G. Ungerleider,et al.  Complementary neural mechanisms for tracking items in human working memory. , 2000, Science.

[25]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[26]  Steven G. Potkin,et al.  Sex-Related Difference in Amygdala Activity during Emotionally Influenced Memory Storage , 2001, Neurobiology of Learning and Memory.

[27]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[28]  Thomas Elbert,et al.  Dissociation in human prefrontal cortex of affective influences on working memory-related activity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  P. Petrovic,et al.  Placebo and Opioid Analgesia-- Imaging a Shared Neuronal Network , 2002, Science.

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

[31]  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.

[32]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[34]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[35]  Amishi P. Jha,et al.  The role of prefrontal cortex in resolving distractor interference , 2004, Cognitive, affective & behavioral neuroscience.

[36]  E. Phelps.  Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

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

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

[39]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[40]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

[41]  Tali Sharot,et al.  How emotion enhances the feeling of remembering , 2004, Nature Neuroscience.

[42]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Teasell,et al.  Lesion Location and Poststroke Depression: Systematic Review of the Methodological Limitations in the Literature , 2004, Stroke.

[44]  Florin Dolcos,et al.  Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: an event-related fMRI study , 2004, NeuroImage.

[45]  J. D. McGaugh.  The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[46]  Robert T. Knight,et al.  Behavioral and Electrophysiological Evidence of a Right Hemisphere Bias for the Influence of Negative Emotion on Higher Cognition , 2005, Journal of Cognitive Neuroscience.

[47]  R. Cabeza,et al.  Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Miclea,et al.  Emotion-induced retrograde amnesia and trait anxiety. , 2005, Journal of Experimental Psychology. Learning, Memory and Cognition.

[49]  G. McCarthy,et al.  Amygdala activation to sad pictures during high-field (4 tesla) functional magnetic resonance imaging. , 2005, Emotion.

[50]  Marvin M. Chun,et al.  Attentional rubbernecking: Cognitive control and personality in emotion-induced blindness , 2005, Psychonomic bulletin & review.

[51]  Clayton E. Curtis,et al.  Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex , 2006, NeuroImage.

[52]  Mara Mather,et al.  Emotional Arousal Can Impair Feature Binding in Working Memory , 2006, Journal of Cognitive Neuroscience.

[53]  R. Cabeza,et al.  The Memory Enhancing Effect of Emotion: Functional Neuroimaging Evidence , 2008 .

[54]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[55]  B. Uttl,et al.  Memory and Emotion from Interdisciplinary Perspectives , 2008 .