Early detection and late cognitive control of emotional distraction by the prefrontal cortex

Unpleasant emotional distraction can impair the retention of non-emotional information in working memory (WM). Research links the prefrontal cortex with the successful control of such biologically relevant distractors, although the temporal changes in this brain mechanism remain unexplored. We use magnetoencephalography to investigate the temporal dynamics of the cognitive control of both unpleasant and pleasant distraction, in the millisecond (ms) scale. Behavioral results demonstrate that pleasant events do not affect WM maintenance more than neutral ones. Neuroimaging results show that prefrontal cortices are recruited for the rapid detection of emotional distraction, at early latencies of the processing (70-130 ms). Later in the processing (360-450 ms), the dorsolateral, the medial and the orbital sections of the prefrontal cortex mediate the effective control of emotional distraction. In accordance with the behavioral performance, pleasant distractors do not require higher prefrontal activity than neutral ones. These findings extend our knowledge about the brain mechanisms of coping with emotional distraction in WM. In particular, they show for the first time that overriding the attentional capture triggered by emotional distractors, while maintaining task-relevant elements in mind, is based on the early detection of such linked-to-survival information and on its later cognitive control by the prefrontal cortex.

[1]  S. Thorpe,et al.  The orbitofrontal cortex: Neuronal activity in the behaving monkey , 2004, Experimental Brain Research.

[2]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[3]  A. Hamm,et al.  Emotional memories are resilient to time: Evidence from the parietal ERP old/new effect , 2011, Human brain mapping.

[4]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[5]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[6]  K. Ochsner,et al.  Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. , 2000, Journal of experimental psychology. General.

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

[8]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[9]  Nicolás Seisdedos Cubero,et al.  Cuestionario de ansiedad estado-rasgo: manual , 1982 .

[10]  Florin Dolcos,et al.  Role of the inferior frontal cortex in coping with distracting emotions , 2006, Neuroreport.

[11]  M. Petrides Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory , 2000, The Journal of Neuroscience.

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

[13]  S. Paradiso,et al.  Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. , 1999, The American journal of psychiatry.

[14]  Florin Dolcos,et al.  The Impact of Anxiety-Inducing Distraction on Cognitive Performance: A Combined Brain Imaging and Personality Investigation , 2010, PloS one.

[15]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[16]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[17]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[18]  Jan Derrfuss,et al.  Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory , 2004, NeuroImage.

[19]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[20]  Joshua W. Brown,et al.  A meta-analysis of executive components of working memory. , 2013, Cerebral cortex.

[21]  Jennifer A. Silvers,et al.  Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion , 2012, Annals of the New York Academy of Sciences.

[22]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[23]  B. Postle,et al.  Superior Parietal Cortex Is Critical for the Manipulation of Information in Working Memory , 2009, The Journal of Neuroscience.

[24]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

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

[26]  Jonathan D. Cohen,et al.  The Role of Prefrontal Cortex in Normal and Disordered Cognitive Control: A Cognitive Neuroscience Perspective , 2009 .

[27]  G. McCarthy,et al.  Brain Systems Mediating Cognitive Interference by Emotional Distraction , 2006, The Journal of Neuroscience.

[28]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[29]  A. Damasio,et al.  Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. , 1996, Cerebral cortex.

[30]  Amanda Parker,et al.  The von Restorff Effect in Visual Object Recognition Memory in Humans and Monkeys: The Role of Frontal/Perirhinal Interaction , 1998, Journal of Cognitive Neuroscience.

[31]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[32]  M. Raichle,et al.  The Emotional Modulation of Cognitive Processing: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[33]  R. Elliott,et al.  Ventromedial prefrontal cortex mediates guessing , 1999, Neuropsychologia.

[34]  Jonathan D. Cohen,et al.  A Developmental Functional MRI Study of Prefrontal Activation during Performance of a Go-No-Go Task , 1997, Journal of Cognitive Neuroscience.

[35]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[36]  G. McCarthy,et al.  Opposing influences of emotional and non-emotional distracters upon sustained prefrontal cortex activity during a delayed-response working memory task , 2008, Neuropsychologia.

[37]  D. Louis Collins,et al.  Design and construction of a realistic digital brain phantom , 1998, IEEE Transactions on Medical Imaging.

[38]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[39]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[40]  Deanna M. Barch,et al.  Resisting emotional interference: Brain regions facilitating working memory performance during negative distraction , 2010, Cognitive, affective & behavioral neuroscience.

[41]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[42]  Ingrid R. Olson,et al.  The right parietal lobe is critical for visual working memory , 2008, Neuropsychologia.

[43]  S. Zeki,et al.  Neural correlates of beauty. , 2004, Journal of neurophysiology.

[44]  Lisa Y. M. Chuah,et al.  Sleep deprivation and interference by emotional distracters. , 2010, Sleep.

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

[46]  Mortimer Mishkin,et al.  The role of the inferior prefrontal convexity in performance of delayed nonmatching-to-sample , 1991, Neuropsychologia.

[47]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[48]  R. Kötter,et al.  Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. , 2000, Cerebral cortex.

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

[50]  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.

[51]  Florin Dolcos,et al.  NEURAL CORRELATES OF EMOTIONAL MEMORIES: A REVIEW OF EVIDENCE FROM BRAIN IMAGING STUDIES , 2012 .

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

[53]  M. Bradley,et al.  Activation of the visual cortex in motivated attention. , 2003, Behavioral neuroscience.

[54]  Luis Carretié,et al.  Automatic attention to emotional stimuli: Neural correlates , 2004, Human brain mapping.

[55]  M. Bradley,et al.  Remembering pictures: pleasure and arousal in memory. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[56]  Lisa Feldman Barrett,et al.  Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies , 2008, NeuroImage.

[57]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[58]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[59]  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.

[60]  Catherine J. Harmer,et al.  Expectancy and surprise predict neural and behavioral measures of attention to threatening stimuli , 2012, NeuroImage.

[61]  K. Mogg,et al.  Time course of attentional bias for threat information in non-clinical anxiety. , 1997, Behaviour research and therapy.

[62]  Florin Dolcos,et al.  Neural Correlates of Opposing Effects of Emotional Distraction on Working Memory and Episodic Memory: An Event-Related fMRI Investigation , 2013, Front. Psychol..

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

[64]  Elizabeth A. Kensinger,et al.  Negative Emotion Enhances Memory Accuracy , 2007 .

[65]  Alexandru D. Iordan,et al.  Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations , 2013, Front. Hum. Neurosci..

[66]  Dealing with messy data , 2012 .

[67]  Alexandru D. Iordan,et al.  Neural correlates of emotion–cognition interactions: A review of evidence from brain imaging investigations , 2011, Journal of cognitive psychology.

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

[69]  M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[70]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[71]  D. Grandjean,et al.  Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: Time course and topographic evoked‐potentials mapping , 2005, Human brain mapping.

[72]  M. Rushworth,et al.  Distinct Roles of Three Frontal Cortical Areas in Reward-Guided Behavior , 2011, The Journal of Neuroscience.