Event-related induced frontal alpha as a marker of lateral prefrontal cortex activation during cognitive reappraisal

Electrocortical activity, typically used to track the effects of cognitive reappraisal on the processing of emotional stimuli, has not been used to index the prefrontal-cortex-mediated regulatory mechanisms responsible for these effects. In the present study, we examined the novel possibility that induced frontal alpha (i.e., 8–13 Hz), shown to reflect the inhibition and disengagement of task-relevant cortical regions, may be quantified to explore cortical activation that is specifically enhanced during cognitive reappraisal. For this purpose, 44 participants viewed unpleasant and neutral pictures followed by auditory instructions to either continue viewing the picture or reduce their emotional response to the picture by making the picture seem less emotional (i.e., cognitive reappraisal). In line with previous work, unpleasant pictures elicited a larger late positive potential (LPP) than did neutral pictures. Also corroborating previous work, the mid-latency LPP was reduced when pictures were cognitively reappraised. However, the present study showed for the first time that whereas unpleasant pictures elicited higher frontal alpha power bilaterally than did the neutral pictures, frontal alpha power was reduced (indicative of more activation and cognitive control) during cognitive reappraisal of both picture types over the left hemisphere. Taken together, the LPP and event-related induced frontal-alpha findings contribute unique information about the distinct neural substrates and cognitive processes underlying reappraisal.

[1]  R. Simons,et al.  Modulations of the electrophysiological response to pleasant stimuli by cognitive reappraisal. , 2008, Emotion.

[2]  F. Harris On the use of windows for harmonic analysis with the discrete Fourier transform , 1978, Proceedings of the IEEE.

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

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

[5]  Barry D. Smith,et al.  Cerebral processing of nonverbal affective stimuli: Differential effects of cognitive and affective sets on hemispheric asymmetry , 1987, Biological Psychology.

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

[7]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[8]  Marty G. Woldorff,et al.  Dissociation of event-related potentials indexing arousal and semantic cohesion during emotional word encoding , 2006, Brain and Cognition.

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

[10]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[11]  Dan Foti,et al.  Deconstructing Reappraisal: Descriptions Preceding Arousing Pictures Modulate the Subsequent Neural Response , 2008, Journal of Cognitive Neuroscience.

[12]  I. Franken,et al.  Intentional Modulation of the Late Positive Potential in Response to Smoking Cues by Cognitive Strategies in Smokers , 2011, PloS one.

[13]  K. LaBar,et al.  Startle Modulation during Conscious Emotion Regulation Is Arousal-dependent , 2022 .

[14]  Michael J Kahana,et al.  EEG correlates of verbal and nonverbal working memory , 2005, Behavioral and Brain Functions.

[15]  Brent L. Hughes,et al.  Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation , 2008, Neuron.

[16]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[17]  R. Davidson,et al.  Suppression and enhancement of emotional responses to unpleasant pictures. , 2000, Psychophysiology.

[18]  G. Hajcak,et al.  Event-Related Potentials, Emotion, and Emotion Regulation: An Integrative Review , 2010, Developmental neuropsychology.

[19]  Greg Hajcak,et al.  The persistence of attention to emotion: brain potentials during and after picture presentation. , 2008, Emotion.

[20]  John J. B. Allen,et al.  Prefrontal brain asymmetry and pre-menstrual dysphoric disorder symptomatology. , 2011, Journal of affective disorders.

[21]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[22]  R. Simons,et al.  Electrophysiological correlates of decreasing and increasing emotional responses to unpleasant pictures. , 2009, Psychophysiology.

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

[24]  M. Iacoboni,et al.  Movement-related desynchronization of alpha rhythms is lower in athletes than non-athletes: A high-resolution EEG study , 2010, Clinical Neurophysiology.

[25]  Dan Foti,et al.  Neural response to emotional pictures is unaffected by concurrent task difficulty: an event-related potential study. , 2007, Behavioral neuroscience.

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

[27]  J. Gross Emotion regulation: affective, cognitive, and social consequences. , 2002, Psychophysiology.

[28]  A. Turken,et al.  Left inferior frontal gyrus is critical for response inhibition , 2008, BMC Neuroscience.

[29]  Matthew C. Keller,et al.  Increased sensitivity in neuroimaging analyses using robust regression , 2005, NeuroImage.

[30]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[31]  Greg Hajcak,et al.  See no evil: directing visual attention within unpleasant images modulates the electrocortical response. , 2009, Psychophysiology.

[32]  G. Hajcak,et al.  Differentiating neural responses to emotional pictures: evidence from temporal-spatial PCA. , 2009, Psychophysiology.

[33]  J. Gross,et al.  Hiding feelings: the acute effects of inhibiting negative and positive emotion. , 1997, Journal of abnormal psychology.

[34]  Matti Laine,et al.  Cortical activation related to auditory semantic matching of concrete versus abstract words , 1999, Clinical Neurophysiology.

[35]  Robert T. Knight,et al.  Effects of frontal lobe damage on interference effects in working memory , 2002, Cognitive, affective & behavioral neuroscience.

[36]  A. Horn,et al.  The Neural Substrate of Positive Bias in Spontaneous Emotional Processing , 2010, PloS one.

[37]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[38]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[39]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[40]  H. Barbas,et al.  Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey , 2002, Neuroscience.

[41]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[42]  Jaeseung Jeong,et al.  Decreased Phase Synchronization of the EEG in Patients with Major Depressive Disorder , 2007 .

[43]  Claudio Del Percio,et al.  Brains “in concert”: Frontal oscillatory alpha rhythms and empathy in professional musicians , 2012, NeuroImage.

[44]  J. Thayer,et al.  The quest for the EEG reference revisited: a glance from brain asymmetry research. , 2001, Psychophysiology.

[45]  Simon Hanslmayr,et al.  Resting frontal EEG alpha-asymmetry predicts the evaluation of affective musical stimuli , 2009, Neuroscience Letters.

[46]  M. Bradley,et al.  Affective picture processing: the late positive potential is modulated by motivational relevance. , 2000, Psychophysiology.

[47]  Greg Hajcak,et al.  Previously reappraised: the lasting effect of description type on picture-elicited electrocortical activity. , 2011, Social cognitive and affective neuroscience.

[48]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[49]  Nora D. Volkow,et al.  Cognitive control of drug craving inhibits brain reward regions in cocaine abusers , 2010, NeuroImage.

[50]  Kewei Chen,et al.  Association between trait emotional awareness and dorsal anterior cingulate activity during emotion is arousal-dependent , 2008, NeuroImage.

[51]  G Nolte,et al.  Partial signal space projection for artefact removal in MEG measurements: a theoretical analysis. , 2001, Physics in medicine and biology.

[52]  Anna Weinberg,et al.  Beyond good and evil: the time-course of neural activity elicited by specific picture content. , 2010, Emotion.

[53]  L. Aftanas,et al.  Event-Related Synchronization and Desynchronization During Affective Processing: Emergence of Valence-Related Time-Dependent Hemispheric Asymmetries in Theta and Upper Alpha Band , 2001, The International journal of neuroscience.

[54]  W. Klimesch,et al.  Simultaneous desynchronization and synchronization of different alpha responses in the human electroencephalograph: a neglected paradox? , 2000, Neuroscience Letters.

[55]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

[56]  Dan Foti,et al.  Motivated and controlled attention to emotion: Time-course of the late positive potential , 2009, Clinical Neurophysiology.

[57]  B. Mensour,et al.  Neural basis of emotional self-regulation in childhood , 2004, Neuroscience.

[58]  Markus Heinrichs,et al.  The neural correlates of sex differences in emotional reactivity and emotion regulation , 2009, Human brain mapping.

[59]  J. Gross Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. , 1998, Journal of personality and social psychology.

[60]  Claus C. Hilgetag,et al.  Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala , 2007, NeuroImage.

[61]  J. Gross The Emerging Field of Emotion Regulation: An Integrative Review , 1998 .

[62]  J. Gross,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES Emotion Regulation and Memory: The Cognitive Costs of Keeping One's Cool , 2004 .

[63]  J. Henry,et al.  Effective regulation of the experience and expression of negative affect in old age. , 2008, The journals of gerontology. Series B, Psychological sciences and social sciences.

[64]  S. Nieuwenhuis,et al.  Reappraisal modulates the electrocortical response to unpleasant pictures , 2006, Cognitive, affective & behavioral neuroscience.

[65]  Febo Cincotti,et al.  Sub-second "temporal attention" modulates alpha rhythms. A high-resolution EEG study. , 2004, Brain research. Cognitive brain research.

[66]  R. Davidson What does the prefrontal cortex “do” in affect: perspectives on frontal EEG asymmetry research , 2004, Biological Psychology.

[67]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[68]  Dan Foti,et al.  Tell me about it: neural activity elicited by emotional pictures and preceding descriptions. , 2009, Emotion.

[69]  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.

[70]  Greg Hajcak,et al.  Attending to affect: appraisal strategies modulate the electrocortical response to arousing pictures. , 2006, Emotion.

[71]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[72]  S. Rossi,et al.  Human cortical responses during one-bit short-term memory. A high-resolution EEG study on delayed choice reaction time tasks , 2004, Clinical Neurophysiology.

[73]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

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

[75]  Andreas Keil,et al.  The dynamic allocation of attention to emotion: Simultaneous and independent evidence from the late positive potential and steady state visual evoked potentials , 2013, Biological Psychology.

[76]  R. Sinha,et al.  Difficulties in emotion regulation and impulse control during cocaine abstinence. , 2007, Drug and alcohol dependence.

[77]  R. Simons,et al.  Intentional modulation of emotional responding to unpleasant pictures: an ERP study. , 2006, Psychophysiology.

[78]  John Polich,et al.  Affective ERP processing in a visual oddball task: Arousal, valence, and gender , 2008, Clinical Neurophysiology.

[79]  Frank Telang,et al.  Motivated attention to cocaine and emotional cues in abstinent and current cocaine users – an ERP study , 2011, The European journal of neuroscience.

[80]  Kevin N. Ochsner,et al.  The neural architecture of emotion regulation , 2007 .

[81]  Francesco Versace,et al.  Affective picture perception: Emotion, context, and the late positive potential , 2008, Brain Research.

[82]  J. Gross,et al.  Thinking makes it so: A social cognitive neuroscience approach to emotion regulation. , 2004 .

[83]  R. Reilly,et al.  Behavioural and physiological impairments of sustained attention after traumatic brain injury. , 2004, Brain research. Cognitive brain research.

[84]  J. Gabrieli,et al.  Gender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal , 2008, Group processes & intergroup relations : GPIR.

[85]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[86]  Heather L. Urry,et al.  Amygdala and Ventromedial Prefrontal Cortex Are Inversely Coupled during Regulation of Negative Affect and Predict the Diurnal Pattern of Cortisol Secretion among Older Adults , 2006, The Journal of Neuroscience.

[87]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[88]  G. Knyazev Motivation, emotion, and their inhibitory control mirrored in brain oscillations , 2007, Neuroscience & Biobehavioral Reviews.

[89]  J. Gross,et al.  Emotional suppression: physiology, self-report, and expressive behavior. , 1993, Journal of personality and social psychology.

[90]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.