Decrease of prefrontal–posterior EEG coherence: Loose control during social–emotional stimulation

In two experiments we aimed to investigate if individual differences in state-dependent decreases or increases of EEG coherence between prefrontal and posterior cortical regions may be indicative of a mechanism modulating the impact social-emotional information has on an individual. Two independent samples were exposed to an emotional stimulation paradigm in which the participants were invited to get involved and sympathize with the persons they were watching (study 1) or listening to (study 2), and who were expressing sadness or anxiety. The two studies yielded consistent results. Higher scores in trait absorption and in the propensity to ruminate were associated with decreased EEG beta coherence during the stimulation, whereas coherence increased in individuals low in absorption or rumination. Coherence changes did not predict to which degree the participants felt infected by the displayed emotions, but in individuals showing decreased prefrontal-posterior coupling during the stimulation, feelings of sadness and anxiety had a greater tendency to persist. The findings suggest that more loose prefrontal-posterior coupling may be related to loosening of control of the prefrontal cortex over incoming social-emotional information and, consequently, to deeper emotional involvement and absorption, whereas increased prefrontal-posterior coupling may be related to strong control, dampening of emotional experience, and not letting oneself become emotionally affected.

[1]  E. Watkins Constructive and Unconstructive Repetitive Thought , 2008, Psychological bulletin.

[2]  Jan Seifert,et al.  Resting Brain Asymmetry and Affective Reactivity Aggregated Data Support the Right-Hemisphere Hypothesis , 2005 .

[3]  Eric Granholm,et al.  Pupillary and reaction time measures of sustained processing of negative information in depression , 2001, Biological Psychiatry.

[4]  Response styles questionnaire , 2012 .

[5]  Jean Decety,et al.  The empathic brain and its dysfunction in psychiatric populations: implications for intervention across different clinical conditions , 2007, BioPsychoSocial medicine.

[6]  J. Hietanen,et al.  Facial electromyographic responses to vocal affect expressions. , 1998, Psychophysiology.

[7]  B. McEwen Protective and damaging effects of stress mediators. , 1998, The New England journal of medicine.

[8]  Katie A McLaughlin,et al.  Rumination as a transdiagnostic factor in depression and anxiety. , 2011, Behaviour research and therapy.

[9]  Philip A. Gable,et al.  The role of asymmetric frontal cortical activity in emotion-related phenomena: A review and update , 2010, Biological Psychology.

[10]  Peter Erhard,et al.  A common neural basis for receptive and expressive communication of pleasant facial affect , 2005, NeuroImage.

[11]  N. Volf,et al.  Sex differences in EEG coherence during a verbal memory task in normal adults. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  K. Bredemeier,et al.  Psychological trauma and schizotypal personality disorder. , 2008, Journal of abnormal psychology.

[13]  Dimitri Van De Ville,et al.  Impact of transient emotions on functional connectivity during subsequent resting state: A wavelet correlation approach , 2011, NeuroImage.

[14]  Andreas A. Ioannides,et al.  Real-time neural activity and connectivity in healthy individuals and schizophrenia patients , 2004, NeuroImage.

[15]  B. Dahme,et al.  Die Absorption-Skala: Konzeptuelle Aspekte, psychometrische Kennwerte und Dimensionalität einer deutschsprachigen Adaptation. , 1995 .

[16]  Günter Schulter,et al.  Typical performance measures of emotion regulation and emotion perception and frontal EEG asymmetry in an emotional contagion paradigm , 2011 .

[17]  M. Reuter,et al.  Evidence for a common biological basis of the absorption trait, hallucinogen effects, and positive symptoms: Epistasis between 5‐HT2a and COMT polymorphisms , 2005, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[18]  P. Nunez,et al.  Neocortical Dynamics and Human EEG Rhythms , 1995 .

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

[20]  Peter Falkai,et al.  The power of imagination — How anticipatory mental imagery alters perceptual processing of fearful facial expressions , 2011, NeuroImage.

[21]  Kimron Shapiro,et al.  Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. D. Frith,et al.  The Role of the Dorsolateral Prefrontal Cortex in Random Number Generation: A Study with Positron Emission Tomography , 2000, NeuroImage.

[23]  G. Lienert,et al.  Hand-Dominanz-Test , 1971 .

[24]  Bartholomäus Wissmath,et al.  Immersion in Mediated Environments: The Role of Personality Traits , 2009, Cyberpsychology Behav. Soc. Netw..

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

[26]  André Aleman,et al.  Auditory Hallucinations in Schizophrenia Are Associated with Reduced Functional Connectivity of the Temporo-Parietal Area , 2010, Biological Psychiatry.

[27]  U. Hess,et al.  Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  M. Phillips,et al.  A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder , 2008, Molecular Psychiatry.

[29]  S. Nolen-Hoeksema Responses to depression and their effects on the duration of depressive episodes. , 1991, Journal of abnormal psychology.

[30]  P. Rappelsberger,et al.  EEG cohererence and reference signals: experimental results and mathematical explanations , 1998, Medical and Biological Engineering and Computing.

[31]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[32]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  Owe Svensson,et al.  Gender differences in facial imitation and verbally reported emotional contagion from spontaneous to emotionally regulated processing levels. , 2008, Scandinavian journal of psychology.

[34]  R. Davidson Anxiety and affective style: role of prefrontal cortex and amygdala , 2002, Biological Psychiatry.

[35]  R. Coppola,et al.  Functional and effective frontotemporal connectivity and genetic risk for schizophrenia , 2003, Biological Psychiatry.

[36]  S. Scott,et al.  Positive Emotions Preferentially Engage an Auditory–Motor “Mirror” System , 2006, The Journal of Neuroscience.

[37]  Günter Schulter,et al.  Frontal brain asymmetry and affective flexibility in an emotional contagion paradigm. , 2012, Psychophysiology.

[38]  J. Jonides,et al.  Brain mechanisms of proactive interference in working memory , 2006, Neuroscience.

[39]  Karl J. Friston,et al.  Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations , 2002, Biological Psychiatry.

[40]  John Gruzelier,et al.  Frontal functions, connectivity and neural efficiency underpinning hypnosis and hypnotic susceptibility , 2006 .

[41]  M. Rusalova,et al.  EEG Asymmetry in Humans: Relationship with Success in Recognizing Emotions in the Voice , 2009, Neuroscience and Behavioral Physiology.

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

[43]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[44]  A. Tellegen,et al.  Openness to absorbing and self-altering experiences ("absorption"), a trait related to hypnotic susceptibility. , 1974, Journal of abnormal psychology.

[45]  Magnus Lindgren,et al.  Differential frontal-parietal phase synchrony during hypnosis as a function of hypnotic suggestibility. , 2011, Psychophysiology.

[46]  Amishi P. Jha,et al.  Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain , 2005, NeuroImage.

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

[48]  K. James,et al.  The neural correlates of attempting to suppress negative versus neutral memories , 2010, Cognitive, affective & behavioral neuroscience.

[49]  E. Glucksman,et al.  Do Cognitive Models Help in Predicting the Severity of Posttraumatic Stress Disorder, Phobia, and Depression After Motor Vehicle Accidents? A Prospective Longitudinal Study , 2008, Journal of consulting and clinical psychology.

[50]  M. P. Abrams,et al.  The Attentional Resource Allocation Scale (ARAS): psychometric properties of a composite measure for dissociation and absorption , 2010, Depression and anxiety.

[51]  Moïra Mikolajczak,et al.  If you can regulate sadness, you can probably regulate shame: Associations between trait emotional intelligence, emotion regulation and coping efficiency across discrete emotions , 2008 .

[52]  H. Crawford Cognitive and Physiological Flexibility: Multiple Pathways to Hypnotic Responsiveness , 1989 .

[53]  Andreas Keil,et al.  Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks , 2004, NeuroImage.

[54]  I. Papousek,et al.  Gelotophobia, emotion-related skills and responses to the affective states of others , 2009 .

[55]  J. Sommerville,et al.  Shared representations between self and other: a social cognitive neuroscience view , 2003, Trends in Cognitive Sciences.

[56]  Sheri L. Johnson,et al.  Positive affect regulation in anxiety disorders. , 2009, Journal of anxiety disorders.

[57]  R. de Raedt,et al.  Deficient inhibition of emotional information in depression. , 2006, Journal of affective disorders.

[58]  John E. Hunter,et al.  Methods of Meta-Analysis: Correcting Error and Bias in Research Findings , 1991 .

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

[60]  Jutta Joormann,et al.  Updating the contents of working memory in depression: interference from irrelevant negative material. , 2008, Journal of abnormal psychology.

[61]  D. Schopflocher,et al.  The role of absorption in experiential involvement. , 1995 .

[62]  B. Schmeichel,et al.  Behavioural, affective, and physiological effects of negative and positive emotional exaggeration , 2004 .

[63]  A. Ehlers,et al.  The effects of rumination on mood and intrusive memories after exposure to traumatic material: An experimental study , 2009, Journal of behavior therapy and experimental psychiatry.

[64]  T. Giesbrecht,et al.  Alexithymia, Absorption, and Cognitive Failures in Depersonalization Disorder: A Comparison to Posttraumatic Stress Disorder and Healthy Volunteers , 2009, The Journal of nervous and mental disease.

[65]  T. Gasser,et al.  EEG power and coherence while male adults watch emotional video films. , 1990, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[66]  K. Bowers,et al.  A frontal assault on dissociated control. , 1994 .

[67]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[68]  María Corsi-Cabrera,et al.  Differential alpha coherence hemispheric patterns in men and women during pleasant and unpleasant musical emotions. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  S. Nolen-Hoeksema,et al.  A prospective study of depression and posttraumatic stress symptoms after a natural disaster: the 1989 Loma Prieta Earthquake. , 1991, Journal of personality and social psychology.

[70]  Alexander A. Fingelkurts,et al.  Cortex functional connectivity as a neurophysiological correlate of hypnosis: An EEG case study , 2007, Neuropsychologia.

[71]  J. Deakin,et al.  Abnormal neural oscillations in schizotypy during a visual working memory task: Support for a deficient top-down network? , 2011, Neuropsychologia.

[72]  R. de Raedt,et al.  Understanding depressive rumination from a cognitive science perspective: the impaired disengagement hypothesis. , 2011, Clinical psychology review.

[73]  Y. Dudai,et al.  Mesmerizing Memories: Brain Substrates of Episodic Memory Suppression in Posthypnotic Amnesia , 2008, Neuron.

[74]  I. Papousek,et al.  Effects of emotionally contagious films on changes in hemisphere-specific cognitive performance. , 2009, Emotion.

[75]  D. Hagemann,et al.  Individual differences in anterior EEG asymmetry: methodological problems and solutions , 2004, Biological Psychology.

[76]  J. Joormann Differential Effects of Rumination and Dysphoria on the Inhibition of Irrelevant Emotional Material: Evidence from a Negative Priming Task , 2006, Cognitive Therapy and Research.

[77]  M. Rusalova,et al.  EEG coherence in humans: relationship with success in recognizing emotions in the voice , 2009, Neuroscience and Behavioral Physiology.

[78]  J. Régis,et al.  Acute alteration of emotional behaviour in epileptic seizures is related to transient desynchrony in emotion-regulation networks , 2005, Clinical Neurophysiology.

[79]  Jack Block,et al.  Absorption: Construct Explication by Q-Sort Assessments of Personality , 2002 .

[80]  D. van Kampen The 5-Dimensional Personality Test (5DPT): Relationships With Two Lexically Based Instruments and the Validation of the Absorption Scale , 2012, Journal of personality assessment.

[81]  I. Papousek,et al.  Quantitative assessment of five behavioural laterality measures: distributions of scores and intercorrelations among right-handers. , 1999, Laterality.

[82]  J. Thayer,et al.  Stop that! Inhibition, sensitization, and their neurovisceral concomitants. , 2002, Scandinavian journal of psychology.

[83]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[84]  W Linden,et al.  Physiological stress reactivity and recovery: conceptual siblings separated at birth? , 1997, Journal of psychosomatic research.

[85]  M. Kikuchi,et al.  State-dependent changes in intrahemispheric EEG coherence for patients with acute exacerbation of schizophrenia , 2007, Psychiatry Research.

[86]  A. Kring,et al.  Sex differences in emotion: expression, experience, and physiology. , 1998, Journal of personality and social psychology.

[87]  P. Nunez,et al.  EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics , 2007, Journal of Neuroscience Methods.

[88]  D. Terhune,et al.  Hypnotic Experience is Related to Emotional Contagion , 2008, The International journal of clinical and experimental hypnosis.

[89]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[90]  B. T. Thomas Yeo,et al.  The Organization of Local and Distant Functional Connectivity in the Human Brain , 2010, PLoS Comput. Biol..

[91]  L. Cronbach,et al.  How we should measure "change": Or should we? , 1970 .

[92]  D Yves von Cramon,et al.  Distinct fMRI responses to laughter, speech, and sounds along the human peri-sylvian cortex. , 2005, Brain research. Cognitive brain research.

[93]  T. Sejnowski,et al.  Brain and cognition , 1989 .

[94]  Guido Gainotti,et al.  Neuropsychological theories of emotion. , 2000 .

[95]  S. Nolen-Hoeksema,et al.  Explaining the gender difference in depressive symptoms. , 1999, Journal of personality and social psychology.

[96]  N. V. Lotova,et al.  Non-linear dynamical coupling between different brain areas during evoked emotions: An EEG investigation , 1998, Biological Psychology.

[97]  Christopher K. Kovach,et al.  Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture , 2008, The Journal of Neuroscience.

[98]  I. Papousek,et al.  The interplay of perceiving and regulating emotions in becoming infected with positive and negative moods , 2008 .

[99]  Suzanne M. Roche,et al.  Absorption: Nature, assessment, and correlates. , 1990 .

[100]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[101]  V. Knott,et al.  Nicotine and the hallucinating brain: Effects on mismatch negativity (MMN) in schizophrenia , 2012, Psychiatry Research.

[102]  H. Flor,et al.  Retrieval and emotional processing of traumatic memories in posttraumatic stress disorder: Peripheral and central correlates , 2006, Neuropsychologia.

[103]  Mark Hamer,et al.  Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: a quantitative review of 30 years of investigations. , 2008, Psychological bulletin.

[104]  D. Keltner,et al.  Functional Accounts of Emotions , 1999 .

[105]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[106]  L. Schmidt,et al.  Cross-regional cortical synchronization during affective image viewing , 2010, Brain Research.