Event related beta and gamma oscillatory responses during perception of affective pictures

Several studies reveal that unpleasant pictures elicit higher beta and gamma responses than pleasant and/or neutral pictures; however, the effect of stimulation design (block or random) has not been studied before. The aim of the study is to analyze the common and distinct parameters of affective picture perception in block and random designs by means of analysis of high frequency oscillatory dynamics (beta and gamma). EEG of 22 healthy subjects was recorded at 32 locations. The participants passively viewed 120 emotional pictures (10 × 4 unpleasant, 10 × 4 pleasant, 10 × 4 neutral) in block and random designs. The phase-locking and power of event related beta (14-28 Hz) and gamma (29-48 Hz) oscillations were analyzed for two different time windows (0-200 ms/200-400 ms). Statistical analysis showed that in the 0-200 ms time window, during the block design, unpleasant stimulation elicited higher beta phase-locking and beta power than the pleasant and neutral stimulation (p<0.05). In the 200-400 ms time window, during the block design, over occipital electrodes unpleasant stimulation elicited higher gamma response power than the pleasant stimulation and neutral stimulation (p<0.05). Unpleasant stimulation did not elicit higher beta or gamma responses in the random design. The present study showed that experimental design highly influences the perception of IAPS pictures. Unpleasant stimulation elicited higher event related beta and gamma phase-locking and power only in block design but not in random design. It seems that longer blocks of aversive pictures affect the brain more than the rapid observation of these pictures.

[1]  M. Balconi,et al.  Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[2]  D. A. Peterson,et al.  Delay modulates spectral correlates in the human EEG of non-verbal auditory working memory , 2002, Neuroscience Letters.

[3]  E. Basar,et al.  Beta oscillatory responses in healthy subjects and subjects with mild cognitive impairment , 2013, NeuroImage: Clinical.

[4]  Christoph S. Herrmann,et al.  Altered evoked gamma-band responses reveal impaired early visual processing in ADHD children , 2010, Neuropsychologia.

[5]  R. Adolphs,et al.  Electrophysiological Responses in the Human Amygdala Discriminate Emotion Categories of Complex Visual Stimuli , 2002, The Journal of Neuroscience.

[6]  Erol Basar,et al.  Emotional face expressions are differentiated with brain oscillations. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[7]  Erol Başar,et al.  Brain oscillations : principles and approaches , 1998 .

[8]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[9]  R. Knight,et al.  Mechanisms of human attention: event-related potentials and oscillations , 2001, Neuroscience & Biobehavioral Reviews.

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

[11]  E. Basar,et al.  A review of brain oscillations in perception of faces and emotional pictures , 2014, Neuropsychologia.

[12]  Ingo Fründ,et al.  Human gamma-band activity: A review on cognitive and behavioral correlates and network models , 2010, Neuroscience & Biobehavioral Reviews.

[13]  G. Rhodes,et al.  Are you always on my mind? A review of how face perception and attention interact , 2007, Neuropsychologia.

[14]  A. Tzelepi,et al.  Functional properties of sub-bands of oscillatory brain waves to pattern visual stimulation in man , 2000, Clinical Neurophysiology.

[15]  R. James R. Blair,et al.  Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG , 2007, NeuroImage.

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

[17]  R. Maddock,et al.  Time course of the subjective emotional response to aversive pictures: relevance to fMRI studies , 2001, Psychiatry Research: Neuroimaging.

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

[19]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[20]  Jonas K. Olofsson,et al.  Affective picture processing: An integrative review of ERP findings , 2008, Biological Psychology.

[21]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[22]  M. Whittington,et al.  Gamma and beta frequency oscillations in response to novel auditory stimuli: A comparison of human electroencephalogram (EEG) data with in vitro models. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Angelo Gemignani,et al.  The dynamics of EEG gamma responses to unpleasant visual stimuli: From local activity to functional connectivity , 2012, NeuroImage.

[24]  Gennady G. Knyazev,et al.  Anxiety and oscillatory responses to emotional facial expressions , 2008, Brain Research.

[25]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[26]  G. Pfurtscheller,et al.  Motor imagery and action observation: Modulation of sensorimotor brain rhythms during mental control of a brain–computer interface , 2009, Clinical Neurophysiology.

[27]  E. Basar,et al.  Gamma-band responses in the brain: a short review of psychophysiological correlates and functional significance. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  Hannu Tiitinen,et al.  Human auditory event-related processes in the time-frequency plane , 2004, Neuroreport.

[29]  M Schürmann,et al.  Selectively distributed gamma band system of the brain. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[30]  G. Pfurtscheller,et al.  Patterns of cortical activation during planning of voluntary movement. , 1989, Electroencephalography and clinical neurophysiology.

[31]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[32]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[33]  Erol Başar,et al.  Brain oscillations evoked by the face of a loved person , 2008, Brain Research.

[34]  Rodrigo Quian Quiroga,et al.  Spatio-temporal frequency characteristics of intersensory components in audiovisually evoked potentials. , 2005, Brain research. Cognitive brain research.

[35]  G. Knyazev,et al.  Event-related delta and theta synchronization during explicit and implicit emotion processing , 2009, Neuroscience.

[36]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[37]  Andreas Keil,et al.  Adaptation in human visual cortex as a mechanism for rapid discrimination of aversive stimuli , 2007, NeuroImage.

[38]  T. Kochiyama,et al.  Rapid amygdala gamma oscillations in response to fearful facial expressions , 2011, Neuropsychologia.

[39]  E. Basar,et al.  A new interpretation of P300 responses upon analysis of coherences , 2010, Cognitive Neurodynamics.

[40]  E. Basar Brain Function and Oscillations , 1998 .

[41]  B. Bogerts,et al.  Altered evoked γ-band responses as a neurophysiological marker of schizophrenia? , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  J. Shaw EEG-brain dynamics E. Basar Elsevier/North-Holland, Amsterdam, 1980, pp. 411 Dfl. 184 , 1982, Biological Psychology.

[43]  E. Basar,et al.  Event-related beta oscillations are affected by emotional eliciting stimuli , 2010, Neuroscience Letters.

[44]  Matthias M. Müller,et al.  Processing of affective pictures modulates right-hemispheric gamma band EEG activity , 1999, Clinical Neurophysiology.

[45]  M. Eimer,et al.  Event-related brain potential correlates of emotional face processing , 2007, Neuropsychologia.

[46]  Matthias M. Müller,et al.  Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials , 2001, Clinical Neurophysiology.

[47]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.

[48]  E. Basar,et al.  Gender differences influence brain's beta oscillatory responses in recognition of facial expressions , 2007, Neuroscience Letters.

[49]  Juliana Yordanova,et al.  Tuning the brain for novelty detection under emotional threat: The role of increasing gamma phase-synchronization , 2010, NeuroImage.

[50]  C. C. Woodruff,et al.  Electroencephalographic &agr;-band and &bgr;-band correlates of perspective-taking and personal distress , 2011, Neuroreport.

[51]  Erol Başar,et al.  A review of gamma oscillations in healthy subjects and in cognitive impairment. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[53]  G. Pfurtscheller,et al.  Post-movement beta synchronization. A correlate of an idling motor area? , 1996, Electroencephalography and clinical neurophysiology.

[54]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[55]  F. Carver,et al.  Visual Awareness, Emotion, and Gamma Band Synchronization , 2008, Cerebral cortex.

[56]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[57]  E. Basar EEG-brain dynamics: Relation between EEG and Brain evoked potentials , 1980 .

[58]  W. Klimesch Brain Function and Oscillations, Vol. II: Integrative Brain Function. Neurophysiology and Cognitive Processes, edited by Erol Basar , 1999, Trends in Cognitive Sciences.

[59]  John J. Foxe,et al.  Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. , 2005, Cerebral cortex.

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