Inter-hemispherical functional coupling of EEG rhythms during the perception of facial emotional expressions

OBJECTIVE Brain rhythms of both hemispheres are involved in the processing of emotional stimuli but their interdependence between the two hemispheres is poorly known. Here we tested the hypothesis that passive visual perception of facial emotional expressions is related to a coordination of the two hemispheres as revealed by the inter-hemispherical functional coupling of brain electroencephalographic (EEG) rhythms. METHODS To this aim, EEG data were recorded in 14 subjects observing emotional faces with neutral, happy or sad facial expressions (about 33% for each class). The EEG data were analyzed by directed transfer function (DTF), which estimates directional functional coupling of EEG rhythms. The EEG rhythms of interest were theta (about 4-6 Hz), alpha 1 (about 6-8 Hz), alpha 2 (about 8-10 Hz), alpha 3 (about 10-12 Hz), beta 1 (13-20 Hz), beta 2 (21-30 Hz), and gamma (31-44 Hz). RESULTS In the frontal regions, inter-hemispherical DTF values were bidirectionally higher in amplitude across all frequency bands, during the perception of faces with sad compared to neutral or happy expressions. CONCLUSIONS These results suggest that the processing of emotional negative facial expressions is related to an enhancement of a reciprocal inter-hemispherical flux of information in frontal cortex, possibly optimizing executive functions and motor control. SIGNIFICANCE Dichotomical view of hemispherical functional specializations does not take into account remarkable reciprocal interactions between frontal areas of the two hemispheres during the processing of negative facial expressions.

[1]  P. Rossini,et al.  Coupling between "hand" primary sensorimotor cortex and lower limb muscles after ulnar nerve surgical transfer in paraplegia. , 2004, Behavioral neuroscience.

[2]  P. Corballis.  Visuospatial processing and the right-hemisphere interpreter , 2003, Brain and Cognition.

[3]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[4]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[5]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[6]  Leslie G. Ungerleider,et al.  Repetition suppression of faces is modulated by emotion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Diana Van Lancker-Sidtis,et al.  Communicative deficits in agenesis of the corpus callosum: Nonliteral language and affective prosody , 2003, Brain and Language.

[8]  Margot J. Taylor,et al.  N170 or N1? Spatiotemporal differences between object and face processing using ERPs. , 2004, Cerebral cortex.

[9]  A. Nowicka,et al.  Interhemispheric transmission of information and functional asymmetry of the human brain , 1996, Neuropsychologia.

[10]  M. Banich,et al.  A generalized role of interhemispheric interaction under attentionally demanding conditions: evidence from the auditory and tactile modality , 2002, Neuropsychologia.

[11]  Simultaneous verbal and affective laterality effects , 1994, Neuropsychologia.

[12]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[13]  M. Kaminski,et al.  Information flow between hippocampus and related structures during various types of rat's behavior , 1997, Journal of Neuroscience Methods.

[14]  Kylie J. Barnett,et al.  Lack of asymmetrical transfer for linguistic stimuli in schizophrenia: an ERP study , 2005, Clinical Neurophysiology.

[15]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[16]  W. Klimesch.  Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[17]  M. Hallett,et al.  Functional coupling of human right and left cortical motor areas demonstrated with partial coherence analysis , 2000, Neuroscience Letters.

[18]  M. Kaminski,et al.  Topographic analysis of coherence and propagation of EEG activity during sleep and wakefulness. , 1997, Electroencephalography and clinical neurophysiology.

[19]  A. Damasio,et al.  Face agnosia and the neural substrates of memory. , 1990, Annual review of neuroscience.

[20]  Aina Puce,et al.  Neural responses elicited to face motion and vocalization pairings , 2007, Neuropsychologia.

[21]  M. Banich,et al.  The cerebral hemispheres cooperate to perform complex but not simple tasks. , 2000, Neuropsychology.

[22]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[23]  Leslie G. Ungerleider,et al.  The Representation of Objects in the Human Occipital and Temporal Cortex , 2000, Journal of Cognitive Neuroscience.

[24]  G. Tononi.  Consciousness, information integration, and the brain. , 2005, Progress in brain research.

[25]  Michela Balconi,et al.  Arousal effect on emotional face comprehension Frequency band changes in different time intervals , 2009, Physiology & Behavior.

[26]  Jerre Levy,et al.  Effects of processing speed on cerebral asymmetry for left- and right-oriented faces , 1991, Brain and Cognition.

[27]  H. Groenewegen,et al.  The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia , 1997, Journal of psychopharmacology.

[28]  M. Coltheart,et al.  The role of affect and reasoning in a patient with a delusion of misidentification , 2002, Cognitive neuropsychiatry.

[29]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[30]  R. Sullivan,et al.  Hemispheric Asymmetry in Stress Processing in Rat Prefrontal Cortex and the Role of Mesocortical Dopamine , 2004, Stress.

[31]  Febo Cincotti,et al.  Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis. , 2004, Behavioral neuroscience.

[32]  J B Hellige,et al.  Effects of concurrent verbal memory on recognition of stimuli from the left and right visual fields. , 1976, Journal of experimental psychology. Human perception and performance.

[33]  M. Kinsbourne.  The cerebral basis of lateral asymmetries in attention. , 1970, Acta psychologica.

[34]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[35]  W. Klimesch,et al.  Induced alpha band power changes in the human EEG and attention , 1998, Neuroscience Letters.

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

[37]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[38]  Samuel W. Fernberger,et al.  Reaction Time To Retinal Stimulation: With Special Reference To The Time Lost In Conduction Through Nerve Centers... , 2009 .

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

[40]  V. Bruce.  Influences of Familiarity on the Processing of Faces , 1986, Perception.

[41]  R. Bauer,et al.  Autonomic recognition of names and faces in prosopagnosia: A neuropsychological application of the guilty knowledge test , 1984, Neuropsychologia.

[42]  Claudio Babiloni,et al.  Directional information flows between brain hemispheres across waking, non-REM and REM sleep states: An EEG study , 2009, Brain Research Bulletin.

[43]  K. Bötzel,et al.  Scalp topography and analysis of intracranial sources of face-evoked potentials , 2004, Experimental Brain Research.

[44]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[45]  J. Sergent,et al.  Prosopagnosia in a right hemispherectomized patient. , 1989, Brain : a journal of neurology.

[46]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Bruno Rossion,et al.  Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170 , 2008, NeuroImage.

[48]  Claudio Babiloni,et al.  Cortical responses to consciousness of schematic emotional facial expressions: A high‐resolution EEG study , 2010, Human brain mapping.

[49]  Brigitte Rockstroh,et al.  Reduced interhemispheric transmission in schizophrenia patients: evidence from event-related potentials , 2002, Neuroscience Letters.

[50]  P. Rossini,et al.  Changes in fronto‐posterior functional coupling at sleep onset in humans , 2004, Journal of sleep research.

[51]  C J Price,et al.  The neural systems sustaining face and proper-name processing. , 1998, Brain : a journal of neurology.

[52]  M S Gazzaniga.  Regional Differences in Cortical Organization , 2000, Science.

[53]  J. Liederman.  Determinants of the Enhancement of the Right Visual Field Advantage by Bilateral vs. Unilateral Stimuli , 1986, Cortex.

[54]  C. E. Izard.  Emotions as motivations: an evolutionary-developmental perspective. , 1978, Nebraska Symposium on Motivation. Nebraska Symposium on Motivation.

[55]  Jacqueline Liederman,et al.  The Dynamics of Interhemispheric Collaboration and Hemispheric Control , 1998, Brain and Cognition.

[56]  Katarzyna J. Blinowska,et al.  Determination of EEG activity propagation: pair-wise versus multichannel estimate , 2004, IEEE Transactions on Biomedical Engineering.

[57]  V. Bruce,et al.  Recognition of unfamiliar faces , 2000, Trends in Cognitive Sciences.

[58]  Michèle Fabre-Thorpe,et al.  Animal and human faces in natural scenes: How specific to human faces is the N170 ERP component? , 2004, Journal of vision.

[59]  M. Kaminski,et al.  Granger causality and information flow in multivariate processes. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  K. Zilles,et al.  The neural correlates of person familiarity. A functional magnetic resonance imaging study with clinical implications. , 2001, Brain : a journal of neurology.

[61]  Á. Pascual-Leone,et al.  Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex , 2001, Nature Neuroscience.

[62]  A. Young,et al.  Impaired recognition and experience of disgust following brain injury , 2000, Nature Neuroscience.

[63]  P. Rossini,et al.  Directional information flows between brain hemispheres during presleep wake and early sleep stages. , 2007, Cerebral cortex.

[64]  E. Ross,et al.  Lateralization of Affective Prosody in Brain and the Callosal Integration of Hemispheric Language Functions , 1997, Brain and Language.

[65]  James M. Kilner,et al.  Brain systems for assessing facial attractiveness , 2007, Neuropsychologia.

[66]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[67]  Jill Keane,et al.  Impaired recognition of anger following damage to the ventral striatum. , 2004, Brain : a journal of neurology.

[68]  Karl J. Friston,et al.  Interhemispheric Integration of Visual Processing during Task-Driven Lateralization , 2007, The Journal of Neuroscience.

[69]  M. Tarr,et al.  The N170 occipito‐temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face‐specific processes in the human brain , 2000, Neuroreport.

[70]  J D Holtzman,et al.  Dissociation of spatial information for stimulus localization and the control of attention. , 1981, Brain : a journal of neurology.

[71]  Fabrizio Vecchio,et al.  An electroencephalographic fingerprint of human sleep , 2005, NeuroImage.