Face-elicited ERPs and affective attitude: brain electric microstate and tomography analyses

OBJECTIVES Although behavioral studies have demonstrated that normative affective traits modulate the processing of facial and emotionally charged stimuli, direct electrophysiological evidence for this modulation is still lacking. METHODS Event-related potential (ERP) data associated with personal, traitlike approach- or withdrawal-related attitude (assessed post-recording and 14 months later) were investigated in 18 subjects during task-free (i.e. unrequested, spontaneous) emotional evaluation of faces. Temporal and spatial aspects of 27 channel ERP were analyzed with microstate analysis and low resolution electromagnetic tomography (LORETA), a new method to compute 3 dimensional cortical current density implemented in the Talairach brain atlas. RESULTS Microstate analysis showed group differences 132-196 and 196-272 ms poststimulus, with right-shifted electric gravity centers for subjects with negative affective attitude. During these (over subjects reliably identifiable) personality-modulated, face-elicited microstates, LORETA revealed activation of bilateral occipito-temporal regions, reportedly associated with facial configuration extraction processes. Negative compared to positive affective attitude showed higher activity right temporal; positive compared to negative attitude showed higher activity left temporo-parieto-occipital. CONCLUSIONS These temporal and spatial aspects suggest that the subject groups differed in brain activity at early, automatic, stimulus-related face processing steps when structural face encoding (configuration extraction) occurs. In sum, the brain functional microstates associated with affect-related personality features modulate brain mechanisms during face processing already at early information processing stages.

[1]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[2]  C. Michel,et al.  Evidence for rapid face recognition from human scalp and intracranial electrodes , 1997, Neuroreport.

[3]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[4]  R Hari,et al.  Face-specific responses from the human inferior occipito-temporal cortex , 1997, Neuroscience.

[5]  T. Koenig,et al.  Brain electric microstates and momentary conscious mind states as building blocks of spontaneous thinking: I. Visual imagery and abstract thoughts. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[6]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]. , 1994, Journal of physiology, Paris.

[7]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[8]  A. Nakamura,et al.  Neuroanatomical correlates of the assessment of facial attractiveness , 1998, Neuroreport.

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

[10]  H Fischer,et al.  The amygdala and individual differences in human fear conditioning , 1997, Neuroreport.

[11]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[12]  W. Singer,et al.  Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey , 1992, The European journal of neuroscience.

[13]  E. Silberman,et al.  Hemispheric lateralization of functions related to emotion , 1986, Brain and Cognition.

[14]  E. Olivares,et al.  An ERP Study of Expectancy Violation in Face Perception , 1994, Brain and Cognition.

[15]  J. H. Steiger Tests for comparing elements of a correlation matrix. , 1980 .

[16]  H. Goldsmith Temperament: Variability in developing emotion systems. , 1993 .

[17]  Dietrich Lehmann,et al.  Source localization of brain electric activity during positive, neutral and negative emotional states , 2002 .

[18]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[20]  R A McCarthy,et al.  Prosopagnosia and structural encoding of faces: evidence from event-related potentials. , 1999, Neuroreport.

[21]  C M Michel,et al.  Extracranial localization of intracranial interictal epileptiform activity using LORETA (low resolution electromagnetic tomography). , 1997, Electroencephalography and clinical neurophysiology.

[22]  D. Lehmann,et al.  Adaptive segmentation of spontaneous EEG map series into spatially defined microstates. , 1993, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  D Brandeis,et al.  Neuroelectric mapping reveals precursor of stop failures in children with attention deficits , 1998, Behavioural Brain Research.

[24]  B. Renault,et al.  ERPs and chronometry of face recognition: following‐up Seeck et al. and George et al. , 1998, Neuroreport.

[25]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  D Lehmann,et al.  Affective attitudes to face images associated with intracerebral EEG source location before face viewing. , 1999, Brain research. Cognitive brain research.

[27]  E. Reiman,et al.  The application of positron emission tomography to the study of normal and pathologic emotions. , 1997, The Journal of clinical psychiatry.

[28]  T. Landis,et al.  Affective and Cognitive Decisions on Faces in Normals , 1986 .

[29]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[30]  E Halgren,et al.  Event-related potentials elicited by familiar and unfamiliar faces. , 1987, Electroencephalography and clinical neurophysiology. Supplement.

[31]  T. Allison,et al.  Face recognition in human extrastriate cortex. , 1994, Journal of neurophysiology.

[32]  J. Eccles The actions of antidromic impulses on ganglion cells , 1936, The Journal of physiology.

[33]  T. Koenig,et al.  Low resolution brain electromagnetic tomography (LORETA) functional imaging in acute, neuroleptic-naive, first-episode, productive schizophrenia , 1999, Psychiatry Research: Neuroimaging.

[34]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[35]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[36]  a.R.V.,et al.  Clinical neurophysiology , 1961, Neurology.

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

[38]  D. Jeffreys Evoked Potential Studies of Face and Object Processing , 1996 .

[39]  A. Young,et al.  Aspects of face processing , 1986 .

[40]  J. Rohrbaugh,et al.  Current trends in event-related potential research , 1987 .

[41]  D Lehmann,et al.  Event-related electric microstates of the brain differ between words with visual and abstract meaning. , 1998, Electroencephalography and clinical neurophysiology.

[42]  N. Kanwisher,et al.  Brain Imaging , 2003, Encyclopedia of Behavioral Medicine.

[43]  S. J. Swithenby,et al.  Neural processing of human faces: a magnetoencephalographic study , 1998, Experimental Brain Research.

[44]  J. Desmond,et al.  Hemispheric asymmetry for emotional stimuli detected with fMRI , 1998, Neuroreport.

[45]  A. Fallgatter,et al.  Three-dimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation. , 1998, Electroencephalography and clinical neurophysiology.

[46]  M. D’Esposito,et al.  Stimulus inversion and the responses of face and object-sensitive cortical areas. , 1999, Neuroreport.

[47]  Dietrich Lehmann,et al.  Microstates in Language-Related Brain Potential Maps Show Noun–Verb Differences , 1996, Brain and Language.

[48]  H. Lüders,et al.  American Electroencephalographic Society Guidelines for Standard Electrode Position Nomenclature , 1991, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[49]  P. Niedenthal,et al.  Emotional state and the use of stimulus dimensions in judgment. , 1997, Journal of personality and social psychology.

[50]  S M Kosslyn,et al.  Brain mechanisms in human classical conditioning: a PET blood flow study , 1995, Neuroreport.

[51]  Dietrich Lehmann,et al.  Spatial analysis of evoked potentials in man—a review , 1984, Progress in Neurobiology.

[52]  Dietrich Lehmann,et al.  Faces and emotions: brain electric field sources during covert emotional processing , 1998, Neuropsychologia.

[53]  R. Post,et al.  Abnormal Facial Emotion Recognition in Depression: , 1998, Behavior modification.

[54]  E Vaadia,et al.  Dynamics of neuronal interactions: Relation to behavior, firing rates, and distance between neurons , 1997, Human brain mapping.

[55]  R. Davidson Cerebral asymmetry, emotion, and affective style. , 1995 .

[56]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[57]  W. Sommer,et al.  Human brain potential correlates of face encoding into memory. , 1991, Electroencephalography and clinical neurophysiology.

[58]  E Callaway,et al.  Scopolamine effects on visual information processing, attention, and event-related potential map latencies. , 1992, Psychophysiology.

[59]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[60]  P. Ekman,et al.  Approach-withdrawal and cerebral asymmetry: emotional expression and brain physiology. I. , 1990, Journal of personality and social psychology.

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