Affective Judgments of Faces Modulate Early Activity (∼160 ms) within the Fusiform Gyri

Functional neuroimaging studies have implicated the fusiform gyri (FG) in structural encoding of faces, while event-related potential (ERP) and magnetoen- cephalography studies have shown that such encoding occurs approximately 170 ms poststimulus. Behavioral and functional neuroimaging studies suggest that pro- cesses involved in face recognition may be strongly modulated by socially relevant information conveyed by faces. To test the hypothesis that affective informa- tion indeed modulates early stages of face processing, ERPs were recorded to individually assessed liked, neutral, and disliked faces and checkerboard-reversal stimuli. At the N170 latency, the cortical three-dimen- sional distribution of current density was computed in stereotactic space using a tomographic source local- ization technique. Mean activity was extracted from the FG, defined by structure-probability maps, and a meta-cluster delineated by the coordinates of the voxel with the strongest face-sensitive response from five published functional magnetic resonance imaging studies. In the FG, 160 ms poststimulus, liked faces elicited stronger activation than disliked and neutral faces and checkerboard-reversal stimuli. Further, confirming recent results, affect-modulated brain elec- trical activity started very early in the human brain (112 ms). These findings suggest that affective fea- tures conveyed by faces modulate structural face en- coding. Behavioral results from an independent study revealed that the stimuli were not biased toward par- ticular facial expressions and confirmed that liked faces were rated as more attractive. Increased FG ac- tivation for liked faces may thus be interpreted as reflecting enhanced attention due to their saliency.

[1]  E. Halgren,et al.  Cognitive response profile of the human fusiform face area as determined by MEG. , 2000, Cerebral cortex.

[2]  R. E. Gur,et al.  Effects of Emotional Discrimination Tasks on Cerebral Blood Flow: Regional Activation and Its Relation to Performance , 1994, Brain and Cognition.

[3]  R. Dolan,et al.  Contrast polarity and face recognition in the human fusiform gyrus , 1999, Nature Neuroscience.

[4]  K. Nakayama,et al.  RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA , 2000, Cognitive neuropsychology.

[5]  L. Deouell,et al.  STRUCTURAL ENCODING AND IDENTIFICATION IN FACE PROCESSING: ERP EVIDENCE FOR SEPARATE MECHANISMS , 2000, Cognitive neuropsychology.

[6]  B. Tabachnick,et al.  Using Multivariate Statistics , 1983 .

[7]  P. Schlattmann,et al.  Reduced Event-Related Current Density in the Anterior Cingulate Cortex in Schizophrenia , 2001, NeuroImage.

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

[9]  R. Dolan,et al.  Psychology: Reward value of attractiveness and gaze , 2001, Nature.

[10]  D. Lehmann,et al.  Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. , 1999, Neuroreport.

[11]  T Allison,et al.  ERPS EVOKED BY VIEWING FACIAL MOVEMENTS , 2000, Cognitive neuropsychology.

[12]  I. H. Öğüş,et al.  NATO ASI Series , 1997 .

[13]  S Braeutigam,et al.  Task-dependent early latency (30–60 ms) visual processing of human faces and other objects , 2001, Neuroreport.

[14]  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.

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

[16]  T Landis,et al.  Non-invasive epileptic focus localization using EEG-triggered functional MRI and electromagnetic tomography. , 1998, Electroencephalography and clinical neurophysiology.

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

[18]  M. Tarr,et al.  FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise , 2000, Nature Neuroscience.

[19]  W. Heller Neuropsychological mechanisms of individual differences in emotion, personality, and arousal. , 1993 .

[20]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[21]  L. Heimer Basal forebrain in the context of schizophrenia , 2000, Brain Research Reviews.

[22]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[23]  R. Kawashima,et al.  Passive and Active Recognition of One's Own Face , 2000, NeuroImage.

[24]  P. Fox,et al.  Cingulate function in depression: a potential predictor of treatment response , 1997, Neuroreport.

[25]  R. D. Pascual-Marqui,et al.  Localization of hypo- and hyperactivity in neuroleptic-naive, first-break, acute, productive schizophrenia using low resolution electromagnetic tomography (loreta) registered to the talairach human brain atlas , 1998, Schizophrenia Research.

[26]  A. Ohman,et al.  The face in the crowd revisited: a threat advantage with schematic stimuli. , 2001, Journal of personality and social psychology.

[27]  Shingo Yamagata,et al.  Cerebral Asymmetry of the “Top-Down” Allocation of Attention to Global and Local Features , 2000, The Journal of Neuroscience.

[28]  W Gaebel,et al.  Neurophysiological correlates of the recognition of facial expressions of emotion as revealed by magnetoencephalography. , 1999, Brain research. Cognitive brain research.

[29]  M. Eimer The face‐specific N170 component reflects late stages in the structural encoding of faces , 2000, Neuroreport.

[30]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. 1. Depth recorded potentials in the human occipital and parietal lobes , 1994, Journal of Physiology-Paris.

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

[32]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[33]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[34]  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.

[35]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[36]  S. Thorpe,et al.  The Time Course of Visual Processing: From Early Perception to Decision-Making , 2001, Journal of Cognitive Neuroscience.

[37]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[38]  R. Davidson Cerebral asymmetry and emotion: Conceptual and methodological conundrums , 1993 .

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

[40]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[41]  K. K. Tan,et al.  The spatial location of EEG electrodes: locating the best-fitting sphere relative to cortical anatomy. , 1993, Electroencephalography and clinical neurophysiology.

[42]  R. D. Pascual-Marqui,et al.  Face-elicited ERPs and affective attitude: brain electric microstate and tomography analyses , 2000, Clinical Neurophysiology.

[43]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

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

[45]  B. Brinkmann,et al.  Localization of the Epileptic Focus by Low-Resolution Electromagnetic Tomography in Patients with a Lesion Demonstrated by MRI , 2004, Brain Topography.

[46]  Patrik Vuilleumier,et al.  Emotional facial expressions capture attention , 2001, Neurology.

[47]  R. Pascual-Marqui Review of methods for solving the EEG inverse problem , 1999 .

[48]  Mitsuo Endo,et al.  Happy face advantage in recognizing facial expressions , 1995 .

[49]  R Kakigi,et al.  Human face perception traced by magneto- and electro-encephalography. , 1999, Brain research. Cognitive brain research.

[50]  Joan Y. Chiao,et al.  Differential responses in the fusiform region to same-race and other-race faces , 2001, Nature Neuroscience.

[51]  J C Lind,et al.  Low‐resolution electrical tomography of the brain during psychometrically matched verbal and spatial cognitive tasks , 2001, Human brain mapping.

[52]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[53]  K M Heilman,et al.  The neurobiology of emotional experience. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[54]  F. Doré,et al.  Accuracy and Latency of Judgment of Facial Expressions of Emotions , 1983, Perceptual and motor skills.

[55]  Andrew P. Holmes,et al.  CHAPTER 65 – Nonparametric Analysis of Statistic Images from Functional Mapping Experiments , 1996 .

[56]  A J Bruce,et al.  Face recognition as a function of judgments of likability/unlikability. , 1993, The Journal of general psychology.

[57]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

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

[59]  R. Dolan,et al.  Neural Activation during Covert Processing of Positive Emotional Facial Expressions , 1996, NeuroImage.

[60]  E. Halgren,et al.  LOCALISED FACE PROCESSING BY THE HUMAN PREFRONTAL CORTEX: FACE-SELECTIVE INTRACEREBRAL POTENTIALS AND POST-LESION DEFICITS , 2000, Cognitive neuropsychology.

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

[62]  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.

[63]  J. Pardo,et al.  The Role of the Fusiform Gyrus in Successful Encoding of Face Stimuli , 1999, NeuroImage.

[64]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[65]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[66]  N. Kanwisher,et al.  The selectivity of the occipitotemporal M170 for faces , 2000, Neuroreport.

[67]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[68]  R. Davidson,et al.  Anterior cingulate activity as a predictor of degree of treatment response in major depression: evidence from brain electrical tomography analysis. , 2001, The American journal of psychiatry.

[69]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[70]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[71]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[73]  J. Pernier,et al.  Neurophysiological correlates of face gender processing in humans , 2000, The European journal of neuroscience.

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

[75]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[76]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[77]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[78]  A. Ohman,et al.  Masking the face: recognition of emotional facial expressions as a function of the parameters of backward masking. , 1993, Scandinavian journal of psychology.

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

[80]  Mark H. Johnson,et al.  Modulation of event‐related potentials by prototypical and atypical faces , 2000, Neuroreport.

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

[82]  M. Sarter,et al.  Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents , 1999, Neuroscience.

[83]  J. Decety,et al.  Brain Regions Involved in the Perception of Gaze: A PET Study , 1998, NeuroImage.

[84]  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.

[85]  K. Mogg,et al.  ATTENTIONAL BIASES FOR EMOTIONAL FACES , 1997 .

[86]  A. Benton Facial Recognition 1990 , 1990, Cortex.