Dynamics of processing invisible faces in the brain: Automatic neural encoding of facial expression information

The fusiform face area (FFA) and the superior temporal sulcus (STS) are suggested to process facial identity and facial expression information respectively. We recently demonstrated a functional dissociation between the FFA and the STS as well as correlated sensitivity of the STS and the amygdala to facial expressions using an interocular suppression paradigm [Jiang, Y., He, S., 2006. Cortical responses to invisible faces: dissociating subsystems for facial-information processing. Curr. Biol. 16, 2023-2029.]. In the current event-related brain potential (ERP) study, we investigated the temporal dynamics of facial information processing. Observers viewed neutral, fearful, and scrambled face stimuli, either visibly or rendered invisible through interocular suppression. Relative to scrambled face stimuli, intact visible faces elicited larger positive P1 (110-130 ms) and larger negative N1 or N170 (160-180 ms) potentials at posterior occipital and bilateral occipito-temporal regions respectively, with the N170 amplitude significantly greater for fearful than neutral faces. Invisible intact faces generated a stronger signal than scrambled faces at 140-200 ms over posterior occipital areas whereas invisible fearful faces (compared to neutral and scrambled faces) elicited a significantly larger negative deflection starting at 220 ms along the STS. These results provide further evidence for cortical processing of facial information without awareness and elucidate the temporal sequence of automatic facial expression information extraction.

[1]  Margot J. Taylor,et al.  Source analysis of the N170 to faces and objects , 2004, Neuroreport.

[2]  Brian N. Pasley,et al.  Subcortical Discrimination of Unperceived Objects during Binocular Rivalry , 2004, Neuron.

[3]  N. Sadato,et al.  Attention to emotion modulates fMRI activity in human right superior temporal sulcus. , 2001, Brain research. Cognitive brain research.

[4]  A. Damasio,et al.  Intact recognition of facial expression, gender, and age in patients with impaired recognition of face identity , 1988, Neurology.

[5]  M. Hasselmo,et al.  The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey , 1989, Behavioural Brain Research.

[6]  A. Cowey,et al.  Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation , 1990, Neuropsychologia.

[7]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[8]  Margot J. Taylor,et al.  Inversion and contrast-reversal effects on face processing assessed by MEG , 2006, Brain Research.

[9]  Sheng He,et al.  Cortical Responses to Invisible Faces: Dissociating Subsystems for Facial-Information Processing , 2006, Current Biology.

[10]  Alan W Freeman,et al.  Multistage model for binocular rivalry. , 2005, Journal of neurophysiology.

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

[12]  J M Wolfe,et al.  Influence of Spatial Frequency, Luminance, and Duration on Binocular Rivalry and Abnormal Fusion of Briefly Presented Dichoptic Stimuli , 1983, Perception.

[13]  François Mauguière,et al.  Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex A Depth Electrode ERP Study in Human , 2004, Neuron.

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

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

[16]  K. Nakayama,et al.  Rapid adaptation of the m170 response: importance of face parts. , 2008, Cerebral cortex.

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

[18]  A. Cowey,et al.  The role of the 'face-cell' area in the discrimination and recognition of faces by monkeys. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[20]  A. Ishai,et al.  Effective connectivity within the distributed cortical network for face perception. , 2007, Cerebral cortex.

[21]  R. Blake,et al.  Fearful expressions gain preferential access to awareness during continuous flash suppression. , 2007, Emotion.

[22]  N. Sagiv,et al.  Structural Encoding of Human and Schematic Faces: Holistic and Part-Based Processes , 2001, Journal of Cognitive Neuroscience.

[23]  A. Young,et al.  Understanding the recognition of facial identity and facial expression , 2005, Nature Reviews Neuroscience.

[24]  A. Young,et al.  Face processing impairments after amygdalotomy. , 1997, Brain : a journal of neurology.

[25]  Elana Zion-Golumbic,et al.  Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces , 2007, NeuroImage.

[26]  Urs Maurer,et al.  The face-specific N170 component is modulated by emotional facial expression , 2007, Behavioral and Brain Functions.

[27]  Adam P. Morris,et al.  Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression , 2004, The Journal of Neuroscience.

[28]  Sheng He,et al.  Processing of Invisible Stimuli: Advantage of Upright Faces and Recognizable Words in Overcoming Interocular Suppression , 2007, Psychological science.

[29]  K. Nakayama,et al.  Binocular Rivalry and Visual Awareness in Human Extrastriate Cortex , 1998, Neuron.

[30]  J. Katayama,et al.  Face-specific N170 component is modulated by facial expressional change , 2004, Neuroreport.

[31]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

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

[33]  Hervé Abdi,et al.  Processing Faces and Facial Expressions , 2003, Neuropsychology Review.

[34]  C. Koch,et al.  Continuous flash suppression reduces negative afterimages , 2005, Nature Neuroscience.

[35]  David Alais,et al.  Increasing depth of binocular rivalry suppression along two visual pathways , 2003, Vision Research.

[36]  Randolph Blake,et al.  Depth of interocular suppression associated with continuous flash suppression, flash suppression, and binocular rivalry. , 2006, Journal of vision.

[37]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

[38]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[39]  K. Nakayama,et al.  Rapid face-selective adaptation of an early extrastriate component in MEG. , 2006, Cerebral cortex.

[40]  N. Kanwisher,et al.  The M170 is selective for faces, not for expertise , 2005, Neuropsychologia.

[41]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[42]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[43]  Glyn W. Humphreys,et al.  Expression is computed separately from facial identity, and it is computed separately for moving and static faces: Neuropsychological evidence , 1993, Neuropsychologia.

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

[45]  N. Logothetis,et al.  Visual competition , 2002, Nature Reviews Neuroscience.

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