Cortical Responses to Invisible Faces: Dissociating Subsystems for Facial-Information Processing

Perceiving faces is critical for social interaction. Evidence suggests that different neural pathways may be responsible for processing face identity and expression information. By using functional magnetic resonance imaging (fMRI), we measured brain responses when observers viewed neutral, fearful, and scrambled faces, either visible or rendered invisible through interocular suppression. The right fusiform face area (FFA), the right superior temporal sulcus (STS), and the amygdala responded strongly to visible faces. However, when face images became invisible, activity in FFA to both neutral and fearful faces was much reduced, although still measurable; activity in the STS was robust only to invisible fearful faces but not to neutral faces. Activity in the amygdala was equally strong in both the visible and invisible conditions to fearful faces but much weaker in the invisible condition for the neutral faces. In the invisible condition, amygdala activity was highly correlated with that of the STS but not with FFA. The results in the invisible condition support the existence of dissociable neural systems specialized for processing facial identity and expression information. When images are invisible, cortical responses may reflect primarily feed-forward visual-information processing and thus allow us to reveal the distinct functions of FFA and STS.

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

[2]  Peter J. Lang,et al.  Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance , 2005, NeuroImage.

[3]  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.

[4]  N. Kanwisher,et al.  The Neural Basis of the Behavioral Face-Inversion Effect , 2005, Current Biology.

[5]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[6]  Geoffrey M. Boynton,et al.  Efficient Design of Event-Related fMRI Experiments Using M-Sequences , 2002, NeuroImage.

[7]  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.

[8]  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.

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

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

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

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

[13]  L. Weiskrantz,et al.  Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. , 2001, Brain : a journal of neurology.

[14]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[15]  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.

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

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

[18]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

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

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

[21]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

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

[23]  S Zeki,et al.  The relationship between cortical activation and perception investigated with invisible stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[25]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

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

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

[28]  Michael Angstadt,et al.  Beyond threat: Amygdala reactivity across multiple expressions of facial affect , 2006, NeuroImage.

[29]  A. Calder Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear , 1996 .

[30]  F. Fang,et al.  Cortical responses to invisible objects in the human dorsal and ventral pathways , 2005, Nature Neuroscience.

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

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

[33]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[34]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[36]  Jason B. Mattingley,et al.  Differential amygdala responses to happy and fearful facial expressions depend on selective attention , 2005, NeuroImage.