Neural mechanism of unconscious perception of surprised facial expression

Previous functional neuroimaging studies have uncovered partly separable neural substrates for perceiving different facial expressions presented below the level of conscious awareness. However, as one of the six basic emotions, the neural mechanism of unconsciously perceiving surprised faces has not yet been investigated. Using a backward masking procedure, we studied the neural activities in response to surprised faces presented below the threshold of conscious visual perception by means of functional magnetic resonance imaging (fMRI). Eighteen healthy adults were scanned while viewing surprised faces, which presented for 33 ms and immediately "masked" by a neutral face for 467 ms. As a control, they viewed masked happy or neutral faces as well. In comparison to both control conditions, masked surprised faces yielded significantly greater activation in the parahippocampal gyrus and fusiform gyrus, which associated previously with novelty detection. In the present study, automatic activation of these areas to masked surprised faces was investigated as a function of individual differences in the ability of identifying and differentiating one's emotions, as assessed by the 20-item Toronto Alexithymia Scale (TAS-20). The correlation results showed that, the subscale, Difficulty Identifying Feelings, was negatively correlated with the neural response of these areas to masked surprised faces, which suggest that decreased activation magnitude in specific brain regions may reflect increased difficulties in recognizing one's emotions in everyday life. Additionally, we confirmed activation of the right amygdala and right thalamus to the masked surprised faces, which was previously proved to be involved in the unconscious emotional perception system.

[1]  A. Schützwohl,et al.  Surprise and schema strength , 1998 .

[2]  Walter Heindel,et al.  Amygdala activation during masked presentation of emotional faces predicts conscious detection of threat-related faces , 2006, Brain and Cognition.

[3]  P. Ekman An argument for basic emotions , 1992 .

[4]  Dimitri J. Bayle,et al.  Unconsciously Perceived Fear in Peripheral Vision Alerts the Limbic System: A MEG Study , 2009, PloS one.

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

[6]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[7]  Gregory G. Brown,et al.  Functional abnormalities of medial temporal cortex during novel picture learning among patients with chronic schizophrenia , 2003, Schizophrenia Research.

[8]  Andrew L. Alexander,et al.  Contextual Modulation of Amygdala Responsivity to Surprised Faces , 2004, Journal of Cognitive Neuroscience.

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

[10]  C. Darwin The Expression of the Emotions in Man and Animals , .

[11]  R. Bagby,et al.  The twenty-item Toronto Alexithymia Scale--I. Item selection and cross-validation of the factor structure. , 1994, Journal of psychosomatic research.

[12]  A. Schützwohl,et al.  Surprise and schema strength. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

[13]  P. Ekman Unmasking The Face , 1975 .

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

[15]  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.

[16]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[17]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

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

[19]  D. Matsumoto American-Japanese Cultural Differences in the Recognition of Universal Facial Expressions , 1992 .

[20]  Joseph E LeDoux The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1996 .

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

[22]  Norihiro Sadato,et al.  Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study , 2004, NeuroImage.

[23]  M. de Zwaan,et al.  [Validation of the German version of the 20-item Toronto Alexithymia Scale in normal persons and psychiatric patients]. , 1996, Psychotherapie, Psychosomatik, medizinische Psychologie.

[24]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[25]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  R. Schultz Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area , 2005, International Journal of Developmental Neuroscience.

[27]  J. Driver,et al.  Functional Magnetic Resonance Imaging and Evoked Potential Correlates of Conscious and Unconscious Vision in Parietal Extinction Patients , 2001, NeuroImage.

[28]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

[29]  R. Dolan,et al.  fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. , 2004, Journal of neurophysiology.

[30]  R. Knight,et al.  Behavioral / Systems / Cognitive Rapid Prefrontal – Hippocampal Habituation to Novel Events , 2004 .

[31]  P. Ekman,et al.  American-Japanese cultural differences in intensity ratings of facial expressions of emotion , 1989 .

[32]  Raymond J. Dolan,et al.  Information theory, novelty and hippocampal responses: unpredicted or unpredictable? , 2005, Neural Networks.

[33]  U. Schroeder,et al.  Functional neuroanatomy of perceiving surprised faces , 2004, Human brain mapping.

[34]  G J Taylor,et al.  The Twenty-item Toronto Alexithymia Scale--II. Convergent, discriminant, and concurrent validity. , 1994, Journal of psychosomatic research.

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

[36]  T. Suslow,et al.  Alexithymic features and automatic amygdala reactivity to facial emotion , 2008, Neuroscience Letters.

[37]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Evian Gordon,et al.  A Direct Brainstem–amygdala–cortical Dalarmt System for Subliminal Signals of Fear , 2004 .

[39]  A. Young,et al.  Neuropsychology of fear and loathing , 2001 .

[40]  L. Bai,et al.  The Development of Native Chinese Affective Picture System-A pretest in 46 College Students , 2005 .

[41]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[42]  Wenfeng Feng,et al.  Three stages of facial expression processing: ERP study with rapid serial visual presentation , 2010, NeuroImage.

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

[44]  R. Zajonc Feeling and thinking : Preferences need no inferences , 1980 .

[45]  Stephen A. Engel,et al.  Application of Cortical Unfolding Techniques to Functional MRI of the Human Hippocampal Region , 2000, NeuroImage.

[46]  Karl J. Friston,et al.  Time‐dependent changes in effective connectivity measured with PET , 1993 .

[47]  D. Vaitl,et al.  Neuronale Aktivitätsmuster auf affektinduktive Reize bei Alexithymie , 2004 .

[48]  Isabell Wartenburger,et al.  A neural network reflecting individual differences in cognitive processing of emotions during perceptual decision making , 2006, NeuroImage.

[49]  Yuejia Luo,et al.  Neural correlates of the females' susceptibility to negative emotions: An insight into gender‐related prevalence of affective disturbances , 2009, Human brain mapping.

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

[51]  M. Phillips,et al.  Neural Responses to Facial Expressions of Disgust but not Fear are Modulated by Washing Symptoms in OCD , 2007, Biological Psychiatry.

[52]  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.

[53]  T. Suslow,et al.  Difficulty Identifying Feelings and Automatic Activation in the Fusiform Gyrus in Response to Facial Emotion , 2008, Perceptual and motor skills.

[54]  B R Rosen,et al.  Encoding novel face‐name associations: A functional MRI study , 2001, Human brain mapping.

[55]  Daniel L. Schacter,et al.  Perceptual Specificity in Visual Object Priming: fMRI Evidence for a Laterality Difference in Fusiform Cortex , 2001 .

[56]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[57]  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.