Amygdala activation during masked presentation of emotional faces predicts conscious detection of threat-related faces

It has been argued that critical functions of the human amygdala are to modulate the moment-to-moment vigilance level and to enhance the processing and the consolidation of memories of emotionally arousing material. In this functional magnetic resonance study, pictures of human faces bearing fearful, angry, and happy expressions were presented to nine healthy volunteers using a backward masking procedure based on neutral facial expression. Activation of the left and right amygdala in response to the masked fearful faces (compared to neutral faces) was significantly correlated with the number of fearful faces detected. In addition, right but not left amygdala activation in response to the masked angry faces was significantly related to the number of angry faces detected. The present findings underscore the role of the amygdala in the detection and consolidation of memory for marginally perceptible threatening facial expression.

[1]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Joseph E LeDoux The emotional brain , 1996 .

[3]  M. Gabriel,et al.  Learning and Computational Neuroscience: Foundations of Adaptive Networks , 1990 .

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

[5]  Steven G. Potkin,et al.  Sex-Related Difference in Amygdala Activity during Emotionally Influenced Memory Storage , 2001, Neurobiology of Learning and Memory.

[6]  P. Ekman Pictures of Facial Affect , 1976 .

[7]  Hans-Ulrich Wittchen,et al.  DIA-X-Interviews: Manual für Screening-Verfahren und Interview; Interviewheft , 1997 .

[8]  J. Gabrieli,et al.  Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience , 2000, The Journal of Neuroscience.

[9]  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.

[10]  S. Rauch,et al.  Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study , 2003, Brain Research Bulletin.

[11]  A. Kersting,et al.  Evidence for glutamatergic neuronal dysfunction in the prefrontal cortex in chronic but not in first-episode patients with schizophrenia: a proton magnetic resonance spectroscopy study , 2005, Schizophrenia Research.

[12]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[13]  Oliver T Wolf,et al.  MRI volume of the amygdala: a reliable method allowing separation from the hippocampal formation , 1999, Psychiatry Research: Neuroimaging.

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

[15]  Håkan Fischer,et al.  Enhanced amygdala responses to emotional versus neutral schematic facial expressions , 2002, Neuroreport.

[16]  Jessica Turner,et al.  Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. , 2004, Learning & memory.

[17]  J L McGaugh,et al.  Amygdala activity at encoding correlated with long-term, free recall of emotional information. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[19]  Alex Wilson,et al.  A neuro - anatomical systems analysis of conditioned bradycardia in the rabbit , 1991 .

[20]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[21]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

[22]  T. Suslow,et al.  N-acetylaspartate levels of left frontal cortex are associated with verbal intelligence in women but not in men: a proton magnetic resonance spectroscopy study , 2004, Neuroscience.

[23]  V. Arolt,et al.  Acute mania is accompanied by elevated glutamate/glutamine levels within the left dorsolateral prefrontal cortex , 2003, Psychopharmacology.

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

[25]  S Robinson,et al.  Optimized 3 T EPI of the amygdalae , 2004, NeuroImage.

[26]  A. Kersting,et al.  Proton magnetic resonance spectroscopy in anorexia nervosa: correlations with cognition , 2004, Neuroreport.

[27]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[28]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[29]  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.

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

[31]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[32]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[33]  Martin Fiebich,et al.  Effective electroconvulsive therapy reverses glutamate/glutamine deficit in the left anterior cingulum of unipolar depressed patients , 2003, Psychiatry Research: Neuroimaging.

[34]  J. D. McGaugh Memory consolidation and the amygdala: a systems perspective , 2002, Trends in Neurosciences.

[35]  V. Arolt,et al.  Neurotrophic Effects of Electroconvulsive Therapy: A Proton Magnetic Resonance Study of the Left Amygdalar Region in Patients with Treatment-Resistant Depression , 2003, Neuropsychopharmacology.

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

[37]  V. Arolt,et al.  Metabolic changes within the left dorsolateral prefrontal cortex occurring with electroconvulsive therapy in patients with treatment resistant unipolar depression , 2003, Psychological Medicine.

[38]  J. D. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences. , 2004, Annual review of neuroscience.

[39]  R. Nebes,et al.  Reliability and validity of some handedness questionnaire items. , 1974, Neuropsychologia.

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

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

[42]  Larry Cahill,et al.  Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage , 2003, NeuroImage.

[43]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[44]  C. Windischberger Optimized 3 T EPI of the amygdalae S . Robinson , a , 2004 .