A functional MRI study of human amygdala responses to facial expressions of fear versus anger.

Functional magnetic resonance imaging (fMRI) of the human brain was used to compare changes in amygdala activity associated with viewing facial expressions of fear and anger. Pictures of human faces bearing expressions of fear or anger, as well as faces with neutral expressions, were presented to 8 healthy participants. The blood oxygen-level dependent (BOLD) fMRI signal within the dorsal amygdala was significantly greater to Fear versus Anger, in a direct contrast. Significant BOLD signal changes in the ventral amygdala were observed in contrasts of Fear versus Neutral expressions and, in a more spatially circumscribed region, to Anger versus Neutral expressions. Thus, activity in the amygdala is greater to fearful facial expressions when contrasted with either neutral or angry faces. Furthermore, directly contrasting fear with angry faces highlighted involvement of the dorsal amygdaloid region.

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

[2]  W. L. Milligan,et al.  Effects of Partial and Continuous Reinforcement on Conditioned Heart Rate and Corneoretinal Potential Responses in the Rabbit (Oryctolagus Cuniculus) , 1975 .

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

[4]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[5]  J S Schwaber,et al.  Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  A. Sillito,et al.  Cholinergic modulation of the functional organization of the cat visual cortex , 1983, Brain Research.

[7]  D. Amaral,et al.  The afferent connections of the substantia innominata in the monkey, Macaca fascicularis , 1985, The Journal of comparative neurology.

[8]  P. Ekman,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES Universals and Cultural Differences in the Judgments of Facial Expressions of Emotion , 2004 .

[9]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[10]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[12]  M. Gallagher,et al.  The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  R. Metherate,et al.  Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors , 1991, Brain Research.

[14]  A. McDonald,et al.  Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat , 1991, Neuroscience.

[15]  R M Weisskoff,et al.  Ultra-fast imaging. , 1991, Magnetic resonance imaging.

[16]  V. Bowden,et al.  The Journal of Neuropsychiatry and Clinical Neurosciences , 1992 .

[17]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

[19]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[21]  P. Holland,et al.  Effects of amygdala central nucleus lesions on blocking and unblocking. , 1993, Behavioral neuroscience.

[22]  M. Gallagher,et al.  The amygdala complex: multiple roles in associative learning and attention. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[24]  B. Kapp,et al.  Neuronal activity within the nucleus basalis and conditioned neocortical electroencephalographic activation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  P. Ekman,et al.  Strong evidence for universals in facial expressions: a reply to Russell's mistaken critique. , 1994, Psychological bulletin.

[26]  B. Kapp,et al.  Effects of electrical stimulation of the amygdaloid central nucleus on neocortical arousal in the rabbit. , 1994, Behavioral neuroscience.

[27]  J. Richard Hanley,et al.  Face processing impairments after amygdalotomy , 1995 .

[28]  Kenneth Hugdahl,et al.  Affective judgment of the Ekman faces: A dimensional approach. , 1995 .

[29]  Bruce R. Rosen,et al.  Motion detection and correction in functional MR imaging , 1995 .

[30]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  K. Kwong Functional magnetic resonance imaging with echo planar imaging. , 1995, Magnetic resonance quarterly.

[32]  T. L. Davis,et al.  Automated shimming at 1.5 t using echo‐planar image frequency maps , 1995, Journal of magnetic resonance imaging : JMRI.

[33]  R. Rapee Current controversies in the anxiety disorders , 1996 .

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

[35]  Elisabeth A. Murray,et al.  What have ablation studies told us about the neural substrates of stimulus memory , 1996 .

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

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

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

[39]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

[40]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[41]  L. Heimer,et al.  Substantia innominata: a notion which impedes clinical–anatomical correlations in neuropsychiatric disorders , 1997, Neuroscience.

[42]  Younglim Lee,et al.  Roles of the Amygdala and Bed Nucleus of the Stria Terminalis in Fear and Anxiety Measured with the Acoustic Startle Reflex , 1997, Annals of the New York Academy of Sciences.

[43]  Michael Davis,et al.  Neurobiology of fear responses: the role of the amygdala. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[44]  A. McFarlane,et al.  Psychobiology of posttraumatic stress disorder. , 1997 .

[45]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[46]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[47]  T. Robbins,et al.  Central cholinergic systems and cognition. , 1997, Annual review of psychology.

[48]  P. Ekman,et al.  Matsumoto and Ekman's Japanese and Caucasian Facial Expressions of Emotion (JACFEE): Reliability Data and Cross-National Differences , 1997 .

[49]  Andrew W. Young,et al.  Face processing impairments after encephalitis: amygdala damage and recognition of fear , 1998, Neuropsychologia.

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

[51]  Michael Davis,et al.  Are different parts of the extended amygdala involved in fear versus anxiety? , 1998, Biological Psychiatry.

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

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

[54]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.

[55]  E. Murray,et al.  Aspiration lesions of the amygdala disrupt the rhinal corticothalamic projection system in rhesus monkeys , 1998, Experimental Brain Research.

[56]  U. Eysel,et al.  Neural structures associated with recognition of facial expressions of basic emotions , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  David Matsumoto,et al.  American-Japanese Differences in Multiscalar Intensity Ratings of Universal Facial Expressions of Emotion , 1998 .

[59]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[60]  D. Matsumoto,et al.  American-Japanese Cultural Differences in Judgements of Expression Intensity and Subjective Experience , 1999 .

[61]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[62]  M. Crommelinck,et al.  Effect of Familiarity on the Processing of Human Faces , 1999, NeuroImage.

[63]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[64]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[65]  S Z Rapcsak,et al.  Fear recognition deficits after focal brain damage: a cautionary note. , 2000, Neurology.

[66]  H Fischer,et al.  Differential response in the human amygdala to racial outgroup vs ingroup face stimuli , 2000, Neuroreport.

[67]  Lisa M Shin,et al.  Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study , 2000, Biological Psychiatry.

[68]  William A. Cunningham,et al.  Performance on Indirect Measures of Race Evaluation Predicts Amygdala Activation , 2000, Journal of Cognitive Neuroscience.

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

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

[71]  P. Holland,et al.  Lesions of the Amygdala Central Nucleus Alter Performance on a Selective Attention Task , 2000, The Journal of Neuroscience.

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

[73]  Kathleen M. Thomas,et al.  Amygdala response to facial expressions in children and adults , 2001, Biological Psychiatry.

[74]  E. Jolkkonen,et al.  Interconnectivity between the amygdaloid complex and the amygdalostriatal transition area: A PHA‐L study in rat , 2001 .