Brain, Vol. 122, No. 5, 883-893,
May 1999
© 1999 Oxford University Press
Dissociable neural responses to facial expressions of sadness and anger
1 Institute of Cognitive Neuroscience, 2 Department of Psychology, University College London, 3 Wellcome Department of Cognitive Neurology, London, 4 School of Psychology, University of St Andrews, Scotland, UK
Correspondence to:
Dr R. J. R. Blair, Institute of Cognitive Neuroscience, Alexandra House, 17 Queen Square, London WC1N 3AR, UK
Previous neuroimaging and neuropsychological studies have investigated the neural substrates which mediate responses to fearful, disgusted and happy expressions. No previous studies have investigated the neural substrates which mediate responses to sad and angry expressions. Using functional neuroimaging, we tested two hypotheses. First, we tested whether the amygdala has a neural response to sad and/or angry facial expressions. Secondly, we tested whether the orbitofrontal cortex has a specific neural response to angry facial expressions. Volunteer subjects were scanned, using PET, while they performed a sex discrimination task involving static grey-scale images of faces expressing varying degrees of sadness and anger. We found that increasing intensity of sad facial expression was associated with enhanced activity in the left amygdala and right temporal pole. In addition, we found that increasing intensity of angry facial expression was associated with enhanced activity in the orbitofrontal and anterior cingulate cortex. We found no support for the suggestion that angry expressions generate a signal in the amygdala. The results provide evidence for dissociable, but interlocking, systems for the processing of distinct categories of negative facial expression.
amygdala; orbitofrontal cortex; sadness; anger; facial expression
ANCOVA = analysis of covariance; rCBF = regional cerebral blood flow; SPM = statistical parametric mapping
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. L. Wood, V. Murko, and P. Nopoulos Ventral frontal cortex in children: morphology, social cognition and femininity/masculinity Soc Cogn Affect Neurosci, June 1, 2008; 3(2): 168 - 176. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. A. Marsh, E. C. Finger, D. G.V. Mitchell, M. E. Reid, C. Sims, D. S. Kosson, K. E. Towbin, E. Leibenluft, D. S. Pine, and R. J.R. Blair Reduced Amygdala Response to Fearful Expressions in Children and Adolescents With Callous-Unemotional Traits and Disruptive Behavior Disorders Am J Psychiatry, June 1, 2008; 165(6): 712 - 720. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Minagawa-Kawai, S. Matsuoka, I. Dan, N. Naoi, K. Nakamura, and S. Kojima Prefrontal Activation Associated with Social Attachment: Facial-Emotion Recognition in Mothers and Infants Cereb Cortex, May 30, 2008; (2008) bhn081v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Zahn, J. Moll, M. Paiva, G. Garrido, F. Krueger, E. D. Huey, and J. Grafman The Neural Basis of Human Social Values: Evidence from Functional MRI Cereb Cortex, May 22, 2008; (2008) bhn080v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. C. Finger, A. A. Marsh, D. G. Mitchell, M. E. Reid, C. Sims, S. Budhani, D. S. Kosson, G. Chen, K. E. Towbin, E. Leibenluft, et al. Abnormal Ventromedial Prefrontal Cortex Function in Children With Psychopathic Traits During Reversal Learning Arch Gen Psychiatry, May 1, 2008; 65(5): 586 - 594. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. L. LoPresti, K. Schon, M. D. Tricarico, J. D. Swisher, K. A. Celone, and C. E. Stern Working Memory for Social Cues Recruits Orbitofrontal Cortex and Amygdala: A Functional Magnetic Resonance Imaging Study of Delayed Matching to Sample for Emotional Expressions J. Neurosci., April 2, 2008; 28(14): 3718 - 3728. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. S. Heberlein, A. A. Padon, S. J. Gillihan, M. J. Farah, and L. K. Fellows Ventromedial Frontal Lobe Plays a Critical Role in Facial Emotion Recognition J. Cogn. Neurosci., April 1, 2008; 20(4): 721 - 733. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. MOLL, R. DE OLIVEIRA-SOUZA, and R. ZAHN The Neural Basis of Moral Cognition: Sentiments, Concepts, and Values Ann. N.Y. Acad. Sci., March 1, 2008; 1124(1): 161 - 180. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Wood, D. Heitmiller, N. C. Andreasen, and P. Nopoulos Morphology of the Ventral Frontal Cortex: Relationship to Femininity and Social Cognition Cereb Cortex, March 1, 2008; 18(3): 534 - 540. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Monk, R. G. Klein, E. H. Telzer, E. A. Schroth, S. Mannuzza, J. L. Moulton III, M. Guardino, C. L. Masten, E. B. McClure-Tone, S. Fromm, et al. Amygdala and Nucleus Accumbens Activation to Emotional Facial Expressions in Children and Adolescents at Risk for Major Depression Am J Psychiatry, January 1, 2008; 165(1): 90 - 98. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. G. Williams, D. I. Perrett, G. D. Waiter, and S. Pechey Differential effects of tryptophan depletion on emotion processing according to face direction Soc Cogn Affect Neurosci, December 1, 2007; 2(4): 264 - 273. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. L. Keightley, K. S. Chiew, G. Winocur, and C. L. Grady Age-related differences in brain activity underlying identification of emotional expressions in faces Soc Cogn Affect Neurosci, December 1, 2007; 2(4): 292 - 302. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. R. MILAD and S. L. RAUCH The Role of the Orbitofrontal Cortex in Anxiety Disorders Ann. N.Y. Acad. Sci., December 1, 2007; 1121(1): 546 - 561. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Geday, R. Kupers, and A. Gjedde As Time Goes By: Temporal Constraints on Emotional Activation of Inferior Medial Prefrontal Cortex Cereb Cortex, December 1, 2007; 17(12): 2753 - 2759. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Kveraga, J. Boshyan, and M. Bar Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition J. Neurosci., November 28, 2007; 27(48): 13232 - 13240. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. V. Rauch, P. Ohrmann, J. Bauer, H. Kugel, A. Engelien, V. Arolt, W. Heindel, and T. Suslow Cognitive Coping Style Modulates Neural Responses to Emotional Faces in Healthy Humans: A 3-T fMRI Study Cereb Cortex, November 1, 2007; 17(11): 2526 - 2535. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. D. Engell, J. V. Haxby, and A. Todorov Implicit trustworthiness decisions: automatic coding of face properties in the human amygdala. J. Cogn. Neurosci., September 1, 2007; 19(9): 1508 - 1519. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Kipps, A. J. Duggins, E. A. McCusker, and A. J. Calder Disgust and Happiness Recognition Correlate with Anteroventral Insula and Amygdala Volume Respectively in Preclinical Huntington's Disease. J. Cogn. Neurosci., July 1, 2007; 19(7): 1206 - 1217. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. R. Olson, A. Plotzker, and Y. Ezzyat The Enigmatic temporal pole: a review of findings on social and emotional processing Brain, July 1, 2007; 130(7): 1718 - 1731. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. van der Gaag, R. B. Minderaa, and C. Keysers The BOLD signal in the amygdala does not differentiate between dynamic facial expressions Soc Cogn Affect Neurosci, June 1, 2007; 2(2): 93 - 103. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Abe, M. Suzuki, E. Mori, M. Itoh, and T. Fujii Deceiving others: distinct neural responses of the prefrontal cortex and amygdala in simple fabrication and deception with social interactions. J. Cogn. Neurosci., February 1, 2007; 19(2): 287 - 295. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
V. Beaucousin, A. Lacheret, M.-R. Turbelin, M. Morel, B. Mazoyer, and N. Tzourio-Mazoyer FMRI Study of Emotional Speech Comprehension Cereb Cortex, February 1, 2007; 17(2): 339 - 352. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Sullivan, T. Ruffman, and S. B. Hutton Age Differences in Emotion Recognition Skills and the Visual Scanning of Emotion Faces J. Gerontol. B. Psychol. Sci. Soc. Sci., January 1, 2007; 62(1): P53 - P60. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Moll, F. Krueger, R. Zahn, M. Pardini, R. de Oliveira-Souza, and J. Grafman Human fronto-mesolimbic networks guide decisions about charitable donation PNAS, October 17, 2006; 103(42): 15623 - 15628. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Vien and A. R. Beech Psychopathy: theory, measurement, and treatment. Trauma Violence Abuse, July 1, 2006; 7(3): 155 - 174. [Abstract] [PDF]
|
|
|
|
|
|
S. Windmann, P. Kirsch, D. Mier, R. Stark, B. Walter, O. Gunturkun, and D. Vaitl On Framing Effects in Decision Making: Linking Lateral versus Medial Orbitofrontal Cortex Activation to Choice Outcome Processing. J. Cogn. Neurosci., July 1, 2006; 18(7): 1198 - 1211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Ruffman, S. Sullivan, and N. Edge Differences in the way older and younger adults rate threat in faces but not situations. J. Gerontol. B. Psychol. Sci. Soc. Sci., July 1, 2006; 61(4): P187 - P194. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Monk, E. E. Nelson, E. B. McClure, K. Mogg, B. P. Bradley, E. Leibenluft, R. J. R. Blair, G. Chen, D. S. Charney, M. Ernst, et al. Ventrolateral Prefrontal Cortex Activation and Attentional Bias in Response to Angry Faces in Adolescents With Generalized Anxiety Disorder Am J Psychiatry, June 1, 2006; 163(6): 1091 - 1097. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Kawasaki, R. Adolphs, H. Oya, C. Kovach, H. Damasio, O. Kaufman, and M. Howard III Analysis of Single-Unit Responses to Emotional Scenes in Human Ventromedial Prefrontal Cortex J. Cogn. Neurosci., October 1, 2005; 17(10): 1509. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. S. Maxwell, A. J. Shackman, and R. J. Davidson Unattended Facial Expressions Asymmetrically Bias the Concurrent Processing of Nonemotional Information J. Cogn. Neurosci., September 1, 2005; 17(9): 1386 - 1395. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. L. Bufkin and V. R. Luttrell Neuroimaging Studies of Aggressive and Violent Behavior: Current Findings and Implications for Criminology and Criminal Justice Trauma Violence Abuse, April 1, 2005; 6(2): 176 - 191. [Abstract] [PDF]
|
|
|
|
|
|
E. A. Nofzinger, D. J. Buysse, A. Germain, J. C. Price, C. C. Meltzer, J. M. Miewald, and D. J. Kupfer Alterations in Regional Cerebral Glucose Metabolism Across Waking and Non-Rapid Eye Movement Sleep in Depression Arch Gen Psychiatry, April 1, 2005; 62(4): 387 - 396. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. S. Milak, R. V. Parsey, J. Keilp, M. A. Oquendo, K. M. Malone, and J. J. Mann Neuroanatomic Correlates of Psychopathologic Components of Major Depressive Disorder Arch Gen Psychiatry, April 1, 2005; 62(4): 397 - 408. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. N. Ochsner, K. Knierim, D. H. Ludlow, J. Hanelin, T. Ramachandran, G. Glover, and S. C. Mackey Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other J. Cogn. Neurosci., December 1, 2004; 16(10): 1746 - 1772. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Wildgruber, I. Hertrich, A. Riecker, M. Erb, S. Anders, W. Grodd, and H. Ackermann Distinct Frontal Regions Subserve Evaluation of Linguistic and Emotional Aspects of Speech Intonation Cereb Cortex, December 1, 2004; 14(12): 1384 - 1389. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. H. Y. Fu, S. C. R. Williams, A. J. Cleare, M. J. Brammer, N. D. Walsh, J. Kim, C. M. Andrew, E. M. Pich, P. M. Williams, L. J. Reed, et al. Attenuation of the Neural Response to Sad Faces in Major Depression by Antidepressant Treatment: A Prospective, Event-Related Functional Magnetic Resonance Imaging Study Arch Gen Psychiatry, September 1, 2004; 61(9): 877 - 889. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Calder, J. Keane, A. D. Lawrence, and F. Manes Impaired recognition of anger following damage to the ventral striatum Brain, September 1, 2004; 127(9): 1958 - 1969. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. D. Dougherty, S. L. Rauch, T. Deckersbach, C. Marci, R. Loh, L. M. Shin, N. M. Alpert, A. J. Fischman, and M. Fava Ventromedial Prefrontal Cortex and Amygdala Dysfunction During an Anger Induction Positron Emission Tomography Study in Patients With Major Depressive Disorder With Anger Attacks Arch Gen Psychiatry, August 1, 2004; 61(8): 795 - 804. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Hennenlotter, U. Schroeder, P. Erhard, B. Haslinger, R. Stahl, A. Weindl, H. G. von Einsiedel, K. W. Lange, and A. O. Ceballos-Baumann Neural correlates associated with impaired disgust processing in pre-symptomatic Huntington's disease Brain, June 1, 2004; 127(6): 1446 - 1453. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B Brierley, N Medford, P Shaw, and A S David Emotional memory and perception in temporal lobectomy patients with amygdala damage J. Neurol. Neurosurg. Psychiatry, April 1, 2004; 75(4): 593 - 599. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U Schroeder, A Kuehler, A Hennenlotter, B Haslinger, V M Tronnier, M Krause, R Pfister, R Sprengelmeyer, K W Lange, and A O Ceballos-Baumann Facial expression recognition and subthalamic nucleus stimulation J. Neurol. Neurosurg. Psychiatry, April 1, 2004; 75(4): 648 - 650. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. Williams, A. P. Morris, F. McGlone, D. F. Abbott, and J. B. Mattingley Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression J. Neurosci., March 24, 2004; 24(12): 2898 - 2904. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Adolphs and D. Tranel Impaired Judgments of Sadness But Not Happiness Following Bilateral Amygdala Damage J. Cogn. Neurosci., March 1, 2004; 16(3): 453 - 462. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K Dujardin, S Blairy, L Defebvre, P Krystkowiak, U Hess, S Blond, and A Destee Subthalamic nucleus stimulation induces deficits in decoding emotional facial expressions in Parkinson's disease J. Neurol. Neurosurg. Psychiatry, February 1, 2004; 75(2): 202 - 208. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. M. Watson From Interpretation to Identification: a History of Facial Images in the Sciences of Emotion History of the Human Sciences, February 1, 2004; 17(1): 29 - 51. [Abstract] [PDF]
|
|
|
|
|
|
E. LEIBENLUFT, R J. R. BLAIR, D. S. CHARNEY, and D. S. PINE Irritability in Pediatric Mania and Other Childhood Psychopathology Ann. N.Y. Acad. Sci., December 1, 2003; 1008(1): 201 - 218. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Glascher and R. Adolphs Processing of the Arousal of Subliminal and Supraliminal Emotional Stimuli by the Human Amygdala J. Neurosci., November 12, 2003; 23(32): 10274 - 10282. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Kasai, M. E. Shenton, D. F. Salisbury, T. Onitsuka, S. K. Toner, D. Yurgelun-Todd, R. Kikinis, F. A. Jolesz, and R. W. McCarley Differences and Similarities in Insular and Temporal Pole MRI Gray Matter Volume Abnormalities in First-Episode Schizophrenia and Affective Psychosis Arch Gen Psychiatry, November 1, 2003; 60(11): 1069 - 1077. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. S. LaBar, M. J. Crupain, J. T. Voyvodic, and G. McCarthy Dynamic Perception of Facial Affect and Identity in the Human Brain Cereb Cortex, October 1, 2003; 13(10): 1023 - 1033. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Hornak, J. Bramham, E. T. Rolls, R. G. Morris, J. O'Doherty, P. R. Bullock, and C. E. Polkey Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices Brain, July 1, 2003; 126(7): 1691 - 1712. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kano, S. Fukudo, J. Gyoba, M. Kamachi, M. Tagawa, H. Mochizuki, M. Itoh, M. Hongo, and K. Yanai Specific brain processing of facial expressions in people with alexithymia: an H215O-PET study Brain, June 1, 2003; 126(6): 1474 - 1484. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition J. Cogn. Neurosci., May 1, 2003; 15(4): 600 - 609. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. G. Shamay-Tsoory, R. Tomer, B. D. Berger, and J. Aharon-Peretz Characterization of Empathy Deficits following Prefrontal Brain Damage: The Role of the Right Ventromedial Prefrontal Cortex J. Cogn. Neurosci., April 1, 2003; 15(3): 324 - 337. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Critchley Emotion and its disorders: Imaging in clinical neuroscience Br. Med. Bull., March 1, 2003; 65(1): 35 - 47. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Schneider, U. Habel, J. Volkmann, S. Regel, J. Kornischka, V. Sturm, and H.-J. Freund Deep Brain Stimulation of the Subthalamic Nucleus Enhances Emotional Processing in Parkinson Disease Arch Gen Psychiatry, March 1, 2003; 60(3): 296 - 302. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. J. R. Blair Neurobiological basis of psychopathy The British Journal of Psychiatry, January 2, 2003; 182(1): 5 - 7. [Full Text] [PDF]
|
|
|
|
|
|
R. Adolphs, S. Baron-Cohen, and D. Tranel Impaired Recognition of Social Emotions following Amygdala Damage J. Cogn. Neurosci., November 1, 2002; 14(8): 1264 - 1274. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Z. Goldstein and N. D. Volkow Drug Addiction and Its Underlying Neurobiological Basis: Neuroimaging Evidence for the Involvement of the Frontal Cortex Am J Psychiatry, October 1, 2002; 159(10): 1642 - 1652. [Abstract] [Full Text] [PDF]
|