Emotional face processing in schizophrenia.

PURPOSE OF REVIEW Recent studies of face processing deficits in people with schizophrenia have begun to shed light on the answers to four important questions: What is the major component of the deficit? Does it have a neurobiological basis? When does it appear in development? Can it be remediated? RECENT FINDINGS Eye contact is especially important for recognizing fearful expressions. Patients with schizophrenia avoid gazing at important facial feature regions (especially eyes) and are particularly impaired in recognizing fear. Patients were thought to exhibit decreased amygdala activity when viewing fearful faces; however, more recent studies have revealed limbic hyperactivity in patients when viewing nonfearful and fearful faces compared with baseline. Amygdala hyperactivity can also be detected when people with schizophrenia fail to appropriately recognize fear faces. Studies indicate that there are developmental changes in amygdala activation, including limbic hyperactivity to fear faces during adolescence, a critical time for the onset of schizophrenia. New treatment strategies can increase gaze to the eye region, which could improve emotional recognition in patients. SUMMARY These findings suggest that there may soon be more options for overcoming specific problems in emotional face evaluation in people who have schizophrenia.

[1]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[2]  Leanne M Williams,et al.  Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample , 2002, Schizophrenia Research.

[3]  Max Coltheart,et al.  Remediation of facial emotion perception in schizophrenia: Concomitant changes in visual attention , 2008, Schizophrenia Research.

[4]  E. Gordon,et al.  Eye movement response to a facial stimulus in schizophrenia , 1992, Biological Psychiatry.

[5]  David J McGonigle,et al.  Elsevier Editorial System(tm) for Biological Psychiatry Manuscript Draft Title: Overactivation of Fear Systems to Neutral Faces in Schizophrenia Fear of Faces in Schizophrenia in This Issue Statement Overactivation of Fear Systems to Neutral Faces in Schizophrenia , 2022 .

[6]  R. Compton.  The interface between emotion and attention: a review of evidence from psychology and neuroscience. , 2003, Behavioral and cognitive neuroscience reviews.

[7]  J. Kleinman,et al.  Age-related differences in glucocorticoid receptor mRNA levels in the human brain , 2007, Neurobiology of Aging.

[8]  T. Hendler,et al.  Feeling or Features Different Sensitivity to Emotion in High-Order Visual Cortex and Amygdala , 2001, Neuron.

[9]  E. Gordon,et al.  Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia , 2007, Schizophrenia Research.

[10]  Dennis R. Combs,et al.  Social Cognition and Interaction Training (SCIT) for inpatients with schizophrenia spectrum disorders: Preliminary findings , 2007, Schizophrenia Research.

[11]  Ralph Adolphs,et al.  Amygdala Damage Impairs Eye Contact During Conversations with Real People , 2007, The Journal of Neuroscience.

[12]  Kevin S LaBar,et al.  Development of emotional facial recognition in late childhood and adolescence. , 2007, Developmental science.

[13]  H. Silver,et al.  Brief emotion training improves recognition of facial emotions in chronic schizophrenia. A pilot study , 2004, Psychiatry Research.

[14]  U. Habel,et al.  Stability of emotional dysfunctions? A long-term fMRI study in first-episode schizophrenia. , 2007, Journal of psychiatric research.

[15]  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.

[16]  Kosha Ruparel,et al.  Limbic activation associated with misidentification of fearful faces and flat affect in schizophrenia. , 2007, Archives of general psychiatry.

[17]  A W Toga,et al.  Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study , 2009, Molecular Psychiatry.

[18]  G. Glover,et al.  Biological Substrates of Emotional Reactivity and Regulation in Adolescence During an Emotional Go-Nogo Task , 2008, Biological Psychiatry.

[19]  D. Penn,et al.  Emotion recognition and social competence in chronic schizophrenia. , 1996, Journal of abnormal psychology.

[20]  P. Benson,et al.  Neural responses to dynamic expressions of fear in schizophrenia , 2007, Neuropsychologia.

[21]  Ulrich Schall,et al.  Functional MRI of facial emotion recognition deficits in schizophrenia and their electrophysiological correlates , 2005, The European journal of neuroscience.

[22]  M. Bell,et al.  Affect recognition in schizophrenia: a function of global impairment or a specific cognitive deficit , 1997, Psychiatry Research.

[23]  P. Goldman-Rakic,et al.  Differential Postnatal Development of Catecholamine and Serotonin Inputs to Identified Neurons in Prefrontal Cortex of Rhesus Monkey , 2000, The Journal of Neuroscience.

[24]  R. McCarley,et al.  Functional and structural deficits in brain regions subserving face perception in schizophrenia. , 2006, The American journal of psychiatry.

[25]  W. M. Kelley,et al.  Human Amygdala Sensitivity to the Pupil Size of Others , 2008, Cerebral cortex.

[26]  J. Kwon,et al.  Dysfunction in Configural Face Processing in Patients With Schizophrenia , 2007, Schizophrenia bulletin.

[27]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[28]  R. Gur,et al.  Facial emotion discrimination: III. Behavioral findings in schizophrenia , 1992, Psychiatry Research.

[29]  Adriana Galvan,et al.  The adolescent brain. , 2008, Developmental review : DR.

[30]  J. Giedd.  Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[31]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[32]  J. Kleinman,et al.  Alteration in Estrogen Receptor α mRNA Levels in Frontal Cortex and Hippocampus of Patients with Major Mental Illness , 2005, Biological Psychiatry.

[33]  Simon Surguladze,et al.  Facial fear processing and psychotic symptoms in schizophrenia: functional magnetic resonance imaging study , 2008, British Journal of Psychiatry.

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

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

[36]  T. Hare,et al.  The Adolescent Brain , 2008, Annals of the New York Academy of Sciences.

[37]  Garrison W. Cottrell,et al.  Transmitting and Decoding Facial Expressions , 2005, Psychological science.

[38]  U. Habel,et al.  Neuronal Correlates of Facial Emotion Discrimination in Early Onset Schizophrenia , 2009, Neuropsychopharmacology.

[39]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[40]  D. Penn,et al.  Attentional-shaping as a means to improve emotion perception deficits in schizophrenia , 2008, Schizophrenia Research.

[41]  K. Mueser,et al.  Deficits in facial-affect recognition and schizophrenia. , 1988, Schizophrenia bulletin.

[42]  M. Webster,et al.  Alterations in trkB mRNA in the human prefrontal cortex throughout the lifespan , 2002, The European journal of neuroscience.

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

[44]  C. Marvel,et al.  Configural processing in face recognition in schizophrenia , 2002, Cognitive neuropsychiatry.

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

[46]  P. Veinante,et al.  Vasopressin and Oxytocin Excite Distinct Neuronal Populations in the Central Amygdala , 2005, Science.

[47]  R. J. Dolan,et al.  Human Amygdala Responses to Fearful Eyes , 2002, NeuroImage.

[48]  I. Feinberg,et al.  Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? , 1982, Journal of psychiatric research.

[49]  J. Rapoport,et al.  Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years , 1995, The Journal of comparative neurology.

[50]  G. Glover,et al.  Earlier Development of the Accumbens Relative to Orbitofrontal Cortex Might Underlie Risk-Taking Behavior in Adolescents , 2006, The Journal of Neuroscience.

[51]  R. Blake,et al.  Fearful expressions gain preferential access to awareness during continuous flash suppression. , 2007, Emotion.

[52]  Michael F. Green,et al.  Biosocial pathways to functional outcome in schizophrenia , 2005, Schizophrenia Research.

[53]  Robin M. Chan,et al.  An fMRI study of facial emotion processing in patients with schizophrenia. , 2002, The American journal of psychiatry.

[54]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

[55]  Peter Kirsch,et al.  Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans , 2005, The Journal of Neuroscience.

[56]  Ahmad R. Hariri,et al.  Neural bases of different cognitive strategies for facial affect processing in schizophrenia , 2008, Schizophrenia Research.

[57]  M. Phillips,et al.  A Reversal of the Normal Pattern of Parahippocampal Response to Neutral and Fearful Faces Is Associated with Reality Distortion in Schizophrenia , 2006, Biological Psychiatry.

[58]  Imre Kiss,et al.  Sharing secrets: Oxytocin and trust in schizophrenia , 2009, Social neuroscience.

[59]  E. Walker,et al.  Facial discrimination and emotional recognition in schizophrenia and affective disorders. , 1986, Archives of general psychiatry.

[60]  M. Phillips,et al.  Visual scan paths are abnormal in deluded schizophrenics , 1997, Neuropsychologia.

[61]  P. Pattison,et al.  Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. , 2002, Clinical psychology review.

[62]  R. Gur,et al.  Facial emotion recognition in schizophrenia: intensity effects and error pattern. , 2003, The American journal of psychiatry.

[63]  M. Mandal,et al.  Facial expressions of emotions and schizophrenia: a review. , 1998, Schizophrenia bulletin.

[64]  E. Walker,et al.  Childhood precursors of schizophrenia: facial expressions of emotion. , 1993, The American journal of psychiatry.

[65]  M. Kosmidis,et al.  Impaired emotion perception in schizophrenia: A differential deficit , 2007, Psychiatry Research.

[66]  Philip B. Mitchell,et al.  Oxytocin Increases Gaze to the Eye Region of Human Faces , 2008, Biological Psychiatry.

[67]  D. Amaral,et al.  The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages , 2004, The Journal of Neuroscience.

[68]  N. Franck,et al.  Second-order facial information processing in schizophrenia. , 2008, Neuropsychology.

[69]  F. Karayanidis,et al.  Facial emotion processing in schizophrenia: No evidence for a deficit specific to negative emotions in a differential deficit design , 2006, Psychiatry Research.

[70]  T. Okada,et al.  Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study , 2002, Schizophrenia Research.

[71]  Reactions of chronic schizophrenic patients and college students to facial expressions and geometric forms. , 1962, Journal of clinical psychology.

[72]  J. Kleinman,et al.  Reduced glucocorticoid and estrogen receptor alpha messenger ribonucleic acid levels in the amygdala of patients with major mental illness , 2004, Biological Psychiatry.

[73]  Mark D'Esposito,et al.  Preserved function of the fusiform face area in schizophrenia as revealed by fMRI , 2006, Psychiatry Research: Neuroimaging.

[74]  P. Johnston,et al.  A generalised deficit can account for problems in facial emotion recognition in schizophrenia , 2001, Biological Psychology.

[75]  D. Tsoi,et al.  Is facial emotion recognition impairment in schizophrenia identical for different emotions? A signal detection analysis , 2008, Schizophrenia Research.

[76]  K. Amunts,et al.  Impairment in the specificity of emotion processing in schizophrenia. , 2006, The American journal of psychiatry.

[77]  R. W. Irvin,et al.  Increased amygdala fMRI activation after secretin administration. , 2008, Experimental and clinical psychopharmacology.

[78]  R. Gur,et al.  Brain activation during eye gaze discrimination in stable schizophrenia , 2008, Schizophrenia Research.

[79]  Ellen Leibenluft,et al.  A Developmental Examination of Amygdala Response to Facial Expressions , 2008, Journal of Cognitive Neuroscience.

[80]  M. Webster,et al.  Postnatal alterations in dopaminergic markers in the human prefrontal cortex , 2007, Neuroscience.

[81]  Daniella J. Furman,et al.  Menstrual cycle phase modulates reward-related neural function in women , 2007, Proceedings of the National Academy of Sciences.

[82]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[83]  Stephan Heckers,et al.  Increased medial temporal lobe activation during the passive viewing of emotional and neutral facial expressions in schizophrenia , 2006, Schizophrenia Research.

[84]  Daniel R. Weinberger,et al.  Variants in the estrogen receptor alpha gene and its mRNA contribute to risk for schizophrenia , 2008, Human molecular genetics.

[85]  Stephan Heckers,et al.  Sustained activation of the hippocampus in response to fearful faces in schizophrenia , 2005, Biological Psychiatry.

[86]  U. Fischbacher,et al.  Oxytocin increases trust in humans , 2005, Nature.

[87]  Evian Gordon,et al.  Visual scanpaths in schizophrenia: is there a deficit in face recognition? , 1999, Schizophrenia Research.