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Emotional face processing and flat affect in schizophrenia: functional and structural neural correlates

Published online by Cambridge University Press:  02 February 2011

M. Lepage ,
K. Sergerie ,
A. Benoit ,
Y. Czechowska ,
E. Dickie  and
J. L. Armony
M. Lepage*
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
K. Sergerie
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
A. Benoit
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
Y. Czechowska
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
E. Dickie
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
J. L. Armony
Affiliation:
Douglas Mental Health University Institute, Department of Psychiatry, McGill University, Verdun, Québec, Canada
*
*Address for correspondence: M. Lepage, Ph.D., Douglas Mental Health University Institute, 6875 LaSalle Boulevard, Verdun, Québec, H4H 1R3, Canada. (Email: [email protected])
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Abstract

Background

There is a general consensus in the literature that schizophrenia causes difficulties with facial emotion perception and discrimination. Functional brain imaging studies have observed reduced limbic activity during facial emotion perception but few studies have examined the relation to flat affect severity.

Method

A total of 26 people with schizophrenia and 26 healthy controls took part in this event-related functional magnetic resonance imaging study. Sad, happy and neutral faces were presented in a pseudo-random order and participants indicated the gender of the face presented. Manual segmentation of the amygdala was performed on a structural T1 image.

Results

Both the schizophrenia group and the healthy control group rated the emotional valence of facial expressions similarly. Both groups exhibited increased brain activity during the perception of emotional faces relative to neutral ones in multiple brain regions, including multiple prefrontal regions bilaterally, the right amygdala, right cingulate cortex and cuneus. Group comparisons, however, revealed increased activity in the healthy group in the anterior cingulate, right parahippocampal gyrus and multiple visual areas. In schizophrenia, the severity of flat affect correlated significantly with neural activity in several brain areas including the amygdala and parahippocampal region bilaterally.

Conclusions

These results suggest that many of the brain regions involved in emotional face perception, including the amygdala, are equally recruited in both schizophrenia and controls, but flat affect can also moderate activity in some other brain regions, notably in the left amygdala and parahippocampal gyrus bilaterally. There were no significant group differences in the volume of the amygdala.

Keywords

Amygdala volumetryblunted affectfunctional magnetic resonance imagingnegative symptoms
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 9 , September 2011 , pp. 1833 - 1844
Copyright
Copyright © Cambridge University Press 2011

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References

Addington, J, Saeedi, H, Addington, D (2006). Facial affect recognition: a mediator between cognitive and social functioning in psychosis? Schizophrenia Research 85, 142–150.CrossRefGoogle ScholarPubMed
Adolphs, R (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology 12, 169–177.CrossRefGoogle ScholarPubMed
Aleman, A, Kahn, RS (2005). Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Progress in Neurobiology 77, 283–298.Google ScholarPubMed
Andreasen, N (1984 a). Scale for the Assessment of Positive Symptoms (SAPS). Department of Psychiatry, College of Medicine, The University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC (1984 b). Modified Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City, IA.Google Scholar
Berretta, S, Pantazopoulos, H, Lange, N (2007). Neuron numbers and volume of the amygdala in subjects diagnosed with bipolar disorder or schizophrenia. Biological Psychiatry 62, 884–893.CrossRefGoogle ScholarPubMed
Chance, SA, Esiri, MM, Crow, TJ (2002). Amygdala volume in schizophrenia: post-mortem study and review of magnetic resonance imaging findings. British Journal of Psychiatry 180, 331–338.CrossRefGoogle ScholarPubMed
Chen, Y, Norton, D, Ongur, D, Heckers, S (2008). Inefficient face detection in schizophrenia. Schizophrenia Bulletin 34, 367–374.CrossRefGoogle ScholarPubMed
Edwards, J, Jackson, HJ, Pattison, PE (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review 22, 789–832.CrossRefGoogle ScholarPubMed
Edwards, J, Pattison, PE, Jackson, HJ, Wales, RJ (2001). Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophrenia Research 48, 235–253.CrossRefGoogle ScholarPubMed
Fahim, C, Stip, E, Mancini-Marie, A, Mensour, B, Boulay, LJ, Leroux, JM, Beaudoin, G, Bourgouin, P, Beauregard, M (2005). Brain activity during emotionally negative pictures in schizophrenia with and without flat affect: an fMRI study. Psychiatry Research 140, 1–15.CrossRefGoogle ScholarPubMed
Foussias, G, Remington, G (2008). Negative symptoms in schizophrenia: avolition and Occam's razor. Schizophrenia Bulletin 36, 359–369.CrossRefGoogle ScholarPubMed
Gur, RE, Cowell, PE, Latshaw, A, Turetsky, BI, Grossman, RI, Arnold, SE, Bilker, WB, Gur, RC (2000). Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Archives of General Psychiatry 57, 761–768.CrossRefGoogle ScholarPubMed
Gur, RE, Kohler, CG, Ragland, JD, Siegel, SJ, Lesko, K, Bilker, WB, Gur, RC (2006). Flat affect in schizophrenia: relation to emotion processing and neurocognitive measures. Schizophrenia Bulletin 32, 279–287.CrossRefGoogle ScholarPubMed
Gur, RE, Loughead, J, Kohler, CG, Elliott, MA, Lesko, K, Ruparel, K, Wolf, DH, Bilker, WB, Gur, RC (2007). Limbic activation associated with misidentification of fearful faces and flat affect in schizophrenia. Archives of General Psychiatry 64, 1356–1366.CrossRefGoogle ScholarPubMed
Hall, J, Whalley, HC, McKirdy, JW, Romaniuk, L, McGonigle, D, McIntosh, AM, Baig, BJ, Gountouna, VE, Job, DE, Donaldson, DI, Sprengelmeyer, R, Young, AW, Johnstone, EC, Lawrie, SM (2008). Overactivation of fear systems to neutral faces in schizophrenia. Biological Psychiatry 64, 70–73.CrossRefGoogle ScholarPubMed
Harvey, PO, Bodnar, M, Sergerie, K, Armony, J, Lepage, M (2009). Relation between emotional face memory and social anhedonia in schizophrenia. Journal of Psychiatry and Neuroscience 34, 102–110.Google ScholarPubMed
Johnston, PJ, Devir, H, Karayanidis, F (2006). Facial emotion processing in schizophrenia: no evidence for a deficit specific to negative emotions in a differential deficit design. Psychiatry Research 143, 51–61.CrossRefGoogle Scholar
Johnston, PJ, Stojanov, W, Devir, H, Schall, U (2005). Functional MRI of facial emotion recognition deficits in schizophrenia and their electrophysiological correlates. European Journal of Neuroscience 22, 1221–1232.CrossRefGoogle ScholarPubMed
Josephs, O, Turner, R, Friston, K (1997). Event-relatd fMRI. Human Brain Mapping 5, 243–248.3.0.CO;2-3>CrossRefGoogle Scholar
Kohler, CG, Turner, TH, Bilker, WB, Brensinger, CM, Siegel, SJ, Kanes, SJ, Gur, RE, Gur, RC (2003). Facial emotion recognition in schizophrenia: intensity effects and error pattern. American Journal of Psychiatry 160, 1768–1774.CrossRefGoogle ScholarPubMed
Kohler, CG, Walker, JB, Martin, EA, Healey, KM, Moberg, PJ (2010). Facial emotion perception in schizophrenia: a meta-analytic review. Schizophrenia Bulletin 36, 1009–1019.CrossRefGoogle ScholarPubMed
Lacerda, AL, Hardan, AY, Yorbik, O, Vemulapalli, M, Prasad, KM, Keshavan, MS (2007). Morphology of the orbitofrontal cortex in first-episode schizophrenia: relationship with negative symptomatology. Progress in Neuro-Psychopharmacology and Biological Psychiatry 31, 510–516.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN (1995). International Affective Picture System (IAPS): Technical Manual and Affective Ratings. NIMH Center for the Study of Emotion and Attention: Gainesville, FL.Google Scholar
Lawrie, SM, Whalley, HC, Job, DE, Johnstone, EC (2003). Structural and functional abnormalities of the amygdala in schizophrenia. Annals of the New York Academy of Sciences 985, 445–460.CrossRefGoogle ScholarPubMed
Li, H, Chan, RC, McAlonan, GM, Gong, QY (2009). Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophrenia Bulletin 36, 1029–1039.CrossRefGoogle ScholarPubMed
Mandal, M, Pandey, R, Prasad, A (1998). Facial expressions of emotions and schizophrenia: a review. Schizophrenia Bulletin 24, 399–412.CrossRefGoogle ScholarPubMed
Merens, W, Willem, Van der Does AJ, Spinhoven, P (2007). The effects of serotonin manipulations on emotional information processing and mood. Journal of Affective Disorders 103, 43–62.CrossRefGoogle ScholarPubMed
Michalopoulou, PG, Surguladze, S, Morley, LA, Giampietro, VP, Murray, RM, Shergill, SS (2008). Facial fear processing and psychotic symptoms in schizophrenia: functional magnetic resonance imaging study. British Journal of Psychiatry 192, 191–196.CrossRefGoogle ScholarPubMed
Nesvag, R, Saetre, P, Lawyer, G, Jonsson, EG, Agartz, I (2009). The relationship between symptom severity and regional cortical and grey matter volumes in schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry 33, 482–490.CrossRefGoogle ScholarPubMed
Nichols, T, Brett, M, Andersson, J, Wager, T, Poline, JB (2005). Valid conjunction inference with the minimum statistic. Neuroimage 25, 653–660.CrossRefGoogle ScholarPubMed
Norbury, R, Taylor, MJ, Selvaraj, S, Murphy, SE, Harmer, CJ, Cowen, PJ (2009). Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacology 206, 197–204.CrossRefGoogle ScholarPubMed
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16, 331–348.CrossRefGoogle ScholarPubMed
Pruessner, JC, Li, LM, Serles, W, Pruessner, M, Collins, DL, Kabani, N, Lupien, S, Evans, AC (2000). Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cerebral Cortex 10, 433–442.CrossRefGoogle ScholarPubMed
Sergerie, K, Armony, JL, Menear, M, Sutton, H, Lepage, M (2010). Influence of emotional expression on memory recognition bias in schizophrenia as revealed by fMRI. Schizophrenia Bulletin 36, 800–810.CrossRefGoogle ScholarPubMed
Sergerie, K, Chochol, C, Armony, JL (2008). The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews 32, 811–830.CrossRefGoogle ScholarPubMed
Sergerie, K, Lepage, M, Armony, JL (2005). A face to remember: emotional expression modulates prefrontal activity during memory formation. Neuroimage 24, 580–585.CrossRefGoogle ScholarPubMed
Sergerie, K, Lepage, M, Armony, JL (2006). A process-specific functional dissociation of the amygdala in emotional memory. Journal of Cognitive Neuroscience 18, 1359–1367.CrossRefGoogle ScholarPubMed
Sergerie, K, Lepage, M, Armony, JL (2007). Influence of emotional expression on memory recognition bias: a functional magnetic resonance imaging study. Biological Psychiatry 62, 1126–1133.CrossRefGoogle Scholar
Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW (2001). A review of MRI findings in schizophrenia. Schizophrenia Research 49, 1–52.CrossRefGoogle ScholarPubMed
Shin, YW, Na, MH, Ha, TH, Kang, DH, Yoo, SY, Kwon, JS (2008). Dysfunction in configural face processing in patients with schizophrenia. Schizophrenia Bulletin 34, 538–543.CrossRefGoogle ScholarPubMed
Tanskanen, P, Veijola, JM, Piippo, UK, Haapea, M, Miettunen, JA, Pyhtinen, J, Bullmore, ET, Jones, PB, Isohanni, MK (2005). Hippocampus and amygdala volumes in schizophrenia and other psychoses in the Northern Finland 1966 birth cohort. Schizophrenia Research 75, 283–294.CrossRefGoogle ScholarPubMed
Tranter, R, Bell, D, Gutting, P, Harmer, C, Healy, D, Anderson, IM (2009). The effect of serotonergic and noradrenergic antidepressants on face emotion processing in depressed patients. Journal of Affective Disorders 118, 87–93.CrossRefGoogle ScholarPubMed
Van't Wout, M, van Dijke, A, Aleman, A, Kessels, RP, Pijpers, W, Kahn, RS (2007). Fearful faces in schizophrenia: the relationship between patient characteristics and facial affect recognition. Journal of Nervous and Mental Disease 195, 758–764.CrossRefGoogle ScholarPubMed
Williams, LM, Das, P, Liddell, BJ, Olivieri, G, Peduto, AS, David, AS, Gordon, E, Harris, AW (2007). Fronto-limbic and autonomic disjunctions to negative emotion distinguish schizophrenia subtypes. Psychiatry Research 155, 29–44.CrossRefGoogle ScholarPubMed