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Neuronal correlates of affective theory of mind in schizophrenia out-patients: evidence for a baseline deficit

Published online by Cambridge University Press:  08 January 2010

D. Mier ,
C. Sauer ,
S. Lis ,
C. Esslinger ,
J. Wilhelm ,
B. Gallhofer  and
P. Kirsch
D. Mier*
Affiliation:
Division for Imaging in Psychiatry, Central Institute of Mental Health, Mannheim, Germany Department for Clinical Psychology, Central Institute of Mental Health, Mannheim, Germany
C. Sauer
Affiliation:
Division for Imaging in Psychiatry, Central Institute of Mental Health, Mannheim, Germany
S. Lis
Affiliation:
Centre for Psychiatry and Psychotherapy, University of Giessen, Germany
C. Esslinger
Affiliation:
Division for Imaging in Psychiatry, Central Institute of Mental Health, Mannheim, Germany
J. Wilhelm
Affiliation:
Centre for Psychiatry and Psychotherapy, University of Giessen, Germany
B. Gallhofer
Affiliation:
Centre for Psychiatry and Psychotherapy, University of Giessen, Germany
P. Kirsch
Affiliation:
Division for Imaging in Psychiatry, Central Institute of Mental Health, Mannheim, Germany Mannheim School of Medicine, University of Heidelberg, Germany
*
*Address for correspondence: D. Mier, Division for Imaging in Psychiatry, Central Institute of Mental Health, J5, D-68159Mannheim, Germany. (Email: [email protected])
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Abstract

Background

Schizophrenia out-patients have deficits in affective theory of mind (ToM) but also on more basal levels of social cognition, such as the processing of neutral and emotional expressions. These deficits are associated with changes in brain activation in the amygdala and the superior temporal sulcus (STS). However, until now there have been no studies that examined these different levels of social cognition and their neurobiological underpinnings in patients within one design.

Method

Sixteen medicated schizophrenia out-patients and 16 matched healthy controls were studied with functional magnetic resonance imaging (fMRI) during a social cognition task that allows the investigation of affective ToM (aToM), emotion recognition and the processing of neutral facial expressions.

Results

Patients showed a deficit in emotion recognition and a more prominent deficit in aToM. The performance in aToM and in emotion recognition was correlated in the control group but not in the schizophrenia group. Region-of-interest analysis of functional brain imaging data revealed no difference between groups during aToM, but a hyperactivation in the schizophrenia group in the left amygdala and right STS during emotion recognition and the processing of neutral facial expressions.

Conclusions

The results indicate that schizophrenia out-patients have deficits at several levels of social cognition and provide the first evidence that deficits on higher-order social cognitive processes in schizophrenia may be traced back to an aberrant processing of faces per se.

Keywords

Emotion recognitionfMRIschizophreniasocial cognitiontheory of mind
Type
Original Articles
Information
Psychological Medicine , Volume 40 , Issue 10 , October 2010 , pp. 1607 - 1617
Copyright
Copyright © Cambridge University Press 2010

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References

Addington, J, Addington, D (1998). Facial affect recognition and information processing in schizophrenia and bipolar disorder. Schizophrenia Research 32, 171–181.CrossRefGoogle ScholarPubMed
Andreasen, NC (1983). The Scale for the Assessment of Negative Symptoms (SANS). The University of Iowa: Iowa City.Google Scholar
Andreasen, NC (1984). The Scale for the Assessment of Positive Symptoms (SAPS). The University of Iowa: Iowa City.Google Scholar
Andreasen, NC, Calage, CA, O'Leary, DS (2008). Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophrenia Bulletin 34, 708–719.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Ring, HA, Wheelwright, S, Bullmore, ET, Brammer, MJ, Simmons, A, Williams, SCR (1999). Social intelligence in the normal and autistic brain. European Journal of Neuroscience 11, 1891–1898.Google Scholar
Brothers, L (1990). The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts in Neuroscience 1, 27–51.Google Scholar
Brothers, L, Ring, B (1992). A neuroethological framework for the representation of minds. Journal of Cognitive Neuroscience 4, 107–118.Google Scholar
Brüne, M (2003). Social cognition and behaviour in schizophrenia. In The Social Brain: Evolution and Pathology (ed. Brüne, M., Ribbert, H. and Schiefenhövel, W.), pp. 277–313. John Wiley & Sons: Chichester.CrossRefGoogle Scholar
Brüne, M (2005). Emotion recognition, ‘theory of mind’, and social behavior in schizophrenia. Psychiatry Research 133, 135–147.CrossRefGoogle ScholarPubMed
Brüne, M, Lissek, S, Fuchs, N, Witthaus, H, Peters, S, Nicolas, V, Juckel, G, Tegenthoff, M (2008). An fMRI study of theory of mind in schizophrenic patients with ‘passivity’ symptoms. Neuropsychologia 46, 1992–2001.Google Scholar
Brunet, E, Sarfati, Y, Hardy-Bayle, M, Decety, J (2003). Abnormalities of brain function during a nonverbal theory of mind task in schizophrenia. Neuropsychologia 21, 1574–1582.Google Scholar
Callicott, JH, Mattay, VS, Verchinski, BA, Marenco, S, Egan, MF, Weinberger, D (2003). Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. American Journal of Psychiatry 160, 2209–2215.CrossRefGoogle ScholarPubMed
Castelli, F, Happé, F, Frith, U, Frith, C (2000). Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. NeuroImage 12, 314–325.Google Scholar
Corcoran, R, Cahill, C, Frith, CD (1997). The appreciation of visual jokes in people with schizophrenia: a study of ‘mentalizing’ ability. Schizophrenia Research 24, 319–327.Google Scholar
Doody, GA, Götz, M, Johnstone, EC, Frith, C, Cunningham Owens, DG (1998). Theory of mind and psychoses. Psychological Medicine 28, 397–405.Google Scholar
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.Google Scholar
Fahim, C, Stip, E, Mancini-Marie, A, Mensour, B, Boulay, JC, Leroux, J, Beaudoin, G, Bourgoin, P, Beauregard, M (2005). Brain activity during emotional negative pictures in schizophrenia with and without flat affect: an fMRI study. Psychiatry Research: Neuroimaging 140, 1–15.CrossRefGoogle ScholarPubMed
Fakra, E, Salgado-Pineda, P, Delaveau, P, Hariri, AR, Blin, O (2008). Neural bases of different cognitive strategies for facial affect processing in schizophrenia. Schizophrenia Research 100, 191–205.CrossRefGoogle ScholarPubMed
Frith, CD (1992). The Cognitive Neuropsychology of Schizophrenia. Lawrence Erlbaum Associates Inc.: Hillsdale, NJ.Google Scholar
Gallwitz, A, Lehrl, S, Blaha, L (1992). Short Test for General Intelligence [in German]. Hogrefe: Göttingen.Google Scholar
Gregory, C, Lough, S, Stone, V, Erzinclioglu, S, Martin, L, Baron-Cohen, S, Hodges, JR (2002). Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer's disease: theoretical and practical implications. Brain 125, 752–764.Google Scholar
Greig, TC, Bryson, BJ, Bell, MD (2004). Theory of mind performance in schizophrenia: diagnostic, symptom, and neuropsychological correlates. Journal of Nervous and Mental Disease 192, 12–18.Google Scholar
Grèzes, J, Berthoz, S, Passingham, RE (2006). Amygdala activation when one is the target of deceit: did he lie to you or to someone else? NeuroImage 30, 601–608.CrossRefGoogle Scholar
Gur, RE, McGrath, C, Chan, RM, Schroeder, L, Turner, T, Turetsky, BI, Kohler, C, Alsop, D, Maldajian, J, Ragland, JD, Gur, RC (2002). An fMRI study of facial emotion processing in patients with schizophrenia. American Journal of Psychiatry 159, 1992–1999.Google Scholar
Hempel, A, Hempel, E, Schönknecht, P, Stippich, C, Schröder, J (2003). Impairment in basal limbic function in schizophrenia during affect recognition. Psychiatry Research: Neuroimaging 122, 115–124.CrossRefGoogle ScholarPubMed
Herold, R, Tényi, T, Lénárd, K, Trixler, M (2002). Theory of mind deficit in people with schizophrenia during remission. Psychological Medicine 32, 1125–1129.CrossRefGoogle ScholarPubMed
Holt, DJ, Kunkel, L, Weiss, AP, Goff, DC, Wright, CI, Shin, LM, Rauch, SL, Hootnick, J, Heckers, S (2006). Increased medial temporal lobe activation during the passive viewing of emotional and neutral facial expressions in schizophrenia. Schizophrenia Research 82, 153–162.CrossRefGoogle ScholarPubMed
Horan, WP, Nuechterlein, KH, Wynn, JK, Lee, J, Castelli, F, Green, MF (2009). Disturbances in the spontaneous attribution of social meaning in schizophrenia. Psychological Medicine 39, 635–643.CrossRefGoogle ScholarPubMed
Inoue, Y, Yamada, K, Hirano, M, Shinohara, M, Tamaoki, T, Iguchi, H, Tonooka, Y, Kanba, S (2006). Impairment of theory of mind in patients in remission following first episode of schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 256, 326–328.CrossRefGoogle ScholarPubMed
Janssen, I, Krabbendam, L, Jolles, J, van Os, J (2003). Alterations in theory of mind in patients with schizophrenia and non-psychotic relatives. Acta Psychiatrica Scandinavica 108, 110–117.Google Scholar
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
Kelemen, O, Kéri, S, Must, A, Benedek, G, Janka, Z (2005). No evidence for impaired ‘theory of mind’ in unaffected first-degree relatives of schizophrenia patients. Acta Psychiatrica Scandinavica 110, 146–149.CrossRefGoogle Scholar
Kern, RS, Green, MF, Fiske, AP, Kee, KS, Lee, J, Sergi, MJ, Horan, WP, Subotnik, KL, Sugar, CA, Nuechterlein, KH (2009). Theory of mind deficits for processing counterfactual information in persons with chronic schizophrenia. Psychological Medicine 39, 645–654.Google Scholar
Kington, JM, Jones, LA, Watt, AA, Hopkins, EJ, Williams, J (2000). Impaired eye expression recognition in schizophrenia. Journal of Psychiatric Research 34, 341–347.CrossRefGoogle ScholarPubMed
Kosaka, K, Omori, M, Murata, T, Iidaka, T, Yamada, H, Okada, T, Takahashi, T, Sadato, N, Itoh, H, Yonekura, Y, Wada, Y (2002). Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study. Schizophrenia Research 57, 87–95.Google Scholar
LeDoux, J (2007). The amygdala. Current Biology 17, R868–R874.CrossRefGoogle ScholarPubMed
Lehrl, S (1977). Multiple-choice Vocabulary Test [in German]. Straube: Erlangen.Google Scholar
Li, H, Chan, RCK, McAlonan, GM, Gong, Q (2009). Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophrenia Bulletin. Published online: 30 March 2009. doi:10.1093/schbul/sbn190.Google Scholar
Liberzon, I, Phan, KL, Decker, LR, Taylor, SF (2003). Extended amygdala and emotional salience: a PET activation study of positive and negative affect. Neuropsychopharmacology 28, 726–733.CrossRefGoogle ScholarPubMed
López-Ibor, JJ, López-Ibor, M, Méndez, M, Morón, M, Ortiz-Terán, L, Fernandez, A, Diaz-Marsá, M, Ortiz, T (2008). The perception of emotion free faces in schizophrenia: a magneto-encephalography study. Schizophrenia Research 98, 278–286.CrossRefGoogle ScholarPubMed
Loughland, CM, Williams, LM, Gordon, E (2002). Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample. Schizophrenia Research 55, 159–170.Google Scholar
Mandal, MK, Pandey, R, Prasad, AB (1998). Facial expression of emotions and schizophrenia: a review. Schizophrenia Bulletin 24, 399–412.Google Scholar
Manor, BR, Gordon, E, Williams, LM, Rennie, CJ, Bahramali, H, Latimer, CR, Barry, RJ, Meares, RA (1999). Eye movements reflect impaired face processing in patients with schizophrenia. Biological Psychiatry 46, 963–969.CrossRefGoogle ScholarPubMed
Margraf, J (1994). Short Diagnostic Structured Interview for Mental Disorders: Mini-DIPS [in German]. Springer: Berlin.Google Scholar
Mizrah, R, Bagby, RM, Zipursky, RB, Kapur, S (2005). How antipsychotics work: the patients' perspective. Progress in Neuro-Psychopharmacology and Biological Psychiatry 29, 859–864.CrossRefGoogle Scholar
Mo, S, Su, Y, Chan, RCK, Liu, J (2008). Comprehension of metaphor and irony in schizophrenia during remission: the role of theory of mind and IQ. Psychiatry Research 157, 21–29.CrossRefGoogle ScholarPubMed
Pelphrey, KA, Morris, JP, McCarty, G (2004). Grasping the intentions of others: the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. Journal of Cognitive Neuroscience 16, 1706–1716.CrossRefGoogle ScholarPubMed
Penn, DL, Combs, DR, Ritchie, M, Franzis, J, Cassisi, J, Morris, S, Townsend, M (2000). Emotion recognition in schizophrenia: further investigation of generalized versus specific deficit models. Journal of Abnormal Psychology 109, 512–516.Google Scholar
Penn, DL, Sanna, LJ, Roberts, DL (2008). Social cognition in schizophrenia: an overview. Schizophrenia Bulletin 34, 408–411.CrossRefGoogle ScholarPubMed
Pinkham, AE, Gur, RE, Gur, RC (2007). Affect recognition deficits in schizophrenia: neural substrates and psychopharmacological implications. Expert Review of Neurotherapeutics 7, 807–816.CrossRefGoogle ScholarPubMed
Pinkham, AE, Hopfinger, JB, Pelphrey, KA, Piven, J, Penn, DL (2008). Neural bases for impaired theory of mind in schizophrenia and autism spectrum disorder. Schizophrenia Research 99, 164–175.CrossRefGoogle Scholar
Pinkham, AE, Penn, DL, Perkins, DO, Lieberman, J (2003). Implications for the neural basis of social cognition for the study of schizophrenia. American Journal of Psychiatry 160, 815–824.CrossRefGoogle Scholar
Premack, D, Woodruff, G (1978). Does the chimpanzee have a theory of mind? Behavioral and Brain Sciences 4, 515–526.CrossRefGoogle Scholar
Russell, TA, Rubia, KR, Bullmore, ET, Soni, W, Suckling, J, Brammer, MJ, Simmons, A, Williams, SCR, Sharma, T (2000). Exploring the social brain in schizophrenia. Left prefrontal underactivation during mental state attribution. American Journal of Psychiatry 157, 2040–2042.Google Scholar
Saxe, R, Xiao, D-K, Kovacs, G, Perrett, DI, Kahnwisher, N (2004). A region of right posterior superior temporal sulcus responds to observed intentional actions. Neuropsychologia 42, 1435–1446.CrossRefGoogle ScholarPubMed
Seiferth, NY, Pauly, K, Habel, U, Kellermann, T, Shah, NJ, Ruhrmann, S, Klosterkötter, J, Schneider, F, Kircher, T (2008). Increased neural response related to neutral faces in individuals at risk for psychosis. NeuroImage 40, 289–297.CrossRefGoogle ScholarPubMed
Shamay-Tsoory, SG, Shur, S, Barcai-Goodman, L, Medlovich, S, Harari, H, Levkovitz, Y (2007). Dissociation of cognitive from affective components of theory of mind in schizophrenia. Psychiatry Research 149, 11–23.Google Scholar
Shamay-Tsoory, SG, Tomer, R, Aharon-Peretz, J (2005). The neuroanatomical basis of understanding sarcasm and its relationship to social cognition. Neuropsychology 19, 288–300.CrossRefGoogle ScholarPubMed
Surguladze, S, Russell, T, Kucharska-Pietura, K, Travis, MJ, Giampietro, V, David, AS, Phillips, ML (2006). A reversal of the normal pattern of parahippocampal response to neutral and fearful faces is associated with reality distortion in schizophrenia. Biological Psychiatry 60, 423–421.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.Google Scholar
Walter, B, Blecker, C, Kirsch, P, Sammer, G, Schienle, A, Stark, R, Vaitl, D (2003). MARINA: an easy to use tool for the creation of MAsks for Region of INterest Analyses [Abstract]. Presented at the 9th International Conference on Functional Mapping of the Human Brain, 19–22 June 2003, New York, NY. (Available on CD-Rom in NeuroImage vol. 19, no. 2.)Google Scholar
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