Aberrant activity and connectivity of the posterior superior temporal sulcus during social cognition in schizophrenia

Springer Science and Business Media LLC - Tập 267 - Trang 597-610 - 2016
Daniela Mier1, Sarah Eisenacher2, Franziska Rausch2, Susanne Englisch2, Martin Fungisai Gerchen1, Vera Zamoscik1, Andreas Meyer-Lindenberg2, Mathias Zink2, Peter Kirsch1
1Department of Clinical Psychology, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany
2Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany

Tóm tắt

Schizophrenia is associated with significant impairments in social cognition. These impairments have been shown to go along with altered activation of the posterior superior temporal sulcus (pSTS). However, studies that investigate connectivity of pSTS during social cognition in schizophrenia are sparse. Twenty-two patients with schizophrenia and 22 matched healthy controls completed a social-cognitive task for functional magnetic resonance imaging that allows the investigation of affective Theory of Mind (ToM), emotion recognition and the processing of neutral facial expressions. Moreover, a resting-state measurement was taken. Patients with schizophrenia performed worse in the social-cognitive task (main effect of group). In addition, a group by social-cognitive processing interaction was revealed for activity, as well as for connectivity during the social-cognitive task, i.e., patients with schizophrenia showed hyperactivity of right pSTS during neutral face processing, but hypoactivity during emotion recognition and affective ToM. In addition, hypoconnectivity between right and left pSTS was revealed for affective ToM, but not for neutral face processing or emotion recognition. No group differences in connectivity from right to left pSTS occurred during resting state. This pattern of aberrant activity and connectivity of the right pSTS during social cognition might form the basis of false-positive perceptions of emotions and intentions and could contribute to the emergence and sustainment of delusions.

Tài liệu tham khảo

Green MF, Bearden CE, Cannon TD, Fiske AP, Hellemann GS, Horan WP, Kee K, Kern RS, Lee J, Sergi MJ, Subotnik KL, Sugar CA, Ventura J, Yee CM, Nuechterlein KH (2012) Social cognition in schizophrenia, part 1: performance across phase of illness. Schizophr Bull 38(4):854–864. doi:10.1093/schbul/sbq171 Horan WP, Green MF, DeGroot M, Fiske A, Hellemann G, Kee K, Kern RS, Lee J, Sergi MJ, Subotnik KL, Sugar CA, Ventura J, Nuechterlein KH (2012) Social cognition in schizophrenia, part 2: 12-month stability and prediction of functional outcome in first-episode patients. Schizophr Bull 38(4):865–872. doi:10.1093/schbul/sbr001 Brothers L (1990) The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts Neurosci 1(1):27–51 Mier D, Sauer C, Lis S, Esslinger C, Wilhelm J, Gallhofer B, Kirsch P (2010) Neuronal correlates of affective theory of mind in schizophrenia out-patients: evidence for a baseline deficit. Psychol Med 40(10):1607–1617. doi:10.1017/S0033291709992133 Turetsky BI, Kohler CG, Indersmitten T, Bhati MT, Charbonnier D, Gur RC (2007) Facial emotion recognition in schizophrenia: when and why does it go awry? Schizophr Res 94(1–3):253–263. doi:10.1016/j.schres.2007.05.001 Edwards J, Jackson HJ, Pattison PE (2002) Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clin Psychol Rev J 22(6):789–832 Brune M (2005) Emotion recognition, ‘theory of mind’, and social behavior in schizophrenia. Psychiatry Res 133(2–3):135–147. doi:10.1016/j.psychres.2004.10.007 Premack D, Woodruff G (1978) Does the chimpanzee have a theory of mind? Behav Brain Sci 4:515–526 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 Res 149(1):11–23 Mehta UM, Thirthalli J, Naveen Kumar C, Keshav Kumar J, Keshavan MS, Gangadhar BN (2013) Schizophrenia patients experience substantial social cognition deficits across multiple domains in remission. Asian J Psychiatry 6(4):324–329. doi:10.1016/j.ajp.2013.02.001 Amminger GP, Schafer MR, Papageorgiou K, Klier CM, Schlogelhofer M, Mossaheb N, Werneck-Rohrer S, Nelson B, McGorry PD (2012) Emotion recognition in individuals at clinical high-risk for schizophrenia. Schizophr Bull 38(5):1030–1039. doi:10.1093/schbul/sbr015 Eack SM, Mermon DE, Montrose DM, Miewald J, Gur RE, Gur RC, Sweeney JA, Keshavan MS (2010) Social cognition deficits among individuals at familial high risk for schizophrenia. Schizophr Bull 36(6):1081–1088. doi:10.1093/schbul/sbp026 Meyer-Lindenberg A (2010) Intermediate or brainless phenotypes for psychiatric research? Psychol Med 40(7):1057–1062 Meyer-Lindenberg A, Weinberger DR (2006) Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev Neurosci 7(10):818–827. doi:10.1038/nrn1993 Derntl B, Habel U (2011) Deficits in social cognition: a marker for psychiatric disorders? Eur Arch Psychiatry Clin Neurosci 261(Suppl 2):S145–S149. doi:10.1007/s00406-011-0244-0 Li H, Chan RC, McAlonan GM, Gong QY (2010) Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophr Bull 36(5):1029–1039. doi:10.1093/schbul/sbn190 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. Biol Psychiatry 64(1):70–73. doi:10.1016/j.biopsych.2007.12.014 Mier D, Lis S, Zygrodnik K, Sauer C, Ulferts J, Gallhofer B, Kirsch P (2014) Evidence for altered amygdala activation in schizophrenia in an adaptive emotion recognition task. Psychiatry Res 221(3):195–203. doi:10.1016/j.pscychresns.2013.12.001 Anticevic A, Van Snellenberg JX, Cohen RE, Repovs G, Dowd EC, Barch DM (2012) Amygdala recruitment in schizophrenia in response to aversive emotional material: a meta-analysis of neuroimaging studies. Schizophr Bull 38(3):608–621. doi:10.1093/schbul/sbq131 Hooker CI, Bruce L, Fisher M, Verosky SC, Miyakawa A, D’Esposito M, Vinogradov S (2013) The influence of combined cognitive plus social-cognitive training on amygdala response during face emotion recognition in schizophrenia. Psychiatry Res 213(2):99–107. doi:10.1016/j.pscychresns.2013.04.001 Hein G, Knight RT (2008) Superior temporal sulcus—it’s my area: or is it? J Cogn Neurosci 20(12):2125–2136. doi:10.1162/jocn.2008.20148 Backasch B, Straube B, Pyka M, Klohn-Saghatolislam F, Muller MJ, Kircher TT, Leube DT (2013) Hyperintentionality during automatic perception of naturalistic cooperative behavior in patients with schizophrenia. Soc Neurosci 8(5):489–504. doi:10.1080/17470919.2013.820666 Pinkham AE, Hopfinger JB, Pelphrey KA, Piven J, Penn DL (2008) Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders. Schizophr Res 99(1–3):164–175. doi:10.1016/j.schres.2007.10.024 Rasetti R, Mattay VS, Wiedholz LM, Kolachana BS, Hariri AR, Callicott JH, Meyer-Lindenberg A, Weinberger DR (2009) Evidence that altered amygdala activity in schizophrenia is related to clinical state and not genetic risk. Am J Psychiatry 166(2):216–225. doi:10.1176/appi.ajp.2008.08020261 Walter H, Schnell K, Erk S, Arnold C, Kirsch P, Esslinger C, Mier D, Schmitgen MM, Rietschel M, Witt SH, Nothen MM, Cichon S, Meyer-Lindenberg A (2011) Effects of a genome-wide supported psychosis risk variant on neural activation during a theory-of-mind task. Mol Psychiatry 16(4):462–470. doi:10.1038/mp.2010.18 Wible CG (2012) Hippocampal temporal-parietal junction interaction in the production of psychotic symptoms: a framework for understanding the schizophrenic syndrome. Front Hum Neurosci 6:180. doi:10.3389/fnhum.2012.00180 Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356. doi:10.1523/JNEUROSCI.5587-06.2007 Weiland BJ, Sabbineni A, Calhoun VD, Welsh RC, Hutchison KE (2014) Reduced executive and default network functional connectivity in cigarette smokers. Hum Brain Mapp. doi:10.1002/hbm.22672 Crossley NA, Mechelli A, Fusar-Poli P, Broome MR, Matthiasson P, Johns LC, Bramon E, Valmaggia L, Williams SC, McGuire PK (2009) Superior temporal lobe dysfunction and frontotemporal dysconnectivity in subjects at risk of psychosis and in first-episode psychosis. Hum Brain Mapp 30(12):4129–4137. doi:10.1002/hbm.20834 Ciaramidaro A, Bolte S, Schlitt S, Hainz D, Poustka F, Weber B, Bara BG, Freitag C, Walter H (2015) Schizophrenia and autism as contrasting minds: neural evidence for the hypo-hyper-intentionality hypothesis. Schizophr Bull 41(1):171–179. doi:10.1093/schbul/sbu124 Straube B, Green A, Sass K, Kircher T (2014) Superior temporal sulcus disconnectivity during processing of metaphoric gestures in schizophrenia. Schizophr Bull 40(4):936–944. doi:10.1093/schbul/sbt110 Anticevic A, Repovs G, Barch DM (2012) Emotion effects on attention, amygdala activation, and functional connectivity in schizophrenia. Schizophr Bull 38(5):967–980. doi:10.1093/schbul/sbq168 Mukherjee P, Whalley HC, McKirdy JW, Sprengelmeyer R, Young AW, McIntosh AM, Lawrie SM, Hall J (2014) Altered amygdala connectivity within the social brain in schizophrenia. Schizophr Bull 40(1):152–160. doi:10.1093/schbul/sbt086 Adolphs R (2009) The social brain: neural basis of social knowledge. Annu Rev Psychol 60:693–716. doi:10.1146/annurev.psych.60.110707.163514 Blakemore SJ (2008) The social brain in adolescence. Nat Rev Neurosci 9(4):267–277. doi:10.1038/nrn2353 Frith CD, Corcoran R (1996) Exploring ‘theory of mind’ in people with schizophrenia. Psychol Med 26(3):521–530 Lee SM, Gao T, McCarthy G (2014) Attributing intentions to random motion engages the posterior superior temporal sulcus. Soc Cogn Affect Neurosci 9(1):81–87. doi:10.1093/scan/nss110 Mier D, Lis S, Neuthe K, Sauer C, Esslinger C, Gallhofer B, Kirsch P (2010) The involvement of emotion recognition in affective theory of mind. Psychophysiology 47(6):1028–1039. doi:10.1111/j.1469-8986.2010.01031.x Rausch F, Mier D, Eifler S, Esslinger C, Schilling C, Schirmbeck F, Englisch S, Meyer-Lindenberg A, Kirsch P, Zink M (2014) Reduced activation in ventral striatum and ventral tegmental area during probabilistic decision-making in schizophrenia. Schizophr Res 156(2–3):143–149. doi:10.1016/j.schres.2014.04.020 Rausch F, Mier D, Eifler S, Fenske S, Schirmbeck F, Englisch S, Schilling C, Meyer-Lindenberg A, Kirsch P, Zink M (2015) Reduced activation in the ventral striatum during probabilistic decision-making in patients in an at-risk mental state. J Psychiatry Neurosci JPN 40(3):163–173 American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders DSM-IV-TR fourth edition (text revision) Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13(2):261–276 Andreasen NC (1989) The Scale for the Assessment of Negative Symptoms (SANS): conceptual and theoretical foundations. Br J Psychiatry (7):49–58 Patrick DL, Burns T, Morosini P, Rothman M, Gagnon DD, Wild D, Adriaenssen I (2009) Reliability, validity and ability to detect change of the clinician-rated Personal and Social Performance scale in patients with acute symptoms of schizophrenia. Curr Med Res Opin 25(2):325–338. doi:10.1185/03007990802611919 Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33 (quiz 34–57) Lehrl S (2005) Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Spitta Verlag, Bailingen, Germany Kern RS, Gold JM, Dickinson D, Green MF, Nuechterlein KH, Baade LE, Keefe RS, Mesholam-Gately RI, Seidman LJ, Lee C, Sugar CA, Marder SR (2011) The MCCB impairment profile for schizophrenia outpatients: results from the MATRICS psychometric and standardization study. Schizophr Res 126(1–3):124–131. doi:10.1016/j.schres.2010.11.008 Nuechterlein KH, Green MF, Kern RS, Baade LE, Barch DM, Cohen JD, Essock S, Fenton WS, Frese FJ 3rd, Gold JM, Goldberg T, Heaton RK, Keefe RS, Kraemer H, Mesholam-Gately R, Seidman LJ, Stover E, Weinberger DR, Young AS, Zalcman S, Marder SR (2008) The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. Am J Psychiatry 165(2):203–213. doi:10.1176/appi.ajp.2007.07010042 Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M (1997) Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry 38(7):813–822 Tran US, Laireiter AR, Schmitt DP, Neuner C, Leibetseder M, Szente-Voracek SL, Voracek M (2013) Factorial structure and convergent and discriminant validity of the E (Empathy) scale. Psychol Rep 113(2):441–463. doi:10.2466/03.02.PR0.113x20z9 Balogh N, Egerhazi A, Berecz R, Csukly G (2014) Investigating the state-like and trait-like characters of social cognition in schizophrenia: a short term follow-up study. Schizophr Res 159(2–3):499–505. doi:10.1016/j.schres.2014.08.027 Csukly G, Polgar P, Tombor L, Benkovits J, Rethelyi J (2014) Theory of mind impairments in patients with deficit schizophrenia. Compr Psychiatry 55(2):349–356. doi:10.1016/j.comppsych.2013.08.025 Mier D, Lis S, Esslinger C, Sauer C, Hagenhoff M, Ulferts J, Gallhofer B, Kirsch P (2013) Neuronal correlates of social cognition in borderline personality disorder. Soc Cogn Affect Neurosci 8(5):531–537. doi:10.1093/scan/nss028 McLaren DG, Ries ML, Xu G, Johnson SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61(4):1277–1286. doi:10.1016/j.neuroimage.2012.03.068 van Buuren M, Gladwin TE, Zandbelt BB, van den Heuvel M, Ramsey NF, Kahn RS, Vink M (2009) Cardiorespiratory effects on default-mode network activity as measured with fMRI. Hum Brain Mapp 30(9):3031–3042. doi:10.1002/hbm.20729 Lieberman MD, Cunningham WA (2009) Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 4(4):423–428. doi:10.1093/scan/nsp052 Woods SW (2003) Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry 64(6):663–667 Pinkham AE (2014) Social cognition in schizophrenia. J Clin Psychiatry 75(Suppl 2):14–19. doi:10.4088/JCP.13065su1.04 Samson D, Apperly IA, Chiavarino C, Humphreys GW (2004) Left temporoparietal junction is necessary for representing someone else’s belief. Nat Neurosci 7(5):499–500. doi:10.1038/nn1223 Mahy CE, Moses LJ, Pfeifer JH (2014) How and where: theory-of-mind in the brain. Dev Cogn Neurosci 9:68–81. doi:10.1016/j.dcn.2014.01.002 Mar RA (2011) The neural bases of social cognition and story comprehension. Annu Rev Psychol 62:103–134. doi:10.1146/annurev-psych-120709-145406 Straube B, Green A, Sass K, Kirner-Veselinovic A, Kircher T (2013) Neural integration of speech and gesture in schizophrenia: evidence for differential processing of metaphoric gestures. Hum Brain Mapp 34(7):1696–1712. doi:10.1002/hbm.22015 Blakemore SJ, Sarfati Y, Bazin N, Decety J (2003) The detection of intentional contingencies in simple animations in patients with delusions of persecution. Psychol Med 33(8):1433–1441 Frith CD (2004) Schizophrenia and theory of mind. Psychol Med 34(3):385–389 Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7(4):268–277. doi:10.1038/nrn1884 Schilbach L, Derntl B, Aleman A, Caspers S, Clos M, Diederen KM, Gruber O, Kogler L, Liemburg EJ, Sommer IE, Muller VI, Cieslik EC, Eickhoff SB (2016) Differential patterns of dysconnectivity in mirror neuron and mentalizing networks in schizophrenia. Schizophr Bull 42(5):1135–1148. doi:10.1093/schbul/sbw015 Schilbach L, Hoffstaedter F, Muller V, Cieslik EC, Goya-Maldonado R, Trost S, Sorg C, Riedl V, Jardri R, Sommer I, Kogler L, Derntl B, Gruber O, Eickhoff SB (2016) Transdiagnostic commonalities and differences in resting state functional connectivity of the default mode network in schizophrenia and major depression. NeuroImage Clin 10:326–335. doi:10.1016/j.nicl.2015.11.021 Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage 84:320–341. doi:10.1016/j.neuroimage.2013.08.048 Linke M, Jankowski KS, Ciołkiewicz A, Jędrasik-Styła M, Parnowska D, Gruszka A, Denisiuk M, Jarema M, Wichniak A (2015) Age or age at onset? Which of them really matters for neuro and social cognition in schizophrenia? Psychiatry Res 225(1):197–201 Frajo-Apor B, Pardeller S, Kemmler G, Welte A-S, Hofer A (2016) Emotional Intelligence deficits in schizophrenia: the impact of non-social cognition. Schizophr Res 172(1):131–136 Scherzer P, Achim A, Léveillé E, Boisseau E, Stip E (2015) Evidence from paranoid schizophrenia for more than one component of theory of mind. Front Psychol 6:1643. doi:10.3389/fpsyg.2015.01643 Scherzer PB, Leveillé E, Achim A, Boisseau E, Stip E (2012) A study of theory of mind in paranoid schizophrenia: a theory or many theories? Front Psychol 3:432. doi:10.3389/fpsyg.2012.00432 Lehmann A, Bahcesular K, Brockmann EM, Biederbick SE, Dziobek I, Gallinat J, Montag C (2014) Subjective experience of emotions and emotional empathy in paranoid schizophrenia. Psychiatry Res 220(3):825–833. doi:10.1016/j.psychres.2014.09.009 Schilbach L (2016) Towards a second-person neuropsychiatry. Philos Trans R Soc Lond B Biol Sci 371(1686):20150081. doi:10.1098/rstb.2015.0081