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European Archives of Psychiatry and Clinical Neuroscience

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Open Access 01-06-2021 | Schizophrenia | Original Paper

Increased regional homogeneity modulated by metacognitive training predicts therapeutic efficacy in patients with schizophrenia

Authors: Xiaoxiao Shan, Rongyuan Liao, Yangpan Ou, Pan Pan, Yudan Ding, Feng Liu, Jindong Chen, Jingping Zhao, Wenbin Guo, Yiqun He

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 4/2021

Abstract

Previous studies have demonstrated the efficacy of metacognitive training (MCT) in schizophrenia. However, the underlying mechanisms related to therapeutic effect of MCT remain unknown. The present study explored the treatment effects of MCT on brain regional neural activity using regional homogeneity (ReHo) and whether these regions’ activities could predict individual treatment response in schizophrenia. Forty-one patients with schizophrenia and 20 healthy controls were scanned using resting-state functional magnetic resonance imaging. Patients were randomly divided into drug therapy (DT) and drug plus psychotherapy (DPP) groups. The DT group received only olanzapine treatment, whereas the DPP group received olanzapine and MCT for 8 weeks. The results revealed that ReHo in the right precuneus, left superior medial prefrontal cortex (MPFC), right parahippocampal gyrus and left rectus was significantly increased in the DPP group after 8 weeks of treatment. Patients in the DT group showed significantly increased ReHo in the left ventral MPFC/anterior cingulate cortex (ACC), left superior MPFC/middle frontal gyrus (MFG), left precuneus, right rectus and left MFG, and significantly decreased ReHo in the bilateral cerebellum VIII and left inferior occipital gyrus (IOG) after treatment. Support vector regression analyses showed that high ReHo levels at baseline in the right precuneus and left superior MPFC could predict symptomatic improvement of Positive and Negative Syndrome Scale (PANSS) after 8 weeks of DPP treatment. Moreover, high ReHo levels at baseline and alterations of ReHo in the left ventral MPFC/ACC could predict symptomatic improvement of PANSS after 8 weeks of DT treatment. This study suggests that MCT is associated with the modulation of ReHo in schizophrenia. ReHo in the right precuneus and left superior MPFC may predict individual therapeutic response for MCT in patients with schizophrenia.

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Masse M, Lecomte T (2015) Metacognitive profiles in individuals with a first episode of psychosis and their relation to social functioning and perceived social support. Schizophr Res 166:60–64PubMed

Moritz S, Woodward TS, Balzan R (2016) Is metacognitive training for psychosis effective? Expert Rev Neurother 16:105PubMed

Ochoa S, Lopez-Carrilero R, Barrigon ML et al (2017) Randomized control trial to assess the efficacy of metacognitive training compared with a psycho-educational group in people with a recent-onset psychosis. Psychol Med 47:1573–1584PubMed

Moritz S, Veckenstedt R, Andreou C et al (2014) Sustained and "sleeper" effects of group metacognitive training for schizophrenia: a randomized clinical trial. JAMA Psychiat 71:1103–1111

Eichner C, Berna F (2016) Acceptance and efficacy of metacognitive training (MCT) on positive symptoms and delusions in patients with schizophrenia: a meta-analysis taking into account important moderators. Schizophr Bull 42:952–962PubMedPubMedCentral

Pankowski D, Kowalski J, Gawęda Ł (2016) The effectiveness of metacognitive training for patients with schizophrenia: a narrative systematic review of studies published between 2009 and 2015. Psychiatr 50:787–803 in press

Baird B, Smallwood J, Gorgolewski KJ et al (2013) Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception. J Neurosci 33:16657–16665PubMedPubMedCentral

Francis MM, Hummer TA, Leonhardt BL et al (2017) Association of medial prefrontal resting state functional connectivity and metacognitive capacity in early phase psychosis. Psychiat Res 262:8–14

Murray RJ, Schaer M, Debbané M (2012) Degrees of separation: a quantitative neuroimaging meta-analysis investigating self-specificity and shared neural activation between self- and other-reflection. Neurosci Biobehav Rev 36:1043–1059PubMed

10.

Andreou C, Steinmann S, Leicht G et al (2018) fMRI correlates of jumping-to-conclusions in patients with delusions: Connectivity patterns and effects of metacognitive training. Neuroimage Clin 20:119–127PubMedPubMedCentral

11.

Zang Y, Jiang T, Lu Y et al (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394–400PubMed

12.

Zuo XN, Xu T, Jiang L et al (2013) Toward reliable characterization of functional homogeneity in the human brain: preprocessing, scan duration, imaging resolution and computational space. Neuroimage 65:374–386PubMed

13.

de Pasquale F, Della PS, Snyder AZ et al (2010) Temporal dynamics of spontaneous MEG activity in brain networks. Proc Natl Acad Sci USA 107:6040–6045PubMed

14.

Expert P, Lambiotte R, Chialvo DR et al (2011) Self-similar correlation function in brain resting-state functional magnetic resonance imaging. J R Soc Interface 8:472–479PubMed

15.

Park C, Lazar NA, Ahn J et al (2010) A multiscale analysis of the temporal characteristics of resting-state fMRI data. J Neurosci Methods 193:334–342PubMed

16.

Song XW, Dong ZY, Long XY et al (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE 6:e25031PubMedPubMedCentral

17.

He Y, Wang L, Zang Y et al (2007) Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. Neuroimage 35:488–500PubMed

18.

Rongjun Y, Ming HH, Hsiao-Lan Sharon W et al (2013) Frequency dependent alterations in regional homogeneity of baseline brain activity in schizophrenia. PLoS ONE 8:e57516

19.

Guo WB, Liu F, Xue ZM et al (2011) Abnormal neural activities in first-episode, treatment-naive, short-illness-duration, and treatment-response patients with major depressive disorder: a resting-state fMRI study. J Affect Disord 135(1–3):326–331PubMed

20.

Cao QJ, Zang YF, Wang YF (2007) Brain functions in attention deficit hyperactivity disorder combined and inattentive subtypes: a resting-state functional magnetic resonance imaging study. J Peking Univ 39:261

21.

Wang S, Wang G, Lv H et al (2016) Abnormal regional homogeneity as potential imaging biomarker for psychosis risk syndrome: a resting-state fMRI study and support vector machine analysis. Sci Rep 6:27619PubMedPubMedCentral

22.

Li M, Chen Z, Deng W et al (2012) Volume increases in putamen associated with positive symptom reduction in previously drug-naive schizophrenia after 6 weeks antipsychotic treatment. Psychol Med 42:1475–1483PubMed

23.

Hutcheson NL, Clark DG, Bolding MS et al (2014) Basal ganglia volume in unmedicated patients with schizophrenia is associated with treatment response to antipsychotic medication. Psychiatry Res 221:6–12PubMed

24.

Lahti AC, Weiler MA, Holcomb HH et al (2009) Modulation of limbic circuitry predicts treatment response to antipsychotic medication: a functional imaging study in schizophrenia. Neuropsychopharmacol 34:2675–2690

25.

Li H, Guo W, Liu F et al (2019) Enhanced baseline activity in the left ventromedial putamen predicts individual treatment response in drug-naive, first-episode schizophrenia: results from two independent study samples. Ebiomedicine 46:248–255PubMedPubMedCentral

26.

Li H, Ou Y, Liu F et al (2019) Reduced connectivity in anterior cingulate cortex as an early predictor for treatment response in drug-naive, first-episode schizophrenia: a global-brain functional connectivity analysis. Schizophr Res 215:337–343PubMed

27.

Wu R, Ou Y, Liu F et al (2019) Reduced brain activity in the right putamen as an early predictor for treatment response in drug-naive, first-episode schizophrenia. Front Psychiatry 10:741PubMedPubMedCentral

28.

Cadena EJ, White DM, Kraguljac NV et al (2019) Cognitive control network dysconnectivity and response to antipsychotic treatment in schizophrenia. Schizophr Res 204:262–270PubMed

29.

Cui LB, Cai M, Wang XR et al (2019) Prediction of early response to overall treatment for schizophrenia: a functional magnetic resonance imaging study. Brain Behav 9:e1211

30.

Wang S, Zhan Y, Zhang Y et al (2018) Abnormal long- and short-range functional connectivity in adolescent-onset schizophrenia patients: A resting-state fMRI study. Prog Neuropsychopharmacol Biol Psychiatry 81:445–451PubMed

31.

Shan XX, Ou YP, Pan P et al (2019) Increased frontal gray matter volume in individuals with prodromal psychosis. CNS Neurosci Ther 25:987–994PubMedPubMedCentral

32.

Li P, Jing RX, Zhao RJ et al (2017) Electroconvulsive therapy-induced brain functional connectivity predicts therapeutic efficacy in patients with schizophrenia: a multivariate pattern recognition study. NPJ Schizophr 3:21PubMedPubMedCentral

33.

Redlich R, Opel N, Grotegerd D et al (2016) Prediction of individual response to electroconvulsive therapy via machine learning on structural magnetic resonance imaging data. JAMA Psychiat 73:557–564

34.

Harrison JE (2005) Orthodontic clinical trials III: reporting of ethical issues associated with clinical trials published in three orthodontic journals between 1989 and 1998. J Orthod 32:115–121PubMed

35.

Andrew AM (2000) An introduction to support vector machines and other kernel-based learning methods. Cambridge University Press, Cambridge

36.

Suykens JAK, Gestel TV, Brabanter JD et al (2002) Least squares support vector machines. Int J Circuit Theory Appl 27:605–615

37.

Abdallah FF, Darwish HW, Darwish IA et al (2019) Orthogonal projection to latent structures and first derivative for manipulation of PLSR and SVR chemometric models' prediction: a case study. PLoS ONE 14:e222197

38.

Zomer S (2006) Support vector machines: a recent method for classification in chemometrics. Crit Rev Anal Chem 36:177–188

39.

Guo W, Feng L, Chen J et al (2017) Olanzapine modulation of long- and short-range functional connectivity in the resting brain in a sample of patients with schizophrenia. Eur Neuropsychopharm 27:48–58

40.

Lui S, Li T, Deng W et al (2010) Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by "resting state" functional magnetic resonance imaging. Arch Gen Psychiatry 67:783–792PubMed

41.

Blasi G, Popolizio T, Taurisano P et al (2009) Changes in prefrontal and amygdala activity during olanzapine treatment in schizophrenia. Psychiatry Res 173:31–38PubMedPubMedCentral

42.

Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583PubMed

43.

Richter FR, Cooper RA, Bays PM et al (2016) Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory. Elife 5:e18260PubMedPubMedCentral

44.

van der Meer L, de Vos AE, Stiekema AP et al (2013) Insight in schizophrenia: involvement of self-reflection networks? Schizophr Bull 39:1288–1295PubMed

45.

Sreekumar V, Nielson DM, Smith TA et al (2018) The experience of vivid autobiographical reminiscence is supported by subjective content representations in the precuneus. Sci Rep 8:14899PubMedPubMedCentral

46.

Fleming SM, Weil RS, Nagy Z et al (2010) Relating introspective accuracy to individual differences in brain structure. Science 329:1541–1543PubMedPubMedCentral

47.

Yokoyama O, Miura N, Watanabe J et al (2010) Right frontopolar cortex activity correlates with reliability of retrospective rating of confidence in short-term recognition memory performance. Neurosci Res 68:199–206PubMed

48.

McCurdy LY, Maniscalco B, Metcalfe J et al (2013) Anatomical coupling between distinct metacognitive systems for memory and visual perception. J Neurosci 33:1897–1906PubMedPubMedCentral

49.

Ye Q, Zou F, Lau H et al (2018) Causal Evidence for Mnemonic Metacognition in Human Precuneus. J Neurosci 38:6379–6387PubMed

50.

Song C, Kanai R, Fleming SM et al (2011) Relating inter-individual differences in metacognitive performance on different perceptual tasks. Conscious Cogn 20:1787–1792PubMedPubMedCentral

51.

Andreasen NC, Rezai K, Alliger R et al (1992) Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia. Assessment with xenon 133 single-photon emission computed tomography and the Tower of London. Arch Gen Psychiatry 49:943–958PubMed

52.

Buchsbaum MS, Nuechterlein KH, Haier RJ et al (1990) Glucose metabolic rate in normals and schizophrenics during the continuous performance test assessed by positron emission tomography. Br J Psychiatry 156:216–227PubMed

53.

Allen P, Seal ML, Valli I et al (2011) Altered prefrontal and hippocampal function during verbal encoding and recognition in people with prodromal symptoms of psychosis. Schizophr Bull 37:746–756PubMed

54.

Du Y, Fryer SL, Fu Z et al (2018) Dynamic functional connectivity impairments in early schizophrenia and clinical high-risk for psychosis. Neuroimage 180:632–645PubMed

55.

Wojtalik JA, Smith MJ, Keshavan MS et al (2017) A systematic and meta-analytic review of neural correlates of functional outcome in schizophrenia. Schizoph Bull 43:1329–1347PubMed

56.

Yuan M, Qiu C, Meng Y et al (2018) Pre-treatment resting-state functional MR imaging predicts the long-term clinical outcome after short-term paroxtine treatment in post-traumatic stress disorder. Front Psychiatry 9:532PubMedPubMedCentral

57.

Jiang R, Abbott CC, Jiang T et al (2018) SMRI biomarkers predict electroconvulsive treatment outcomes: accuracy with independent data sets. Neuropsychopharmacol 43:1078–1087

58.

Masuda K, Nakanishi M, Okamoto K et al (2017) Different functioning of prefrontal cortex predicts treatment response after a selective serotonin reuptake inhibitor treatment in patients with major depression. J Affect Disord 214:44–52PubMed

59.

Moritz S, Kerstan A, Veckenstedt R et al (2011) Further evidence for the efficacy of a metacognitive group training in schizophrenia. Behav Res Ther 49:151–157PubMed

60.

Moritz S, Mahlke CI, Westermann S et al (2018) Embracing psychosis: a cognitive insight intervention improves personal narratives and meaning-making in patients with schizophrenia. Schizophr Bull 44:307–316PubMed

61.

Mancevski B, Keilp J, Kurzon M et al (2007) Lifelong course of positive and negative symptoms in chronically institutionalized patients with schizophrenia. Psychopathology 40:83–92PubMed

62.

McGlashan TH, Fenton WS (1992) The positive-negative distinction in schizophrenia. Review of natural history validators. Arch Gen Psychiatry 49:63–72PubMed

Title: Increased regional homogeneity modulated by metacognitive training predicts therapeutic efficacy in patients with schizophrenia
Authors: Xiaoxiao Shan
Rongyuan Liao
Yangpan Ou
Pan Pan
Yudan Ding
Feng Liu
Jindong Chen
Jingping Zhao
Wenbin Guo
Yiqun He
Publication date: 01-06-2021
Publisher: Springer Berlin Heidelberg
Keywords: Schizophrenia
Olanzapine
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 4/2021
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-020-01119-w

ACC 2024 Congress

Springer Medicine

Increased regional homogeneity modulated by metacognitive training predicts therapeutic efficacy in patients with schizophrenia

Abstract

ACC 2024 Congress

Springer Medicine

Abstract

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