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Research Paper

Reduced activation in the ventral striatum during probabilistic decision-making in patients in an at-risk mental state

Franziska Rausch, Daniela Mier, Sarah Eifler, Sabrina Fenske, Frederike Schirmbeck, Susanne Englisch, Claudia Schilling, Andreas Meyer-Lindenberg, Peter Kirsch and Mathias Zink
J Psychiatry Neurosci May 01, 2015 40 (3) 163-173; DOI: https://doi.org/10.1503/jpn.140191
Franziska Rausch
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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  • For correspondence: [email protected]
Daniela Mier
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Sarah Eifler
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Sabrina Fenske
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Frederike Schirmbeck
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Susanne Englisch
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Claudia Schilling
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Andreas Meyer-Lindenberg
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Peter Kirsch
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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Mathias Zink
From the Department of Psychiatry and Psychotherapy (Rausch, Eifler, Englisch, Schilling, Meyer-Lindenberg, Zink) and the Department of Clinical Psychology (Mier, Fenske, Kirsch), Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Germany; and the Academic Medical Centre, Amsterdam University, Netherlands (Schirmbeck).
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  • Fig. 1
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    Fig. 1

    (A) Illustration of the classical beads task. (B) Comparison of draws to decision (DTD) between patients in the at-risk mental state (ARMS) and controls. Results are reported as means and standard errors. (C) Comparison of jumping to conclusions bias (JTC; defined as 1 or 2 beads) between ARMS patients and controls (Fisher exact test, p = 0.015).

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    Fig. 2

    (A) Main effect of the lake decision (lake decision > colour decision). Significance threshold is p < 0.05, family-wise error [FWE]–corrected. (B) Final decision-making, indicating enhanced activation for the last fish (last fish > all previous fish). Significance threshold set at p < 0.05, FWE-corrected. (C) Final decision-making, indicating average signal change for the last fish in comparison to all previous fish in the right ventral striatum. Displayed is the first Eigenvariate of the right ventral striatal activation extracted for a mask of the right nucleus accumbens, with a significance threshold set to 1. ARMS = at-risk mental state.

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    Table 1

    Sociodemographic and psychopathological characteristics of study participants

    Group, mean ± SD*
    CharacteristicARMS, n = 24Control, n = 24p value
    Age22.0 ± 3.323.2 ± 4.30.28
    Sex, female:male10:149:150.52
    Education level, yr11.5 ± 1.611.8 ± 1.50.40
    MWT-B23.4 ± 4.224.3 ± 5.70.57
    Estimated verbal IQ94.8 ± 9.398.3 ± 14.40.32
    ERIraos sum score42.8 ± 14.8——
    ARMS, early:late8:16——
    PANSS
     Total score60.3 ± 12.9——
     Positive symptoms13.2 ± 4.1——
     Negative symptoms12.7 ± 4.8——
     Global psychopathology34.5 ± 7.0——
    SANS30.1 ± 20.1——
    CDSS6.5 ± 4.6——
    PSP61.7 ± 13.0——
    GAF50.8 ± 8.8——
    CGI-S4.0 ± 0.6——
    PSYRATS
     Amount of preoccupation1.3 ± 1.5——
     Duration of preoccupation1.5 ± 1.4——
     Conviction1.4 ± 1.6——
     Amount of distress1.8 ± 1.8——
     Intensity of distress1.8 ± 1.7——
     Disruption0.9 ± 1.2——
    • ARMS = at-risk mental state; CDSS = Calgary Depression Scale for Schizophrenia; CGI-S = Clinical Global Impression — Severity; ERIraos = Early Recognition Inventory based on IRAOS; GAF = Global Assessment of Functioning; MWT-B = Multiple Choice Word Test (version B); PANSS = Positive and Negative Syndrome Scale; PSP = Personal and Social Performance Scale; PSYRATS = Psychotic Symptoms Rating Scale; SANS = Scale for the Assessment of Negative Symptoms; SD = standard deviation.

    • ↵* Unless otherwise indicated.

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    Table 2

    Neurocognitive characteristics of study participants

    Group, mean ± SD
    CharacteristicARMS, n = 24Controls, n = 24p value
    MATRICS test battery
     TMT-A, s28.7 ± 8.326.1 ± 7.80.27
     TMT-B, s58.1 ± 18.253.0 ± 13.70.28
     BACS-SC57.7 ± 9.765.2 ± 10.40.013*
     HVLT-R28.8 ± 4.230.6 ± 4.60.17
     WMS-III-SS18.5 ± 3.720.0 ± 2.50.10
     LNS16.1 ± 2.917.9 ± 3.00.039*
     NAB-Mazes21.4 ± 3.624.0 ± 1.80.003
     BVMT-R29.3 ± 5.429.7 ± 4.70.78
     Fluency25.8 ± 6.626.0 ± 7.40.89
     MSCEIT–Emotion management91.4 ± 11.091.3 ± 7.80.98
     MSCEIT–Social management93.3 ± 7.492.4 ± 9.20.70
     MSCEIT–Managing emotions92.2 ± 8.391.6 ± 8.30.81
     CPT-DPrime2.4 ± 0.62.7 ± 0.60.14
    WCST
     Categories completed6.6 ± 1.26.8 ± 1.10.56
     Total trials78.4 ± 15.579.4 ± 11.10.79
     Total errors (%)19.6 ± 8.018.2 ± 6.00.47
     Perseveration Score (%)15.0 ± 13.113.2 ± 11.60.61
     Concept perseverations0.7 ± 1.00.4 ± 0.70.22
     Failure to maintain set0.9 ± 1.41.0 ± 1.50.77
    • ARMS = at-risk mental state; BACS-SC = Brief Assessment of Cognition in Schizophrenia — Symbol Coding; BVMT-R = Brief Visual Memory Test Revised; CPT = Continuous Performance Test; HVLT-R = Hopkins Verbal Learning Task Revised; LNS = letter-number sequencing; MATRICS = Measurement and Treatment Research to Improve Cognition in Schizophrenia; MSCEIT = Mayer–Salovey–Caruso Emotional Intelligence Test; NAB = Neuropsychological Assessment Battery; SD = standard deviation; TMT = Trail Making Test; WCST = Wisconsin Card Sorting Test; WMSIII-SS = Wechsler Memory Scale III — Spatial Span.

    • ↵* Not significant after Bonferroni correction for multiple testing.

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    Table 3

    Increased activation during the experimental (lake) decision compared to the control (colour) condition*

    MNI†
    ActivationBAk†xyzTmax§
    Inferior parietal lobule40528836−554913.49
    Superior parietal lobule7—27−675213.11
    Inferior parietal lobule40—−36−494610.77
    Inferior frontal gyrus4730243320−212.01
    Cingulate gyrus32—9204911.52
    Middle frontal gyrus11—2750−810.63
    Middle frontal gyrus—289−3956410.76
    Inferior frontal gyrus4796−3023−28.98
    Inferior frontal gyrus9452−458318.79
    Middle frontal gyrus46—−5129316.72
    Middle frontal gyrus6—−30−1526.18
    Cerebellum—220−61−385.96
    • BA = Brodmann area; MNI = Montreal Neurological Institute.

    • ↵* Significance threshold set at p < 0.05, family-wise error–corrected.

    • ↵† Coordinates of the peak voxel in the cluster.

    • ‡ Subcluster peaks are inserted.

    • ↵§ Maximal t value in the cluster.

    • View popup
    Table 4

    Increased activation during the final decision in comparison to all previous decisions in the lake condition*

    MNI†
    ActivationBAk‡xyzTmax§
    Medial frontal gyrus6949−92588.59
    Middle frontal gyrus6302707.51
    Medial frontal gyrus6611527.19
    Inferior frontal gyrus4719653023−28.35
    Putamen188−28.34
    Midbrain−6−28−88.19
    Lingual gyrus178039−8817.98
    Lingual gyrus17−9−8817.56
    Parahippocampal gyrus1930−55−87.42
    Middle frontal gyrus10673641286.34
    Precentral gyrus641−482405.90
    Parahippocampal gyrus1912−27−58−55.85
    Anterior cingulate2411−932195.48
    Anterior cingulate32−1229285.16
    Cerebellum160−34−385.46
    Postcentral gyrus4022−45−31495.41
    Postcentral gyrus3−42−28585.09
    • BA = Brodmann area; MNI = Montreal Neurological Institute.

    • ↵* Significance threshold set at p < 0.05, family-wise error–corrected.

    • ↵† Coordinates of the peak voxel in the cluster.

    • ↵‡ Subcluster peaks are inserted.

    • ↵§ Maximal t value in the cluster.

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Journal of Psychiatry and Neuroscience: 40 (3)
J Psychiatry Neurosci
Vol. 40, Issue 3
1 May 2015
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Reduced activation in the ventral striatum during probabilistic decision-making in patients in an at-risk mental state
Franziska Rausch, Daniela Mier, Sarah Eifler, Sabrina Fenske, Frederike Schirmbeck, Susanne Englisch, Claudia Schilling, Andreas Meyer-Lindenberg, Peter Kirsch, Mathias Zink
J Psychiatry Neurosci May 2015, 40 (3) 163-173; DOI: 10.1503/jpn.140191

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Reduced activation in the ventral striatum during probabilistic decision-making in patients in an at-risk mental state
Franziska Rausch, Daniela Mier, Sarah Eifler, Sabrina Fenske, Frederike Schirmbeck, Susanne Englisch, Claudia Schilling, Andreas Meyer-Lindenberg, Peter Kirsch, Mathias Zink
J Psychiatry Neurosci May 2015, 40 (3) 163-173; DOI: 10.1503/jpn.140191
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