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Aberrant Cortical Integration in First-Episode Psychosis During Natural Audiovisual Processing

  • Teemu Mäntylä
    Correspondence
    Address correspondence to Teemu Mäntylä, M.A., Mental Health Unit, National Institute for Health and Welfare, PO Box 30, Helsinki FI-00271, Finland.
    Affiliations
    Mental Health Unit, National Institute for Health and Welfare, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Psychology and Logopedics, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Neuroscience and Biomedical Engineering and Advanced Magnetic Imaging Center, Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland
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  • Lauri Nummenmaa
    Affiliations
    Department of Neuroscience and Biomedical Engineering and Advanced Magnetic Imaging Center, Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland

    Turku PET Centre and Department of Psychology, University of Turku, Turku, Finland
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  • Eva Rikandi
    Affiliations
    Mental Health Unit, National Institute for Health and Welfare, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Psychology and Logopedics, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Neuroscience and Biomedical Engineering and Advanced Magnetic Imaging Center, Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland
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  • Maija Lindgren
    Affiliations
    Mental Health Unit, National Institute for Health and Welfare, University of Helsinki, Helsinki University Hospital, Helsinki, Finland
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  • Tuula Kieseppä
    Affiliations
    Mental Health Unit, National Institute for Health and Welfare, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Psychiatry, University of Helsinki, Helsinki University Hospital, Helsinki, Finland
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  • Riitta Hari
    Affiliations
    Department of Art, School of Arts, Design and Architecture, Aalto University, Helsinki, Finland

    Department of Neuroscience and Biomedical Engineering and Advanced Magnetic Imaging Center, Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland
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  • Jaana Suvisaari
    Affiliations
    Mental Health Unit, National Institute for Health and Welfare, University of Helsinki, Helsinki University Hospital, Helsinki, Finland
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  • Tuukka T. Raij
    Affiliations
    Department of Psychiatry, University of Helsinki, Helsinki University Hospital, Helsinki, Finland

    Department of Neuroscience and Biomedical Engineering and Advanced Magnetic Imaging Center, Aalto NeuroImaging, Aalto University School of Science, Espoo, Finland
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      Abstract

      Background

      Functional magnetic resonance imaging studies of psychotic disorders have reported both hypoactivity and hyperactivity in numerous brain regions. In line with the dysconnection hypothesis, these regions include cortical integrative hub regions. However, most earlier studies focused on a single cognitive function at a time, assessed by delivering artificial stimuli to patients with chronic psychosis. Thus, it remains unresolved whether these findings are present already in early psychosis and whether they translate to real-life–like conditions that require multisensory processing and integration.

      Methods

      Scenes from the movie Alice in Wonderland (2010) were shown to 51 patients with first-episode psychosis (16 women) and 32 community-based control subjects (17 women) during 3T functional magnetic resonance imaging. We compared intersubject correlation, a measure of similarity of brain signal time courses in each voxel, between the groups. We also quantified the hubness as the number of connections each region has.

      Results

      Intersubject correlation was significantly lower in patients with first-episode psychosis than in control subjects in the medial and lateral prefrontal, cingulate, precuneal, and parietotemporal regions, including the default mode network. Regional magnitude of between-group difference in intersubject correlation was associated with the hubness.

      Conclusions

      Our findings provide novel evidence for the dysconnection hypothesis by showing that during complex real-life–like stimulation, the most prominent functional alterations in psychotic disorders relate to integrative brain functions. Presence of such abnormalities in first-episode psychosis rules out long-term effects of illness or medication. These methods can be used in further studies to map widespread hub alterations in a single functional magnetic resonance imaging session and link them to potential downstream and upstream pathways.

      Keywords

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      Linked Article

      • Cortical Hub Failure in Schizophrenia
        Biological PsychiatryVol. 84Issue 9
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          Schizophrenia is commonly characterized by the combination of positive, negative, and cognitive symptoms. Cognitive symptoms include problems with working memory, attention, and executive function. Integration of these cognitive processes supports many abilities, including social functioning. Impairment in this integration, then, may be a factor in disability in schizophrenia patients, preventing them from working or going to school (1). The brain networks underlying these cognitive abilities span the frontal, parietal, and temporal lobes.
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