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Original article| Volume 45, 102406, October 2020

Visual system damage and network maladaptation are associated with cognitive performance in neuromyelitis optica spectrum disorders.

  • Author Footnotes
    1 current address: University of Queensland Faculty of Medicine, Brisbane, Queensland, Australia
    Velina S. Chavarro
    Footnotes
    1 current address: University of Queensland Faculty of Medicine, Brisbane, Queensland, Australia
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Judith Bellmann-Strobl
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Hanna G. Zimmermann
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Michael Scheel
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Institute of Neuroradiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Claudia Chien
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Frederike C. Oertel
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Multiple Sclerosis Center, Department of Neurology, University of California, San Francisco, CA, USA
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  • Martin Weygandt
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Klemens Ruprecht
    Affiliations
    Department of Neurology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Friedemann Paul
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Department of Neurology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany
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  • Carsten Finke
    Affiliations
    Department of Neurology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Berlin School of Mind & Brain, Humboldt-Universität zu Berlin, Germany
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  • Alexander U. Brandt
    Correspondence
    Corresponding author.
    Affiliations
    NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Experimental and Clinical Research Center, Max Delbrück Center for Molecular Medicine & Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Germany

    Department of Neurology, University of California, Irvine, CA, USA
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  • Author Footnotes
    1 current address: University of Queensland Faculty of Medicine, Brisbane, Queensland, Australia

      Highlights

      • Patients with NMOSD exhibit cognitive deficits but not impairment.
      • Impaired sensory-cognitive parallel processing neural networks may contribute to cognitive performance deficits in patients with NMOSD.
      • A physiological association of the primary visual network functional connectivity and cognitive performance appears absent in patients with NMOSD.
      • Visual network functional connectivity was able to explain 19% of the variance in cognitive performance in healthy controls, but none in patients.

      Abstract

      Background Neuromyelitis Optica Spectrum Disorders (NMOSD) is an autoimmune disease leading to disability from optic neuritis, myelitis and more rarely brain stem attacks and encephalitis. Patients with NMOSD also exhibit cognitive deficits, the cause of which remains unclear. Recent evidence highlights sensory-cognitive parallel processing converging on the primary visual cortex. The objective of this study was to investigate the effect of the primary visual network disruption from damage caused by optic neuritis on cognition in NMOSD.
      Methods Twenty-nine aquaporin-4 antibody seropositive patients with NMOSD and 22 healthy controls (HC) completed the brief repeatable battery of neuropsychological tests (BRB-N) and underwent 3 Tesla MRI. Primary visual network functional connectivity (FC) at resting state was analyzed and correlated with performance on BRB-N. These correlations were compared between the groups.
      Results Patients performed significantly worse than HC on the BRB-N Index score (t = 2.366, p = 0.02). Among HC, visual network FC decreased significantly as cognitive performance on the BRB-N Index score increased (rho(17)=-0.507, p = 0.02). Among patients, this association was absent (rho(23)=0.197, p = 0.18), and the difference in correlation direction and strength to HC was significant (z=-2.175, p = 0.01). Visual network FC was able to explain 19% of the variance in cognitive performance in HC, but none in patients.
      Conclusions A physiological association of the primary visual network FC and cognitive performance appears absent in patients with NMOSD, suggesting a partial explanation for cognitive deficits. Our findings extend neuroscientific concepts on sensory-cognitive parallel processing neural networks to a clearly defined pathological state, and may be relevant for other diseases with visual system damage.

      Keywords

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