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N-Methyl-D-Aspartate Receptor Antagonist Effects on Prefrontal Cortical Connectivity Better Model Early Than Chronic Schizophrenia

  • Alan Anticevic
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    National Institute on Alcohol Abuse and Alcoholism Center for the Translational Neuroscience of Alcoholism, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut
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  • Philip R. Corlett
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut
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  • Michael W. Cole
    Affiliations
    Center for Molecular & Behavioral Neuroscience, Rutgers University, Newark, New Jersey
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  • Aleksandar Savic
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut

    University Psychiatric Hospital Vrapce, University of Zagreb, Zagreb, Croatia
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  • Mark Gancsos
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut
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  • Yanqing Tang
    Affiliations
    Department of Psychiatry, The First Affiliated Hospital, China Medical University, Shenyang, Liaoning, People’s Republic of China
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  • Grega Repovs
    Affiliations
    Department of Psychology, University of Ljubljana, Ljubljana, Slovenia
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  • John D. Murray
    Affiliations
    Department of Neurobiology, Yale University, New Haven, Connecticut

    Department of Physics, Yale University, New Haven, Connecticut
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  • Naomi R. Driesen
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut
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  • Peter T. Morgan
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut
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  • Ke Xu
    Correspondence
    Address correspondence to Fei Wang, Ph.D., Department of Radiology and Psychiatry, The First Affiliated Hospital, China Medical University, 155 Nanjing North Street, Shenyang 110001, Liaoning, PR China and Department of Psychiatry, Yale University School of Medicine, New Haven, CT 06511
    Affiliations
    Department of Radiology, The First Affiliated Hospital, China Medical University, Shenyang, Liaoning, People’s Republic of China
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  • Fei Wang
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    Department of Radiology, The First Affiliated Hospital, China Medical University, Shenyang, Liaoning, People’s Republic of China
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  • John H. Krystal
    Affiliations
    Department of Psychiatry, Yale University School of Medicine, Connecticut Mental Health Center, New Haven, Connecticut

    National Institute on Alcohol Abuse and Alcoholism Center for the Translational Neuroscience of Alcoholism, Connecticut Mental Health Center, New Haven, Connecticut

    Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, Connecticut

    Department of Psychiatry, Yale-New Haven Hospital, New Haven, Connecticut
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      Abstract

      Background

      Prefrontal cortex (PFC) function contributes to schizophrenia onset and progression. However, little is known about neural mechanisms behind PFC functional alterations along illness stages. Recent pharmacologic studies indicate that glutamate dysfunction may produce increased functional connectivity. However, pharmacologic models of schizophrenia overlook effects of illness progression on PFC function. This study compared N-methyl-D-aspartate glutamate receptor (NMDAR) antagonist effects in healthy volunteers with stages of schizophrenia with respect to PFC functional connectivity.

      Methods

      First, we tested ketamine effects on PFC functional connectivity in healthy volunteers in a data-driven way (n = 19). Next, we compared healthy subjects (n = 96) with three clinical groups: individuals at high risk for schizophrenia (n = 21), people early in their course of schizophrenia (EC-SCZ) (n = 28), and patients with chronic illness (n = 20). Across independent analyses, we used data-driven global brain connectivity techniques restricted to PFC to identify functional dysconnectivity.

      Results

      Results revealed robust PFC hyperconnectivity in healthy volunteers administered ketamine (Cohen’s d = 1.46), resembling individuals at high risk for schizophrenia and EC-SCZ. Hyperconnectivity was not found in patients with chronic illness relative to EC-SCZ patients. Results provide the first evidence that ketamine effects on PFC functional connectivity resemble early course but not chronic schizophrenia.

      Conclusions

      Results suggest an illness phase-specific relevance of NMDAR antagonist administration for prefrontal dysconnectivity associated with schizophrenia. This finding has implications for the neurobiology of illness progression and for the widespread use of NMDAR antagonists in the development of therapeutics for schizophrenia.

      Keywords

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      Linked Article

      • Combining Data Across Methodologies and Continents to Test a Mechanistic Hypothesis: Setting Up the Future
        Biological PsychiatryVol. 77Issue 6
        • Preview
          The role of glutamatergic neurotransmission in the pathophysiology of schizophrenia has been intensively examined and supported by converging lines of basic and clinical research, spanning from animal models to neuroimaging and postmortem investigations (1–4). However, the mechanistic path from genetic vulnerability to clinical manifestation is still uncharted. Such a path can be established by identifying reliable endophenotypes that can serve as biomarkers. These continuous quantitative parameters can provide stepping-stones, in which, for example, N-methyl-D-aspartate perturbations known to produce psychotic symptoms (1) are demonstrated to exist in populations at risk or patients in early stages of the disorder.
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      • Erratum
        Biological PsychiatryVol. 79Issue 7
        • Preview
          Erratum to: “N-Methyl-D-Aspartate Receptor Antagonist Effects on Prefrontal Cortical Connectivity Better Model Early Than Chronic Schizophrenia” by Anticevic et al. (2015;77:569-580). The authors discovered an error in the reporting of some of the coordinates in Tables 2 and 3, affecting the information supplied in the first six columns of each table. All other data in the tables remain accurate as originally reported. The corrected tables are reprinted here in their entirety.
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