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Increased white matter metabolic rates in autism spectrum disorder and schizophrenia

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Abstract

Both autism spectrum disorder (ASD) and schizophrenia are often characterized as disorders of white matter integrity. Multimodal investigations have reported elevated metabolic rates, cerebral perfusion and basal activity in various white matter regions in schizophrenia, but none of these functions has previously been studied in ASD. We used 18fluorodeoxyglucose positron emission tomography to compare white matter metabolic rates in subjects with ASD (n = 25) to those with schizophrenia (n = 41) and healthy controls (n = 55) across a wide range of stereotaxically placed regions-of-interest. Both subjects with ASD and schizophrenia showed increased metabolic rates across the white matter regions assessed, including internal capsule, corpus callosum, and white matter in the frontal and temporal lobes. These increases were more pronounced, more widespread and more asymmetrical in subjects with ASD than in those with schizophrenia. The highest metabolic increases in both disorders were seen in the prefrontal white matter and anterior limb of the internal capsule. Compared to normal controls, differences in gray matter metabolism were less prominent and differences in adjacent white matter metabolism were more prominent in subjects with ASD than in those with schizophrenia. Autism spectrum disorder and schizophrenia are associated with heightened metabolic activity throughout the white matter. Unlike in the gray matter, the vector of white matter metabolic abnormalities appears to be similar in ASD and schizophrenia, may reflect inefficient functional connectivity with compensatory hypermetabolism, and may be a common feature of neurodevelopmental disorders.

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Acknowledgements

This work was partly supported by NARSAD Young Investigator Award and NIMH MH 077146 grant to Serge A. Mitelman and by NIMH grants P50 MH 66392-01, MH 60023, and MH 56489 to Monte S. Buchsbaum.

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Authors and Affiliations

  1. Departments of Psychiatry and Neuroscience, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, New York, NY, 10029, USA

    Serge A. Mitelman, M. Mehmet Haznedar, Lina Shihabuddin & Erin A. Hazlett

  2. Department of Psychiatry, Division of Child and Adolescent Psychiatry, Elmhurst Hospital Center, 79-01 Broadway, Elmhurst, NY, 11373, USA

    Serge A. Mitelman

  3. Departments of Psychiatry and Radiology, San Diego School of Medicine, NeuroPET Center, University of California, 11388 Sorrento Valley Road, Suite #100, San Diego, CA, 92121, USA

    Monte S. Buchsbaum

  4. Department of Statistics, University of Kentucky, 725 Rose Street, 323 Multidisciplinary Science Building, Lexington, KY, 40536, USA

    Derek S. Young

  5. Outpatient Psychiatry Care Center, James J. Peters VA Medical Center, Bronx, NY, 10468, USA

    M. Mehmet Haznedar

  6. Autism and Obsessive-Compulsive Spectrum Program, Anxiety and Depression Program, Department of Psychiatry and Behavioral Science, Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, NY, 10467, USA

    Eric Hollander

  7. Research and Development and VISN 2 Mental Illness Research, Education, and Clinical Center, James J. Peters VA Medical Center, Bronx, NY, 10468, USA

    Erin A. Hazlett

  8. Crisalid Unit (FJ5), CHI Clermont de l’Oise, 2 rue des Finets, 60607, Clermont, France

    Marie-Cecile Bralet

  9. Inserm Unit U669, Maison de Solenn, Universities Paris 5-11, 75014, Paris, France

    Marie-Cecile Bralet

  10. GDR 3557 Recherche Psychiatrie, Paris, France

    Marie-Cecile Bralet

Authors
  1. Serge A. Mitelman
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  2. Monte S. Buchsbaum
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  3. Derek S. Young
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  4. M. Mehmet Haznedar
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  5. Eric Hollander
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  6. Lina Shihabuddin
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  7. Erin A. Hazlett
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  8. Marie-Cecile Bralet
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Corresponding author

Correspondence to Serge A. Mitelman.

Ethics declarations

All procedures performed in this study were in accordance with the ethical standards of the Mount Sinai institutional research committee, as well as with the 1964 Helsinki declaration and its later amendments. The project was approved by the institutional review board of The Icahn School of Medicine at Mount Sinai. Informed consent was obtained from all individual participants in the study.

Conflict of interest

Author Serge A. Mitelman declares that he has no conflict of interest to report. Author Marie-Cecile Bralet declares that she has no conflict of interest to report. Author Derek S. Young declares that he has no conflict of interest to report. Author M. Mehmet Haznedar declares that he has no conflict of interest to report. Author Eric Hollander has received consultation fees from Transceit, Neuropharm, and Nastech. Author Lina Shihabuddin declares that she has no conflict of interest to report. Author Erin A. Hazlett declares that she has no conflict of interest to report. Author Monte S. Buchsbaum declares that he has no conflict of interest to report.

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Mitelman, S.A., Buchsbaum, M.S., Young, D.S. et al. Increased white matter metabolic rates in autism spectrum disorder and schizophrenia. Brain Imaging and Behavior 12, 1290–1305 (2018). https://doi.org/10.1007/s11682-017-9785-9

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