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White matter changes in psychosis risk relate to development and are not impacted by the transition to psychosis

Molecular Psychiatry volume 26, pages 6833–6844 (2021)Cite this article

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Abstract

Subtle alterations in white matter microstructure are observed in youth at clinical high risk (CHR) for psychosis. However, the timing of these changes and their relationships to the emergence of psychosis remain unclear. Here, we track the evolution of white matter abnormalities in a large, longitudinal cohort of CHR individuals comprising the North American Prodrome Longitudinal Study (NAPLS-3). Multi-shell diffusion magnetic resonance imaging data were collected across multiple timepoints (1–5 over 1 year) in 286 subjects (aged 12–32 years): 25 CHR individuals who transitioned to psychosis (CHR-P; 61 scans), 205 CHR subjects with unknown transition outcome after the 1-year follow-up period (CHR-U; 596 scans), and 56 healthy controls (195 scans). Linear mixed effects models were fitted to infer the impact of age and illness-onset on variation in the fractional anisotropy of cellular tissue (FAT) and the volume fraction of extracellular free water (FW). Baseline measures of white matter microstructure did not differentiate between HC, CHR-U and CHR-P individuals. However, age trajectories differed between the three groups in line with a developmental effect: CHR-P and CHR-U groups displayed higher FAT in adolescence, and 4% lower FAT by 30 years of age compared to controls. Furthermore, older CHR-P subjects (20+ years) displayed 4% higher FW in the forceps major (p < 0.05). Prospective analysis in CHR-P did not reveal a significant impact of illness onset on regional FAT or FW, suggesting that transition to psychosis is not marked by dramatic change in white matter microstructure. Instead, clinical high risk for psychosis—regardless of transition outcome—is characterized by subtle age-related white matter changes that occur in tandem with development.

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Fig. 1: Flowchart depicting the selection of suitable scans.
Fig. 2: Age-related change in white matter microstructure.
Fig. 3: Significant group differences across ages in white matter microstructure.
Fig. 4: Association between neurobehavioral and dMRI phenotypes.

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Code availability

The Matlab function fitlme was used to perform linear mixed effects (LME) models with bootstrapping confidence intervals. This code is publicly accessible.

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Acknowledgements

MADB was supported by an Australian National Health and Medical Research Council (NHMRC) Investigator Grant (1175754). This study was supported by a National Alliance for Research on Schizophrenia & Depression (NARSAD) Brain and Behavior Research Foundation Young Investigator Award (to AEL) and by the National Institute of Mental Health (grant K01 MH115247-01A1 to AEL; grants R01MH108574, R01MH102377, R01MH074794, P41EB015902 to OP; grant U01MH081984 to JA; grant U01MH081928 to WSS; grant U01MH081944 to KSC; grant U01MH081902 to TDC and CEB; grant U01MH082004 to DOP; grant U01MH082022 to SWW; grant U01MH076989 to DHM; grant U01MH081857 to BAC; and, grant U01MH109977 to MES).

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Authors and Affiliations

  1. Department of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Maria A. Di Biase, Suheyla Cetin-Karayumak, Amanda E. Lyall, Kang Ik Kevin Cho, Marek Kubicki, Yogesh Rathi, Monica G. Lyons, Sylvain Bouix, Tashrif Billah, Martha E. Shenton & Ofer Pasternak

  2. Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne and Melbourne Health, Carlton South, VIC, Australia

    Maria A. Di Biase & Andrew Zalesky

  3. Department of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Suheyla Cetin-Karayumak, Fan Zhang, Marek Kubicki, Yogesh Rathi, Martha E. Shenton & Ofer Pasternak

  4. Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

    Amanda E. Lyall, Marek Kubicki & Martha E. Shenton

  5. Department of Psychiatry and Psychology, Yale University, New Haven, CT, USA

    Alan Anticevic, Jie Lisa Ji, Zailyn Tamayo, Scott W. Woods & Tyrone D. Cannon

  6. UCLA School of Medicine, Los Angeles, CA, USA

    Charlie Schleifer

  7. Yale Interdepartmental Neuroscience Program, Yale School of Medicine, New Haven, CT, USA

    Brendan D. Adkinson

  8. Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada

    Jean Addington

  9. Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior and Department of Psychology, University of California-Los Angeles, Los Angeles, CA, USA

    Carrie E. Bearden

  10. Department of Psychiatry and Psychology, The Feinstein Institute for Medical Research, Manhasset, NY, USA

    Barbara A. Cornblatt

  11. Department of Psychology, Hofstra North Shore-LIJ School of Medicine, Hempstead, NY, USA

    Barbara A. Cornblatt & Diana O. Perkins

  12. The Zucker Hillside Hospital, New York, NY, USA

    Barbara A. Cornblatt

  13. Harvard Medical School and Beth Israel Deaconess Medical Center, Boston, MA, USA

    Matcheri S. Keshavan & William S. Stone

  14. University of California, San Francisco, San Francisco, CA, USA

    Daniel H. Mathalon

  15. San Francisco VA Medical Center, San Francisco, CA, USA

    Daniel H. Mathalon

  16. Department of Psychiatry and Psychology, Yale University, New Haven, CT, USA

    Thomas H. McGlashan

  17. University of North Carolina (UNC), Chapel Hill, NC, USA

    Diana O. Perkins

  18. Department of Psychiatry, University of California San Diego (UCSD), La Jolla, CA, USA

    Kristen S. Cadenhead & Ming T. Tsuang

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  1. Maria A. Di Biase
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Correspondence to Maria A. Di Biase.

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Di Biase, M.A., Cetin-Karayumak, S., Lyall, A.E. et al. White matter changes in psychosis risk relate to development and are not impacted by the transition to psychosis. Mol Psychiatry 26, 6833–6844 (2021). https://doi.org/10.1038/s41380-021-01128-8

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