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Lifespan development of thalamic nuclei and characterizing thalamic nuclei abnormalities in schizophrenia using normative modeling

Neuropsychopharmacology volume 49, pages 1518–1527 (2024)Cite this article

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Abstract

Thalamic abnormalities have been repeatedly implicated in the pathophysiology of schizophrenia and other neurodevelopmental disorders. Uncovering the etiology of thalamic abnormalities and how they may contribute to illness phenotypes faces at least two obstacles. First, the typical developmental trajectories of thalamic nuclei and their association with cognition across the lifespan are largely unknown. Second, modest effect sizes indicate marked individual differences and pose a significant challenge to personalized medicine. To address these knowledge gaps, we characterized the development of thalamic nuclei volumes using normative models generated from the Human Connectome Project Lifespan datasets (5–100+ years), then applied them to an independent clinical cohort to determine the frequency of thalamic volume deviations in people with schizophrenia (17–61 years). Normative models revealed diverse non-linear age effects across the lifespan. Association nuclei exhibited negative age effects during youth but stabilized in adulthood until turning negative again with older age. Sensorimotor nuclei volumes remained relatively stable through youth and adulthood until also turning negative with older age. Up to 18% of individuals with schizophrenia exhibited abnormally small (i.e., below the 5th centile) mediodorsal and pulvinar volumes, and the degree of deviation, but not raw volumes, correlated with the severity of cognitive impairment. While case–control differences are robust, only a minority of patients demonstrate unusually small thalamic nuclei volumes. Normative modeling enables the identification of these individuals, which is a necessary step toward precision medicine.

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Fig. 1: Normative development of thalamic nuclei in the right hemisphere.
Fig. 2: Association between executive function and thalamic nuclei volumes across development.
Fig. 3: Proportions of individuals showing deviations from normative ranges in the Schizophrenia Cohort.
Fig. 4: Comparison of associations of SCIP total scores with centile scores and standardized raw volumes (Std Vols) in the schizophrenia group.

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Data availability

Data for normative modeling were derived from publicly available datasets. Individual-level data for the schizophrenia cohort are not publicly accessible as the participants of this study did not give written consent for their data to be shared publicly. Neuroimaging data storage and processing took place at the Vanderbilt University Institute of Imaging Science Center for Computational Imaging XNAT [78, 79].

Code availability

Neuroimaging processing pipelines were containerized using Singularity, built at Singularity Hub [80] (https://singularity-hub.org), and are accessible through GitHub (https://github.com/baxpr/thomasdocker). Code for statistical analyses is accessible through GitHub (https://github.com/Woodward-Lab/NormModThalamicNuclei).

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Acknowledgements

This work was conducted in part using the resources of the Advanced Computing Center for Research and Education at Vanderbilt University, Nashville, TN.

Funding

This work was supported by NIMH grants R01 MH102266, R01 MH115000, K24 MH126280, P50 MH132642-5980 (awarded to NDW), NIMH grant R01 MH123563 (awarded to SV), NIMH grant R01 MH070560 (awarded to SH); the Charlotte and Donald Test Fund and the Vanderbilt Institute for Clinical and Translational Research (through grant 1-UL-1-TR000445 from the National Center for Research Resources/NIH).

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Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA

    Anna S. Huang, Stephan Heckers & Neil D. Woodward

  2. Department of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA

    Kaidi Kang & Simon Vandekar

  3. Vanderbilt University Institute of Imaging Sciences, Vanderbilt University Medical Center, Nashville, TN, USA

    Baxter P. Rogers

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  1. Anna S. Huang
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Contributions

Anna S. Huang: Conceptualization, Data Curation, Analysis, Data Interpretation, Methodology, Project Administration, Writing–Original Draft; Kaidi Kang: Analysis, Methods, Writing—Review and Edit; Baxter P. Rogers: Analysis, Methods, Writing–Review and Edit; Simon Vandekar: Analysis, Methods, Validation, Writing–Review and Edit; Stephan Heckers: Funding, Data Acquisition, Writing–Review and Edit; Neil D. Woodward: Conceptualization, Funding, Project Administration, Data Interpretation, Resources, Supervision, Writing–Original Draft, Review and Edit.

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Correspondence to Anna S. Huang.

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Huang, A.S., Kang, K., Vandekar, S. et al. Lifespan development of thalamic nuclei and characterizing thalamic nuclei abnormalities in schizophrenia using normative modeling. Neuropsychopharmacol. 49, 1518–1527 (2024). https://doi.org/10.1038/s41386-024-01837-y

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