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Cognitive impairment associated with cerebellar volume loss in spinocerebellar ataxia type 3

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Abstract

Background

Many neuroscience and neurology studies have forced a reconsideration of the traditional motor-related scope of cerebellar function, which has now expanded to include various cognitive functions. Spinocerebellar ataxia type 3 (SCA3; the most common hereditary ataxia) is neuropathologically characterized by cerebellar atrophy and frequently presents with cognitive impairment.

Objective

To characterize cognitive impairment in SCA3 and investigate the cerebellum–cognition associations.

Methods

This prospective, cross-sectional cohort study recruited 126 SCA3 patients and 41 healthy control individuals (HCs). Participants underwent a brain 3D T1-weighted images as well as neuropsychological tests. Voxel-based morphometry (VBM) and region of interest (ROI) approaches were performed on the 3D T1-weighted images. CERES was used to automatically segment cerebellums. Patients were grouped into cognitively impaired (CI) and cognitively preserved (CP), and clinical and MRI parameters were compared. Multivariable regression models were fitted to examine associations between cerebellar microstructural alterations and cognitive domain impairments.

Results

Compared to HCs, SCA3 patients showed cognitive domain impairments in information processing speed, verbal memory, executive function, and visuospatial perception. Between CI and CP subgroups, the CI subgroup was older and had lower education, as well as higher severity scores. VBM and ROI analyses revealed volume loss in cerebellar bilateral lobule VI, right lobule Crus I, and right lobule IV of the CI subgroup, and all these cerebellar lobules were associated with the above cognitive domain impairments.

Conclusions

Our findings demonstrate the multiple cognitive domain impairments in SCA3 patients and indicate the responsible cerebellar lobules for the impaired cognitive domain(s).

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Data Availability

The data sets used or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors would like to thank the kind patients and families who participated in this research.

Funding

This work has been supported by the grants 82230039 (N.W.), 81870902 (N.W.), U21A20360 (Y.F.), 81971082 (S.R.G.) from the National Natural Science Foundation of China.

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Author notes

  1. Zhi-Xian Ye, Jin Bi, Liang-Liang Qiu and Xuan-Yu Chen have contributed equally to this work.

Authors and Affiliations

  1. Department of Neurology and Institute of Neurology of First Affiliated Hospital, Institute of Neuroscience and Fujian Key Laboratory of Molecular Neurology, Fujian Medical University, Fuzhou, 350005, China

    Zhi-Xian Ye, Jin Bi, Liang-Liang Qiu, Yu-Sen Qiu, Ru-Ying Yuan, Xin-Tong Yu, Chun-Yu Huang, Bi Cheng, Wei Lin, Wan-Jin Chen, Ying Fu, Ning Wang & Shi-Rui Gan

  2. Department of Neurology, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou, 350212, China

    Liang-Liang Qiu, Chun-Yu Huang, Wan-Jin Chen, Ying Fu, Ning Wang & Shi-Rui Gan

  3. School of Basic Medical Sciences, Fujian Medical University, Fuzhou, 350005, China

    Xuan-Yu Chen & Ying Fu

  4. Department of Radiology of First Affiliated Hospital, Fujian Medical University, Fuzhou, 350005, China

    Meng-Cheng Li & Jian-Ping Hu

  5. Department of Rehabilitation Medicine of First Affiliated Hospital, Fujian Medical University, Fuzhou, 350005, China

    Xin-Yuan Chen

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Contributions

YF, NW, and SRG formulated and designed the study concept. ZXY, JB, LLQ, XYC, XYC, YSQ, RYY, XTY, CYH, WL, and WJC enrolled the patients and conducted clinical assessments and neuropsychological tests. ZXY, MCL, and JPH conducted imaging data collection. XYC, XTY, BC, and WL performed laboratory determination. ZXY, JB, LLQ, NW, YF, and SRG analyzed the data, and interpreted the results. All authors were involved in drafting/revising the manuscript.

Corresponding authors

Correspondence to Ying Fu, Ning Wang or Shi-Rui Gan.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Ye, ZX., Bi, J., Qiu, LL. et al. Cognitive impairment associated with cerebellar volume loss in spinocerebellar ataxia type 3. J Neurol 271, 918–928 (2024). https://doi.org/10.1007/s00415-023-12042-0

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