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Eye movements and association with regional brain atrophy in clinical subtypes of progressive supranuclear palsy

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Abstract

Objective

To investigate oculomotor impairment in subtypes of progressive supranuclear palsy (PSP) and its associations with clinical features and regional brain volumes in PSP.

Methods

We compared the video-oculography (VOG) findings of 123 PSP patients, consisting of 66 PSP-Richardson syndrome (PSP-RS), 28 PSP-parkinsonism (PSP-P), and 29 PSP-progressive gait freezing (PSP-PGF), along with 80 Parkinson’s disease (PD) patients. We also investigated the associations of the VOG results with clinical features (disease duration, PSP rating scales [PSPRS] scores for dysphagia and postural stability) in the subtypes of PSP patients and with regional volumes in the brainstem, including the midbrain, pons, medulla, and the superior cerebellar peduncle (SCP), among the patients who had MRI images at the time of VOG (30 PSP).

Results

All of the three subtypes of PSP patients showed slower vertical saccades and smooth pursuit than that of the PD patients (adjusted p < 0.05). Among the PSP subtypes, saccadic peak velocity, saccadic accuracy, and pursuit gain were significantly decreased in patients with the PSP-RS compared to those with the PSP-PGF (adjusted p < 0.05). In multiple linear regression model, vertical saccadic velocity, latency, accuracy, and pursuit gain were associated with the PSPRS score for dysphagia (adjusted p < 0.05), and a decrease in vertical saccadic speed and accuracy was associated with SCP atrophy (corrected p < 0.05).

Conclusions

This study demonstrated the severity of oculomotor dysfunction in differentiating the subtypes of PSP and its significant relationships with the dysphagia symptom and SCP volume in PSP.

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Funding

This work was supported by Grant no. 0420193140 from the Seoul National University Hospital Research Fund.

Author information

Authors and Affiliations

  1. Department of Neurology and Movement Disorder Center, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Korea

    Ji-Hyun Choi, Jung Hwan Shin, Han-Joon Kim & Beomseok Jeon

  2. Department of Neurology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Korea

    Ji-Hyun Choi & Jong-Min Kim

  3. Department of Nuclear Medicine, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, Seoul National University College of Medicine, Seoul, Korea

    Heejung Kim

  4. Department of Neurology, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, Seoul National University College of Medicine, Seoul, Korea

    Jung Hwan Shin & Jee-Young Lee

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  1. Ji-Hyun Choi
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Contributions

J-HC, MD: design of the study, data analysis, interpretation of data, drafted and revised the manuscript. HJK, PhD: data analysis, interpretation of data, and revision of manuscript. JH Shin, MD, PhD: interpretation of data and revision of manuscript. J-YL MD, PhD: design of the study, interpretation of data, and revision of manuscript. H-JK, MD, PhD: interpretation of data and revision of manuscript. J-MK, MD, PhD: interpretation of data and revision of manuscript. BJ, MD, PhD: conceptualization and design of study, data analysis, interpretation of data, and revised the manuscript.

Corresponding author

Correspondence to Beomseok Jeon.

Ethics declarations

Conflicts of interest

HJK has received travel grant from International Parkinson and Movement Disorder Society and Korean Movement Disorder Society; research grant from the Seoul National University Hospital, New York University, and C-TRI. BJ has received grants from the International Parkinson and Movement Disorder Society, Peptron, and Abbvie Korea.

Ethical approval

This study was approved by the Ethical Committee of the Seoul National University, Seoul, Korea (No. 1904-062-1026). In addition, this study was conducted in accordance with the Helsinki Declaration.

Data access and responsibility statement

The corresponding author is able to provide the anonymized data of this study upon reasonable request from qualified investigators.

Electronic supplementary material

Below is the link to the electronic supplementary material.

415_2020_10230_MOESM1_ESM.tif

Supplementary file1 Supplementary Fig. 1. Eye movements by disease duration in the patients with PSP. (A) Saccadic peak velocity, (B) Saccadic latency, (C) Saccadic accuracy, (D) Smooth pursuit gain. * p, Significant difference between the PSP-RS subtype and the PSP-P and PSP-PGF subtypes at 1, 2, and 3 years of the disease duration by Mann–Whitney test. * p-value < 0.05, ** < 0.01, and *** < 0.001. Abbreviations: PSP = Progressive supranuclear palsy; RS = Richardson’s syndrome; P = parkinsonism; PGF = progressive gait freezing. (TIF 55640 kb)

415_2020_10230_MOESM2_ESM.tif

Supplementary file2 Supplementary Fig. 2. Correlational analysis between the dysphagia PSP rating scale and eye movements in the patients with PSP. Pearson’s correlation test between the dysphagia PSP rating scale and eye movements in patients with PSP (n = 123). Abbreviations: PSP = Progressive supranuclear palsy. (TIF 1669 kb)

Supplementary file3 Supplementary Table 1. Eye movements in the patients with PSP and PD. (DOCX 37 kb)

415_2020_10230_MOESM4_ESM.docx

Supplementary file4 Supplementary Table 2. Eye movements from 1 to 3 years of the disease duration in the patients with PSP (DOCX 34 kb)

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Supplementary file5 Supplementary Table 3. Correlational analysis between clinical variables and eye movements in the patients with PSP (DOCX 40 kb)

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Supplementary file6 Supplementary Table 4. Regional volumes in the brainstem and the superior cerebellar peduncle in the patients with PSP (DOCX 29 kb)

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Supplementary file7 Supplementary Table 5. Correlational analysis of the regional volumes in the brainstem and the superior cerebellar peduncle with eye movements in the patients with PSP (DOCX 31 kb)

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Supplementary file8 Supplementary Table 6. Multivariate analysis of the regional brain volumes with eye movements in the patients with PSP (DOCX 33 kb)

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Choi, JH., Kim, H., Shin, J.H. et al. Eye movements and association with regional brain atrophy in clinical subtypes of progressive supranuclear palsy. J Neurol 268, 967–977 (2021). https://doi.org/10.1007/s00415-020-10230-w

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  • DOI: https://doi.org/10.1007/s00415-020-10230-w

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