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Decreased aperiodic neural activity in Parkinson’s disease and dementia with Lewy bodies

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Abstract

Neural oscillations and signal complexity have been widely studied in neurodegenerative diseases, whereas aperiodic activity has not been explored yet in those disorders. Here, we assessed whether the study of aperiodic activity brings new insights relating to disease as compared to the conventional spectral and complexity analyses. Eyes-closed resting-state electroencephalography (EEG) was recorded in 21 patients with dementia with Lewy bodies (DLB), 28 patients with Parkinson’s disease (PD), 27 patients with mild cognitive impairment (MCI) and 22 age-matched healthy controls. Spectral power was differentiated into its oscillatory and aperiodic components using the Irregularly Resampled Auto-Spectral Analysis. Signal complexity was explored using the Lempel–Ziv algorithm (LZC). We found that DLB patients showed steeper slopes of the aperiodic power component with large effect sizes compared to the controls and MCI and with a moderate effect size compared to PD. PD patients showed steeper slopes with a moderate effect size compared to controls and MCI. Oscillatory power and LZC differentiated only between DLB and other study groups and were not sensitive enough to detect differences between PD, MCI, and controls. In conclusion, both DLB and PD are characterized by alterations in aperiodic dynamics, which are more sensitive in detecting disease-related neural changes than the traditional spectral and complexity analyses. Our findings suggest that steeper aperiodic slopes may serve as a marker of network dysfunction in DLB and PD features.

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Data availability

The EEG data cannot be made publicly available because of ethical permits.

Abbreviations

DLB:

Dementia with Lewy bodies

IRASA:

Irregularly resampled auto-spectral analysis

LZC:

Lempel–Ziv complexity

MCI:

Mild cognitive impairment

MDS-UPDRS:

Movement disorders society unified Parkinson’s Disease Rating Scale motor part III

MoCA:

Montreal cognitive assessment

PD:

Parkinson’s disease

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Acknowledgements

We would like to thank all the volunteers and patients who participated in this study as well as the patients' caregivers.

Funding

The study was internally funded.

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Authors and Affiliations

  1. Laboratory of Early Markers of Neurodegeneration, Center for the Study of Movement, Cognition and Mobility, Neurological Institute, Tel Aviv Medical Center, Tel Aviv, Israel

    Yevgenia Rosenblum, Nir Giladi, Inbal Maidan & Anat Mirelman

  2. Cognitive Neurology Unit, Neurological Institute, Tel Aviv Medical Center, Tel Aviv, Israel

    Yevgenia Rosenblum, Tamara Shiner, Noa Bregman & Nir Giladi

  3. Epilepsy Unit, Neurological Institute, Tel Aviv Medical Center, Tel Aviv, Israel

    Nir Giladi & Firas Fahoum

  4. Department of Neurology and Neurosurgery, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel

    Yevgenia Rosenblum, Tamara Shiner, Noa Bregman, Nir Giladi, Inbal Maidan, Firas Fahoum & Anat Mirelman

  5. Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Tamara Shiner, Noa Bregman, Nir Giladi, Inbal Maidan & Anat Mirelman

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  1. Yevgenia Rosenblum
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  2. Tamara Shiner
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Contributions

Study concept and design: YR, AM; data acquisition: YR, TS; data analysis and interpretation: YR; drafting the article: YR; critical revision of the manuscript for important intellectual content: YR, IM, FF, NB, NG, TS, AM. All authors approved the final version.

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Correspondence to Anat Mirelman.

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The study was approved by the local ethical committee and was performed according to the Principles of the Declaration of Helsinki.

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Rosenblum, Y., Shiner, T., Bregman, N. et al. Decreased aperiodic neural activity in Parkinson’s disease and dementia with Lewy bodies. J Neurol 270, 3958–3969 (2023). https://doi.org/10.1007/s00415-023-11728-9

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