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Event-related oscillations differentiate between cognitive, motor and visual impairments

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Abstract

Background

Parkinson’s disease (PD) and dementia with Lewy bodies (DLB) share pathological and clinical similarities while differing in the timing and severity of motor cognitive and visual impairment. Previous EEG studies found abnormal neural oscillations in PD, mild cognitive impairment (MCI) and Alzheimer’s disease, however, the electrophysiological signature of clinical symptoms is still unclear. We assessed the specificity of event-related oscillations in distinguishing between cognitive, motor and visual involvement in patients with neurodegenerative conditions.

Methods

EEG was recorded during a visual oddball task in 30 PD, 28 DLB, 30 MCI patients and 32 age-matched healthy controls. Target and non-target event-related power were examined in the time–frequency domain using complex Morlet wavelet convolution and compared within and between the study groups.

Results

MCI (z = − 1.8, p = 0.04, Cohen’s d = − 0.5) and DLB (z = − 3.1, p < 0.001, d = − 1.0) patients showed decreased delta-band target event-related synchronization compared to participants with normal cognition. PD (z = 1.6, p = 0.05, d = 0.5) and DLB (z = 2.7, p < 0.01, d = 0.9) patients showed decreased beta suppression compared to MCI patients and controls. DLB patients with visual hallucinations (VH) showed decreased early-alpha suppression (z = 2.08, p = 0.019, d = 3.19, AUC = 1.0 ± 0.0) compared to DLB-VH−.

Conclusions

Decreased event-related delta-band synchronization, reflecting a decline in information processing ability, was characteristic of cognitive impairment due to any cause. Decreased event-related beta suppression, reflecting impaired execution of motor action, was specific to PD and DLB. Decreased event-related early-alpha suppression was characteristic of the presence of VH in DLB. These findings show that specific oscillations may reflect specific clinical symptoms, being a marker of network dysfunction.

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Data availability

Anonymized data can be obtained by request from a qualified investigator for purposes of replicating procedures and results.

Abbreviations

AD:

Alzheimer’s disease

AUC:

Area under the ROC

DLB:

Dementia with Lewy bodies

ERP:

Event-related potential

MDS:

Movement disorders society

MCI:

Mild cognitive impairment

MoCA:

Montreal cognitive assessment

PD:

Parkinson’s disease

PDD:

Parkinson’s disease dementia

ROC:

Receiver operating characteristic

UPDRS:

Unified PD rating scale motor part III

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Acknowledgements

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

Funding

This work 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, Sackler School of Medicine, Tel-Aviv University, 6 Weizmann Street, 64239, 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

    Firas Fahoum & Nir Giladi

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

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

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

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

Authors
  1. Yevgenia Rosenblum
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  2. Tamara Shiner
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  3. Noa Bregman
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  4. Firas Fahoum
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  5. Nir Giladi
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  6. Inbal Maidan
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  7. Anat Mirelman
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Correspondence to Anat Mirelman.

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Rosenblum, Y., Shiner, T., Bregman, N. et al. Event-related oscillations differentiate between cognitive, motor and visual impairments. J Neurol 269, 3529–3540 (2022). https://doi.org/10.1007/s00415-021-10953-4

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