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February 22, 2022; 98 (8) Research Article

Neural Variability in the Prefrontal Cortex as a Reflection of Neural Flexibility and Stability in Patients With Parkinson Disease

Inbal Maidan, Roni Hacham, Irina Galperin, Nir Giladi, View ORCID ProfileRoee Holtzer, Jeffrey M. Hausdorff, Anat Mirelman
First published December 14, 2021, DOI: https://doi.org/10.1212/WNL.0000000000013217
Inbal Maidan
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Roni Hacham
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Irina Galperin
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Nir Giladi
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Roee Holtzer
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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  • ORCID record for Roee Holtzer
Jeffrey M. Hausdorff
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Anat Mirelman
From the Laboratory of Early Markers of Neurodegeneration (I.M., R.H., I.G., N.G., J.M.H., A.M.), Center for the Study of Movement, Cognition, and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center; Departments of Neurology (I.M., N.G., A.M.) and Physical Therapy (J.M.H.), Sackler School of Medicine, and Sagol School of Neuroscience (I.M., N.G., J.M.H., A.M.), Tel Aviv University, Israel; Yeshiva University (R.H.); Albert Einstein College of Medicine (R.H.), New York, NY; and Rush Alzheimer's Disease Center (J.M.H.) and Department of Orthopaedic Surgery (J.M.H.), Rush University Medical Center, Chicago, IL.
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Neural Variability in the Prefrontal Cortex as a Reflection of Neural Flexibility and Stability in Patients With Parkinson Disease
Inbal Maidan, Roni Hacham, Irina Galperin, Nir Giladi, Roee Holtzer, Jeffrey M. Hausdorff, Anat Mirelman
Neurology Feb 2022, 98 (8) e839-e847; DOI: 10.1212/WNL.0000000000013217

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Abstract

Background and Objectives Functional near-infrared spectroscopy (fNIRS) studies provide direct evidence of the important role of the prefrontal cortex (PFC) during walking in aging and Parkinson disease (PD). Most studies explored mean hemoglobin (HbO2) levels, while moment-to-moment variability measures have rarely been investigated. Variability measures can inform on flexibility, which is imperative for adaptive function. We hypothesized that patients with PD will show less variability in HbO2 signals during walking compared to healthy controls.

Methods Two hundred six participants, 57 healthy controls (age 68.9 ± 1.0 years, 27 women) and 149 patients with idiopathic PD (age 69.8 ± 0.6 years, 50 women, disease duration 8.27 ± 5.51 years), performed usual walking and dual-task walking (serial 3 subtractions) with an fNIRS sensor placed on the forehead. HbO2 variability was calculated from the SD, range, and mean detrended time series of fNIRS-derived HbO2 signal evaluated during each walking task. HbO2 variability was compared between groups and between walking tasks with mixed model analyses.

Results Higher variability (SD, range, mean detrended time series) was observed during dual-task walking compared to usual walking (p < 0.025), but this was derived from the differences within the healthy control group (group × task interaction p < 0.007). On the other hand, task repetition demonstrated reduced variability in healthy controls but increased variability in patients with PD (interaction group × walk repetition p < 0.048). The Movement Disorder Society Unified Parkinson's Disease Rating Scale motor score correlated with HbO2 range (r = 0.142, p = 0.050) and HbO2 SD (r = 0.173, p = 0.018) during usual walking among all participants.

Discussion In this study, we suggest a new way to interpret changes in HbO2 variability. We relate increased HbO2 variability to flexible adaptation to environmental challenges and decreased HbO2 variability to the stability of performance. Our results show that both are limited in PD; however, further investigation of these concepts is required. Moreover, HbO2 variability measures are an important aspect of brain function that add new insights into the role of PFC during walking with aging and PD.

Trial Registration Information ClinicalTrials.gov Identifier: NCT01732653.

Classification of Evidence This study provides Class III evidence that patients with PD have more variability within HbO2 signals during usual walking compared to healthy controls but not during dual-task walking.

Glossary

BOLD=
blood oxygenation level–dependent;
DSM-IV=
Diagnostic and Statistical Manual of Mental Disorders, 4th edition;
fNIRS=
near-infrared spectroscopy;
HbO2=
hemoglobin;
MDS=
Movement Disorder Society;
MoCA=
Montreal Cognitive Assessment;
PD=
Parkinson disease;
PFC=
prefrontal cortex;
UPDRS=
Unified Parkinson’s Disease Rating Scale

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Received June 23, 2021.
  • Accepted in final form November 24, 2021.
  • © 2021 American Academy of Neurology
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