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Brain control of dual-task walking can be improved in aging and neurological disease

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Abstract

The peak prevalence of multiple sclerosis has shifted into older age groups, but co-occurring and possibly synergistic motoric and cognitive declines in this patient population are poorly understood. Dual-task-walking performance, subserved by the prefrontal cortex, and compromised in multiple sclerosis and aging, predicts health outcomes. Whether acute practice can improve dual-task walking performance and prefrontal cortex hemodynamic response efficiency in multiple sclerosis has not been reported. To address this gap in the literature, the current study examined task- and practice-related effects on dual-task-walking and associated brain activation in older adults with multiple sclerosis and controls. Multiple sclerosis (n = 94, mean age = 64.76 ± 4.19 years) and control (n = 104, mean age = 68.18 ± 7.01 years) participants were tested under three experimental conditions (dual-task-walk, single-task-walk, and single-task-alpha) administered over three repeated counterbalanced trials. Functional near-infrared-spectroscopy was used to evaluate task- and practice-related changes in prefrontal cortex oxygenated hemoglobin. Gait and cognitive performances declined, and prefrontal cortex oxygenated hemoglobin was higher in dual compared to both single task conditions in both groups. Gait and cognitive performances improved over trials in both groups. There were greater declines over trials in oxygenated hemoglobin in dual-task-walk compared to single-task-walk in both groups. Among controls, but not multiple sclerosis participants, declines over trials in oxygenated hemoglobin were greater in dual-task-walk compared to single-task-alpha. Dual-task walking and associated prefrontal cortex activation efficiency improved during a single session, but improvement in neural resource utilization, although significant, was attenuated in multiple sclerosis participants. These findings suggest encouraging brain adaptability in aging and neurological disease.

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Funding

This research was supported by grants from the National Institutes of Health (R01NS109023).

Author information

Authors and Affiliations

  1. Department of Neurology, Albert Einstein College of Medicine, Bronx, NY, USA

    Roee Holtzer

  2. Ferkauf Graduate School of Psychology, Yeshiva University, Bronx, NY, USA

    Roee Holtzer & Frederick W. Foley

  3. Department of Epidemiology & Population Health, Albert Einstein College of Medicine, Bronx, NY, USA

    Jaeun Choi

  4. Department of Kinesiology and Nutrition, College of Applied Health Sciences, University of Illinois, Chicago, IL, USA

    Robert W. Motl

  5. Multiple Sclerosis Center, Holy Name Medical Center, Teaneck, NJ, USA

    Frederick W. Foley

  6. Department of Radiology, Gruss Magnetic Resonance Research Center, Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, NY, USA

    Mark E. Wagshul

  7. Department of Kinesiology and Community Health, College of Applied Health Sciences, University of Illinois, Urbana-Champaign, Urbana, IL, USA

    Manuel E. Hernandez

  8. Department of Biomedical and Translational Sciences, Carle Illinois College of Medicine, University of Illinois, Urbana-Champaign, Urbana, IL, USA

    Manuel E. Hernandez

  9. Electrical and Computer Engineering, Villanova University, Villanova, PA, USA

    Meltem Izzetoglu

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  1. Roee Holtzer
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  2. Jaeun Choi
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  5. Mark E. Wagshul
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  6. Manuel E. Hernandez
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  7. Meltem Izzetoglu
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Contributions

RH: Drafting/revision of the manuscript for content, including medical writing for content; major role in the acquisition of data; study concept or design; analysis or interpretation of data. JC: Drafting/revision of the manuscript for content, including medical writing for content; analysis or interpretation of data. RWM: Drafting/revision of the manuscript for content, including medical writing for content. FWF: Drafting/revision of the manuscript for content, including medical writing for content. MEH: Drafting/revision of the manuscript for content, including medical writing for content. MW: Drafting/revision of the manuscript for content, including medical writing for content; analysis or interpretation of data. MI: Analysis or interpretation of data, drafting/revision of the manuscript for content, including medical writing for content.

Corresponding author

Correspondence to Roee Holtzer.

Ethics declarations

Ethics approval

The work described in this manuscript has been executed in adherence with The Code of Ethics of the World Medical Association (Declaration of Helsinki).

Institutional review board

Albert Einstein College of Medicine Institutional Review Board approved this study (IRB #: 2019–10049).

Informed consent

Participants signed written informed consents in the first in-person study visit.

Conflict of interest

Dr. Izzetoglu has a minor share in fNIRS device. All other authors have no conflicts of interest to report in relation to the current article. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Glossary

DTW

Dual-task-walk

STW

Single-task-walk

STA

Single-task-alpha

fNIRS

Functional near-infrared spectroscopy

GHS

Global health status

IRB

Institutional review board

MRI

Magnetic resonance imaging

MS

Multiple sclerosis

PFC

Prefrontal cortex

RBANS

Repeatable battery for the assessment of neuropsychological status

HbO

Oxygenated hemoglobin

HbR

Deoxygenated hemoglobin

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Holtzer, R., Choi, J., Motl, R.W. et al. Brain control of dual-task walking can be improved in aging and neurological disease. GeroScience 46, 3169–3184 (2024). https://doi.org/10.1007/s11357-023-01054-3

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  • DOI: https://doi.org/10.1007/s11357-023-01054-3

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