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Published in: Journal of Neurology 1/2021

01-01-2021 | Parkinson's Disease | Original Communication

Changes in the EEG spectral power during dual-task walking with aging and Parkinson’s disease: initial findings using Event-Related Spectral Perturbation analysis

Authors: Daniel Possti, Firas Fahoum, Ronen Sosnik, Nir Giladi, Jeffrey M. Hausdorff, Anat Mirelman, Inbal Maidan

Published in: Journal of Neurology | Issue 1/2021

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Abstract

Background

The ability to maintain adequate motor-cognitive performance under increasing task demands depends on the regulation and coordination of neural resources. Studies have shown that such resources diminish with aging and disease. EEG spectral analysis is a method that has the potential to provide insight into neural alterations affecting motor-cognitive performance. The aim of this study was to assess changes in spectral analysis during dual-task walking in aging and disease

Methods

10 young adults, ten older adults, and ten patients with Parkinson’s disease (PD) completed an auditory oddball task while standing and while walking on a treadmill. Spectral power within four frequency bandwidths, delta (< 4 Hz), theta (4–8 Hz), alpha (8–12 Hz), and beta (12–30 Hz), was calculated using Event-Related Spectral Perturbation (ERSP) analyses and compared between single task and dual task and between groups.

Results

Differences in ERSP were found in all groups between the single and dual-task conditions. In response to dual-task walking, beta increased in all groups (p < 0.026), delta decreased in young adults (p = 0.03) and patients with PD (0.015) while theta increased in young adults (p = 0.028) but decreased in older adults (p = 0.02) and patients with PD (p = 0.015). Differences were seen between the young, the older adults, and the patients with PD.

Conclusions

These findings are the first to show changes in the power of different frequency bands during dual-task walking with aging and disease. These specific brain modulations may reflect deficits in readiness and allocation of attention that may be responsible for the deficits in dual-task performance.
Literature
1.
go back to reference Hausdorff JM (2007) Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci 26:555–589CrossRef Hausdorff JM (2007) Gait dynamics, fractals and falls: finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci 26:555–589CrossRef
2.
go back to reference Kobsar D, Olson C, Paranjape R, Hadjistavropoulos T, Barden JM (2014) Evaluation of age-related differences in the stride-to-stride fluctuations, regularity and symmetry of gait using a waist-mounted tri-axial accelerometer. Gait Posture 39:553–557CrossRef Kobsar D, Olson C, Paranjape R, Hadjistavropoulos T, Barden JM (2014) Evaluation of age-related differences in the stride-to-stride fluctuations, regularity and symmetry of gait using a waist-mounted tri-axial accelerometer. Gait Posture 39:553–557CrossRef
3.
go back to reference Moon Y, Sung J, An R, Hernandez ME, Sosnoff JJ (2016) Gait variability in people with neurological disorders: a systematic review and meta-analysis. Hum Mov Sci 47:197–208CrossRef Moon Y, Sung J, An R, Hernandez ME, Sosnoff JJ (2016) Gait variability in people with neurological disorders: a systematic review and meta-analysis. Hum Mov Sci 47:197–208CrossRef
4.
go back to reference Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113CrossRef Hausdorff JM (2009) Gait dynamics in Parkinson’s disease: common and distinct behavior among stride length, gait variability, and fractal-like scaling. Chaos 19:026113CrossRef
5.
go back to reference Marmelat V, Reynolds NR, Hellman A (2018) Gait dynamics in Parkinson's disease: short gait trials “stitched” together provide different fractal fluctuations compared to longer trials. Front Physiol 9:861CrossRef Marmelat V, Reynolds NR, Hellman A (2018) Gait dynamics in Parkinson's disease: short gait trials “stitched” together provide different fractal fluctuations compared to longer trials. Front Physiol 9:861CrossRef
6.
go back to reference Montero-Odasso M, Verghese J, Beauchet O, Hausdorff JM (2012) Gait and cognition: a complementary approach to understanding brain function and the risk of falling. J Am Geriatr Soc 60:2127–2136CrossRef Montero-Odasso M, Verghese J, Beauchet O, Hausdorff JM (2012) Gait and cognition: a complementary approach to understanding brain function and the risk of falling. J Am Geriatr Soc 60:2127–2136CrossRef
7.
go back to reference Morley JE (2016) Gait, falls, and dementia. J Am Med Dir Assoc. 17:467–470CrossRef Morley JE (2016) Gait, falls, and dementia. J Am Med Dir Assoc. 17:467–470CrossRef
8.
go back to reference Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342CrossRef Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342CrossRef
9.
go back to reference Berka C, Levendowski DJ, Lumicao MN, Yau A, Davis G, Zivkovic VT, Olmstead RE, Tremoulet PD, Craven PL (2007) EEG correlates of task engagement and mental workload in vigilance, learning, and memory tasks. Aviat Space Environ Med 78:B231–B244PubMed Berka C, Levendowski DJ, Lumicao MN, Yau A, Davis G, Zivkovic VT, Olmstead RE, Tremoulet PD, Craven PL (2007) EEG correlates of task engagement and mental workload in vigilance, learning, and memory tasks. Aviat Space Environ Med 78:B231–B244PubMed
10.
go back to reference Rietschel JC, McDonald CG, Goodman RN, Miller MW, Jones-Lush LM, Wittenberg GF, Hatfield BD (2014) Psychophysiological support of increasing attentional reserve during the development of a motor skill. Biol Psychol 103:349–356CrossRef Rietschel JC, McDonald CG, Goodman RN, Miller MW, Jones-Lush LM, Wittenberg GF, Hatfield BD (2014) Psychophysiological support of increasing attentional reserve during the development of a motor skill. Biol Psychol 103:349–356CrossRef
11.
go back to reference Polich J (2004) Clinical application of the P300 event-related brain potential. Phys Med Rehabil Clin N Am 15:133–161CrossRef Polich J (2004) Clinical application of the P300 event-related brain potential. Phys Med Rehabil Clin N Am 15:133–161CrossRef
12.
go back to reference Burns CG, Fairclough SH (2015) Use of auditory event-related potentials to measure immersion during a computer game. Int J Hum-Comput Stud 73:107–114CrossRef Burns CG, Fairclough SH (2015) Use of auditory event-related potentials to measure immersion during a computer game. Int J Hum-Comput Stud 73:107–114CrossRef
13.
go back to reference Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118:2128–2148CrossRef Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118:2128–2148CrossRef
14.
go back to reference Antal A, Dibo G, Keri S, Gabor K, Janka Z, Vecsei L, Benedek G (2000) P300 component of visual event-related potentials distinguishes patients with idiopathic Parkinson’s disease from patients with essential tremor. J Neural Transm (Vienna ) 107:787–797CrossRef Antal A, Dibo G, Keri S, Gabor K, Janka Z, Vecsei L, Benedek G (2000) P300 component of visual event-related potentials distinguishes patients with idiopathic Parkinson’s disease from patients with essential tremor. J Neural Transm (Vienna ) 107:787–797CrossRef
15.
go back to reference Solis-Vivanco R, Rodriguez-Violante M, Rodriguez-Agudelo Y, Schilmann A, Rodriguez-Ortiz U, Ricardo-Garcell J (2015) The P3a wave: a reliable neurophysiological measure of Parkinson’s disease duration and severity. Clin Neurophysiol 126:2142–2149CrossRef Solis-Vivanco R, Rodriguez-Violante M, Rodriguez-Agudelo Y, Schilmann A, Rodriguez-Ortiz U, Ricardo-Garcell J (2015) The P3a wave: a reliable neurophysiological measure of Parkinson’s disease duration and severity. Clin Neurophysiol 126:2142–2149CrossRef
16.
go back to reference Seer C, Lange F, Georgiev D, Jahanshahi M, Kopp B (2016) Event-related potentials and cognition in Parkinson’s disease: an integrative review. Neurosci Biobehav Rev 71:691–714CrossRef Seer C, Lange F, Georgiev D, Jahanshahi M, Kopp B (2016) Event-related potentials and cognition in Parkinson’s disease: an integrative review. Neurosci Biobehav Rev 71:691–714CrossRef
17.
go back to reference Munte TF, Joppich G, Dauper J, Schrader C, Dengler R, Heldmann M (2015) Random number generation and executive functions in Parkinson's disease: an event-related brain potential study. J Parkinsons Dis 5:613–620CrossRef Munte TF, Joppich G, Dauper J, Schrader C, Dengler R, Heldmann M (2015) Random number generation and executive functions in Parkinson's disease: an event-related brain potential study. J Parkinsons Dis 5:613–620CrossRef
18.
go back to reference Pauletti C, Mannarelli D, Locuratolo N, Curra A, Marinelli L, Fattapposta F (2019) Central fatigue and attentional processing in Parkinson’s disease: an event-related potentials study. Clin Neurophysiol 130:692–700CrossRef Pauletti C, Mannarelli D, Locuratolo N, Curra A, Marinelli L, Fattapposta F (2019) Central fatigue and attentional processing in Parkinson’s disease: an event-related potentials study. Clin Neurophysiol 130:692–700CrossRef
19.
go back to reference Beurskens R, Steinberg F, Antoniewicz F, Wolff W, Granacher U (2016) Neural correlates of dual-task walking: effects of cognitive versus motor interference in young adults. Neural Plast 2016:8032180CrossRef Beurskens R, Steinberg F, Antoniewicz F, Wolff W, Granacher U (2016) Neural correlates of dual-task walking: effects of cognitive versus motor interference in young adults. Neural Plast 2016:8032180CrossRef
20.
go back to reference Bradford JC, Lukos JR, Passaro A, Ries A, Ferris DP (2019) Effects of locomotor demands on cognitive processing. Sci Rep 9(1):1–12CrossRef Bradford JC, Lukos JR, Passaro A, Ries A, Ferris DP (2019) Effects of locomotor demands on cognitive processing. Sci Rep 9(1):1–12CrossRef
21.
go back to reference De SP, Butler JS, Malcolm BR, Foxe JJ (2014) Recalibration of inhibitory control systems during walking-related dual-task interference: a mobile brain-body imaging (MOBI) study. Neuroimage 94:55–64CrossRef De SP, Butler JS, Malcolm BR, Foxe JJ (2014) Recalibration of inhibitory control systems during walking-related dual-task interference: a mobile brain-body imaging (MOBI) study. Neuroimage 94:55–64CrossRef
22.
go back to reference Maidan I, Fahoum F, Shustak S, Gazit E, Patashov D, Tchertov D, Giladi N, Hausdorff JM, Mirelman A (2019) Changes in event-related potentials during dual task walking in aging and Parkinson’s disease. Clin Neurophysiol 130:224–230CrossRef Maidan I, Fahoum F, Shustak S, Gazit E, Patashov D, Tchertov D, Giladi N, Hausdorff JM, Mirelman A (2019) Changes in event-related potentials during dual task walking in aging and Parkinson’s disease. Clin Neurophysiol 130:224–230CrossRef
23.
go back to reference Malcolm BR, Foxe JJ, Butler JS, De SP (2015) The aging brain shows less flexible reallocation of cognitive resources during dual-task walking: a mobile brain/body imaging (MoBI) study. Neuroimage 117:230–242CrossRef Malcolm BR, Foxe JJ, Butler JS, De SP (2015) The aging brain shows less flexible reallocation of cognitive resources during dual-task walking: a mobile brain/body imaging (MoBI) study. Neuroimage 117:230–242CrossRef
24.
go back to reference Shaw EP, Rietschel JC, Hendershot BD, Pruziner AL, Miller MW, Hatfield BD, Gentili RJ (2018) Measurement of attentional reserve and mental effort for cognitive workload assessment under various task demands during dual-task walking. Biol Psychol 134:39–51CrossRef Shaw EP, Rietschel JC, Hendershot BD, Pruziner AL, Miller MW, Hatfield BD, Gentili RJ (2018) Measurement of attentional reserve and mental effort for cognitive workload assessment under various task demands during dual-task walking. Biol Psychol 134:39–51CrossRef
25.
go back to reference Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699CrossRef Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53:695–699CrossRef
27.
go back to reference Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRef Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement disorder society-sponsored revision of the unified Parkinson’s disease rating scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170CrossRef
28.
go back to reference Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21CrossRef Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21CrossRef
29.
go back to reference Gramann K, Gwin JT, Bigdely-Shamlo N, Ferris DP, Makeig S (2010) Visual evoked responses during standing and walking. Front Hum Neurosci 4:202CrossRef Gramann K, Gwin JT, Bigdely-Shamlo N, Ferris DP, Makeig S (2010) Visual evoked responses during standing and walking. Front Hum Neurosci 4:202CrossRef
30.
go back to reference Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190CrossRef Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190CrossRef
31.
go back to reference Basar-Eroglu C, Basar E, Demiralp T, Schurmann M (1992) P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. Int J Psychophysiol 13:161–179CrossRef Basar-Eroglu C, Basar E, Demiralp T, Schurmann M (1992) P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. Int J Psychophysiol 13:161–179CrossRef
32.
go back to reference Basar E (2006) The theory of the whole-brain-work. Int J Psychophysiol 60:133–138CrossRef Basar E (2006) The theory of the whole-brain-work. Int J Psychophysiol 60:133–138CrossRef
33.
go back to reference Picton TW (1992) The P300 wave of the human event-related potential. J Clin Neurophysiol 9:456–479CrossRef Picton TW (1992) The P300 wave of the human event-related potential. J Clin Neurophysiol 9:456–479CrossRef
34.
35.
go back to reference Basar-Eroglu C, Demiralp T, Schurmann M, Basar E (2001) Topological distribution of oddball ‘P300’ responses. Int J Psychophysiol 39:213–220CrossRef Basar-Eroglu C, Demiralp T, Schurmann M, Basar E (2001) Topological distribution of oddball ‘P300’ responses. Int J Psychophysiol 39:213–220CrossRef
36.
go back to reference Basar E, Basar-Eroglu C, Karakas S, Schurmann M (1999) Are cognitive processes manifested in event-related gamma, alpha, theta and delta oscillations in the EEG? Neurosci Lett 259:165–168CrossRef Basar E, Basar-Eroglu C, Karakas S, Schurmann M (1999) Are cognitive processes manifested in event-related gamma, alpha, theta and delta oscillations in the EEG? Neurosci Lett 259:165–168CrossRef
37.
go back to reference Gola M, Kaminski J, Brzezicka A, Wrobel A (2012) beta band oscillations as a correlate of alertness–changes in aging. Int J Psychophysiol 85:62–67CrossRef Gola M, Kaminski J, Brzezicka A, Wrobel A (2012) beta band oscillations as a correlate of alertness–changes in aging. Int J Psychophysiol 85:62–67CrossRef
38.
go back to reference Kline JE, Poggensee K, Ferris DP (2014) Your brain on speed: cognitive performance of a spatial working memory task is not affected by walking speed. Front Hum Neurosci 8:288CrossRef Kline JE, Poggensee K, Ferris DP (2014) Your brain on speed: cognitive performance of a spatial working memory task is not affected by walking speed. Front Hum Neurosci 8:288CrossRef
Metadata
Title
Changes in the EEG spectral power during dual-task walking with aging and Parkinson’s disease: initial findings using Event-Related Spectral Perturbation analysis
Authors
Daniel Possti
Firas Fahoum
Ronen Sosnik
Nir Giladi
Jeffrey M. Hausdorff
Anat Mirelman
Inbal Maidan
Publication date
01-01-2021
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 1/2021
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10104-1

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