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Erschienen in: Journal of Neurology 1/2021

04.08.2020 | 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

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

Erschienen in: Journal of Neurology | Ausgabe 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.
Literatur
1.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat Buzsבki G (2006) Rhythms of the brain. Oxford University Press, New YorkCrossRef Buzsבki G (2006) Rhythms of the brain. Oxford University Press, New YorkCrossRef
35.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat 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
Metadaten
Titel
Changes in the EEG spectral power during dual-task walking with aging and Parkinson’s disease: initial findings using Event-Related Spectral Perturbation analysis
verfasst von
Daniel Possti
Firas Fahoum
Ronen Sosnik
Nir Giladi
Jeffrey M. Hausdorff
Anat Mirelman
Inbal Maidan
Publikationsdatum
04.08.2020
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Neurology / Ausgabe 1/2021
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10104-1

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