Skip to main content
Erschienen in: Journal of NeuroEngineering and Rehabilitation 1/2014

Open Access 01.12.2014 | Research

Increased frontal brain activation during walking while dual tasking: an fNIRS study in healthy young adults

verfasst von: Anat Mirelman, Inbal Maidan, Hagar Bernad-Elazari, Freek Nieuwhof, Miriam Reelick, Nir Giladi, Jeffrey M Hausdorff

Erschienen in: Journal of NeuroEngineering and Rehabilitation | Ausgabe 1/2014

Einloggen, um Zugang zu erhalten

Abstract

Background

Accumulating evidence suggests that gait is influenced by higher order cognitive and cortical control mechanisms. Recently, several studies used functional near infrared spectroscopy (fNIRS) to examine brain activity during walking, demonstrating increased oxygenated hemoglobin (HbO2) levels in the frontal cortex during walking while subjects completed a verbal cognitive task. It is, however, still unclear whether this increase in activation was related to verbalization, if the response was specific to gait, or if it would also be observed during standing, a different motor control task. The aim of this study was to investigate whether an increase in frontal activation is specific to dual tasking during walking.

Methods

Twenty-three healthy young adults (mean 30.9 ± 3.7 yrs, 13 females) were assessed using an electronic walkway. Frontal brain activation was assessed using an fNIRS system consisting of two probes placed on the forehead of the subjects. Assessments included: walking in a self-selected speed; walking while counting forward; walking while serially subtracting 7s (Walking+S7); and standing while serially subtracting 7s (Standing+S7). Data was collected from 5 walks of 30 meters in each condition. Twenty seconds of quiet standing before each walk served as baseline frontal lobe activity. Repeated Measures Analysis of Variance (RM ANOVA) tested for differences between the conditions.

Results

Significant differences were observed in HbO2 levels between all conditions (p = 0.007). HbO2 levels appeared to be graded; walking alone demonstrated the lowest levels of HbO2 followed by walking+counting condition (p = 0.03) followed by Walking+S7 condition significantly increased compared to the two other walking conditions (p < 0.01). No significant differences in HbO2 levels were observed between usual walking and the standing condition (p = 0.38) or between standing with or without serial subtraction (p = 0.76).

Conclusions

This study provides direct evidence that dual tasking during walking is associated with frontal brain activation in healthy young adults. The observed changes are apparently not a response to the verbalization of words and are related to the cognitive load during gait.
Literatur
1.
Zurück zum Zitat Amboni M, Barone P, Hausdorff JM: Cognitive contributions to gait and falls: evidence and implications. Mov Disord 2013,28(11):1520-1533. 10.1002/mds.25674CrossRefPubMedPubMedCentral Amboni M, Barone P, Hausdorff JM: Cognitive contributions to gait and falls: evidence and implications. Mov Disord 2013,28(11):1520-1533. 10.1002/mds.25674CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Yogev-Seligmann G, Hausdorff JM, Giladi N: The role of executive function and attention in gait. Mov Disord 2008, 23: 329-342. 10.1002/mds.21720CrossRefPubMed Yogev-Seligmann G, Hausdorff JM, Giladi N: The role of executive function and attention in gait. Mov Disord 2008, 23: 329-342. 10.1002/mds.21720CrossRefPubMed
3.
Zurück zum Zitat Hausdorff JM, Yogev G, Springer S, Simon ES, Giladi N: Walking is more like catching than tapping: gait in the elderly as a complex cognitive task. Exp Brain Res 2005, 164: 541-548. 10.1007/s00221-005-2280-3CrossRefPubMed Hausdorff JM, Yogev G, Springer S, Simon ES, Giladi N: Walking is more like catching than tapping: gait in the elderly as a complex cognitive task. Exp Brain Res 2005, 164: 541-548. 10.1007/s00221-005-2280-3CrossRefPubMed
4.
Zurück zum Zitat Hausdorff JM, Schweiger A, Herman T, Yogev-Seligmann G, Giladi N: Dual-task decrements in gait: contributing factors among healthy older adults. J Gerontol A Biol Sci Med Sci 2008, 63: 1335-1343. 10.1093/gerona/63.12.1335CrossRefPubMedPubMedCentral Hausdorff JM, Schweiger A, Herman T, Yogev-Seligmann G, Giladi N: Dual-task decrements in gait: contributing factors among healthy older adults. J Gerontol A Biol Sci Med Sci 2008, 63: 1335-1343. 10.1093/gerona/63.12.1335CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Hausdorff JM, Buchman AS: What links gait speed and MCI with dementia? A fresh look at the association between motor and cognitive function. J Gerontol A Biol Sci Med Sci 2013, 68: 409-411. 10.1093/gerona/glt002CrossRefPubMedPubMedCentral Hausdorff JM, Buchman AS: What links gait speed and MCI with dementia? A fresh look at the association between motor and cognitive function. J Gerontol A Biol Sci Med Sci 2013, 68: 409-411. 10.1093/gerona/glt002CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Holtzer R, Burright RG, Donovick PJ: The sensitivity of dual-task performance to cognitive status in aging. J Int Neuropsychol Soc 2004, 10: 230-238.CrossRefPubMed Holtzer R, Burright RG, Donovick PJ: The sensitivity of dual-task performance to cognitive status in aging. J Int Neuropsychol Soc 2004, 10: 230-238.CrossRefPubMed
7.
Zurück zum Zitat Verlinden VJ, van der Geest JN, Hofman A, Ikram MA: Cognition and gait show a distinct pattern of association in the general population. Alzheimers Dement 2013. doi: 10.1016/j.jalz.2013.03.009 Verlinden VJ, van der Geest JN, Hofman A, Ikram MA: Cognition and gait show a distinct pattern of association in the general population. Alzheimers Dement 2013. doi: 10.1016/j.jalz.2013.03.009
8.
Zurück zum Zitat Guo X, Skoog I, Matousek M, Larsson L, Palsson S, Sundh V, Steen B: A population-based study on motor performance and white matter lesions in older women. J Am Geriatr Soc 2000, 48: 967-970.CrossRefPubMed Guo X, Skoog I, Matousek M, Larsson L, Palsson S, Sundh V, Steen B: A population-based study on motor performance and white matter lesions in older women. J Am Geriatr Soc 2000, 48: 967-970.CrossRefPubMed
9.
Zurück zum Zitat Rosano C, Studenski SA, Aizenstein HJ, Boudreau RM, Longstreth WT Jr, Newman AB: Slower gait, slower information processing and smaller prefrontal area in older adults. Age Ageing 2012, 41: 58-64. 10.1093/ageing/afr113CrossRefPubMedPubMedCentral Rosano C, Studenski SA, Aizenstein HJ, Boudreau RM, Longstreth WT Jr, Newman AB: Slower gait, slower information processing and smaller prefrontal area in older adults. Age Ageing 2012, 41: 58-64. 10.1093/ageing/afr113CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM: Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 2013, 80: 1476-1484. 10.1212/WNL.0b013e31828cfaa4CrossRefPubMedPubMedCentral Rosenberg-Katz K, Herman T, Jacob Y, Giladi N, Hendler T, Hausdorff JM: Gray matter atrophy distinguishes between Parkinson disease motor subtypes. Neurology 2013, 80: 1476-1484. 10.1212/WNL.0b013e31828cfaa4CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Yogev-Seligmann G, Rotem-Galili Y, Mirelman A, Dickstein R, Giladi N, Hausdorff JM: How does explicit prioritization alter walking during dual-task performance? Effects of age and sex on gait speed and variability. Phys Ther 2010, 90: 177-186. 10.2522/ptj.20090043CrossRefPubMedPubMedCentral Yogev-Seligmann G, Rotem-Galili Y, Mirelman A, Dickstein R, Giladi N, Hausdorff JM: How does explicit prioritization alter walking during dual-task performance? Effects of age and sex on gait speed and variability. Phys Ther 2010, 90: 177-186. 10.2522/ptj.20090043CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Doi T, Makizako H, Shimada H, Park H, Tsutsumimoto K, Uemura K, Suzuki T: Brain activation during dual-task walking and executive function among older adults with mild cognitive impairment: a fNIRS study. Aging Clin Exp Res 2013,25(5):539-44. 10.1007/s40520-013-0119-5CrossRefPubMed Doi T, Makizako H, Shimada H, Park H, Tsutsumimoto K, Uemura K, Suzuki T: Brain activation during dual-task walking and executive function among older adults with mild cognitive impairment: a fNIRS study. Aging Clin Exp Res 2013,25(5):539-44. 10.1007/s40520-013-0119-5CrossRefPubMed
13.
Zurück zum Zitat Holtzer R, Mahoney JR, Izzetoglu M, Izzetoglu K, Onaral B, Verghese J: fNIRS study of walking and walking while talking in young and old individuals. J Gerontol A Biol Sci Med Sci 2011, 66: 879-887.CrossRefPubMed Holtzer R, Mahoney JR, Izzetoglu M, Izzetoglu K, Onaral B, Verghese J: fNIRS study of walking and walking while talking in young and old individuals. J Gerontol A Biol Sci Med Sci 2011, 66: 879-887.CrossRefPubMed
14.
Zurück zum Zitat Irani F, Platek SM, Bunce S, Ruocco AC, Chute D: Functional near infrared spectroscopy (fNIRS): an emerging neuroimaging technology with important applications for the study of brain disorders. Clin Neuropsychol 2007, 21: 9-37. 10.1080/13854040600910018CrossRefPubMed Irani F, Platek SM, Bunce S, Ruocco AC, Chute D: Functional near infrared spectroscopy (fNIRS): an emerging neuroimaging technology with important applications for the study of brain disorders. Clin Neuropsychol 2007, 21: 9-37. 10.1080/13854040600910018CrossRefPubMed
15.
Zurück zum Zitat Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H: The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005, 53: 695-699. 10.1111/j.1532-5415.2005.53221.xCrossRefPubMed Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H: The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005, 53: 695-699. 10.1111/j.1532-5415.2005.53221.xCrossRefPubMed
16.
Zurück zum Zitat Muthalib M, Anwar AR, Perrey S, Dat M, Galka A, Wolff S, Heute U, Deuschl G, Raethjen J, Muthuraman M: Multimodal integration of fNIRS, fMRI and EEG neuroimaging. Clin Neurophysiol 2013, 124: 2060-2062. 10.1016/j.clinph.2013.03.018CrossRefPubMed Muthalib M, Anwar AR, Perrey S, Dat M, Galka A, Wolff S, Heute U, Deuschl G, Raethjen J, Muthuraman M: Multimodal integration of fNIRS, fMRI and EEG neuroimaging. Clin Neurophysiol 2013, 124: 2060-2062. 10.1016/j.clinph.2013.03.018CrossRefPubMed
17.
Zurück zum Zitat Hausdorff JM: Stride variability: beyond length and frequency. Gait Posture 2004, 20: 304. 10.1016/j.gaitpost.2003.08.002CrossRefPubMed Hausdorff JM: Stride variability: beyond length and frequency. Gait Posture 2004, 20: 304. 10.1016/j.gaitpost.2003.08.002CrossRefPubMed
18.
Zurück zum Zitat Hausdorff JM: Gait variability: methods, modeling and meaning. J NeuroEng Rehabil 2005. doi:10.1186/1743-0003-2-19 Hausdorff JM: Gait variability: methods, modeling and meaning. J NeuroEng Rehabil 2005. doi:10.1186/1743-0003-2-19
19.
Zurück zum Zitat Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, Tsunazawa Y, Suzuki T, Yanagida T, Kubota K: Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 2001, 14: 1186-1192. 10.1006/nimg.2001.0905CrossRefPubMed Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, Tsunazawa Y, Suzuki T, Yanagida T, Kubota K: Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 2001, 14: 1186-1192. 10.1006/nimg.2001.0905CrossRefPubMed
20.
Zurück zum Zitat Grinsted A, Moore JC, Jevreheva S: Application of the cross wavelet transform and wavelt coherence to geophysical time series. Nonlinear Processes Geophys 2004, 11: 561-566. 10.5194/npg-11-561-2004CrossRef Grinsted A, Moore JC, Jevreheva S: Application of the cross wavelet transform and wavelt coherence to geophysical time series. Nonlinear Processes Geophys 2004, 11: 561-566. 10.5194/npg-11-561-2004CrossRef
21.
Zurück zum Zitat Torrence C, Compo GP: A practical guide to wavelet analysis. Bull Am Meterol Soc 1998, 79: 61-78. 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2CrossRef Torrence C, Compo GP: A practical guide to wavelet analysis. Bull Am Meterol Soc 1998, 79: 61-78. 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2CrossRef
22.
Zurück zum Zitat Ruthruff E, Pashler HE, Klaassen A: Processing bottlenecks in dual-task performance: structural limitation or strategic postponement? Psychon Bull Rev 2001, 8: 73-80. 10.3758/BF03196141CrossRefPubMed Ruthruff E, Pashler HE, Klaassen A: Processing bottlenecks in dual-task performance: structural limitation or strategic postponement? Psychon Bull Rev 2001, 8: 73-80. 10.3758/BF03196141CrossRefPubMed
23.
Zurück zum Zitat Tombu M, Jolicoeur P: A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform 2003, 29: 3-18.CrossRefPubMed Tombu M, Jolicoeur P: A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform 2003, 29: 3-18.CrossRefPubMed
24.
Zurück zum Zitat Yamamoto T, Kato T: Paradoxical correlation between signal in functional magnetic resonance imaging and deoxygenated haemoglobin content in capillaries: a new theoretical explanation. Phys Med Biol 2002, 47: 1121-1141. 10.1088/0031-9155/47/7/309CrossRefPubMed Yamamoto T, Kato T: Paradoxical correlation between signal in functional magnetic resonance imaging and deoxygenated haemoglobin content in capillaries: a new theoretical explanation. Phys Med Biol 2002, 47: 1121-1141. 10.1088/0031-9155/47/7/309CrossRefPubMed
25.
Zurück zum Zitat Burgess PW, Veitch E, de Lacy CA, Shallice T: The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia 2000, 38: 848-863. 10.1016/S0028-3932(99)00134-7CrossRefPubMed Burgess PW, Veitch E, de Lacy CA, Shallice T: The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia 2000, 38: 848-863. 10.1016/S0028-3932(99)00134-7CrossRefPubMed
26.
Zurück zum Zitat Burgess PW: Strategy application disorder: the role of the frontal lobes in human multitasking. Psychol Res 2000, 63: 279-288. 10.1007/s004269900006CrossRefPubMed Burgess PW: Strategy application disorder: the role of the frontal lobes in human multitasking. Psychol Res 2000, 63: 279-288. 10.1007/s004269900006CrossRefPubMed
27.
Zurück zum Zitat Okuda J, Fujii T, Ohtake H, Tsukiura T, Yamadori A, Frith CD, Burgess PW: Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory. Int J Psychophysiol 2007,64(3):233-46. 10.1016/j.ijpsycho.2006.09.009CrossRefPubMed Okuda J, Fujii T, Ohtake H, Tsukiura T, Yamadori A, Frith CD, Burgess PW: Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory. Int J Psychophysiol 2007,64(3):233-46. 10.1016/j.ijpsycho.2006.09.009CrossRefPubMed
28.
Zurück zum Zitat Shallice T, Burgess PW: Deficits in strategy application following frontal lobe damage in man. Brain 1991,114(Pt 2):727-741.CrossRefPubMed Shallice T, Burgess PW: Deficits in strategy application following frontal lobe damage in man. Brain 1991,114(Pt 2):727-741.CrossRefPubMed
29.
Zurück zum Zitat Dumontheil I, Gilbert SK, Frith CD, Burgess PW: Recruitment of lateral rostral prefrontal contex in spontaneous and task-related thoughts. Q J Exp Psychol (Hove) 2010, 63: 1740-1756. 10.1080/17470210903538114CrossRef Dumontheil I, Gilbert SK, Frith CD, Burgess PW: Recruitment of lateral rostral prefrontal contex in spontaneous and task-related thoughts. Q J Exp Psychol (Hove) 2010, 63: 1740-1756. 10.1080/17470210903538114CrossRef
30.
Zurück zum Zitat Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K, Cockburn J: Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 2011, 35: 715-728. 10.1016/j.neubiorev.2010.08.008CrossRefPubMed Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K, Cockburn J: Cognitive motor interference while walking: a systematic review and meta-analysis. Neurosci Biobehav Rev 2011, 35: 715-728. 10.1016/j.neubiorev.2010.08.008CrossRefPubMed
31.
Zurück zum Zitat Yogev-Seligmann G, Giladi N, Gruendlinger L, Hausdorff JM: The contribution of postural control and bilateral coordination to the impact of dual tasking on gait. Exp Brain Res 2013, 226: 81-93. 10.1007/s00221-013-3412-9CrossRefPubMed Yogev-Seligmann G, Giladi N, Gruendlinger L, Hausdorff JM: The contribution of postural control and bilateral coordination to the impact of dual tasking on gait. Exp Brain Res 2013, 226: 81-93. 10.1007/s00221-013-3412-9CrossRefPubMed
32.
Zurück zum Zitat Dault MC, Yardley L, Frank JS: Does articulation contribute to modifications of postural control during dual-task paradigms? Brain Res Cogn Brain Res 2003, 16: 434-440. 10.1016/S0926-6410(03)00058-2CrossRefPubMed Dault MC, Yardley L, Frank JS: Does articulation contribute to modifications of postural control during dual-task paradigms? Brain Res Cogn Brain Res 2003, 16: 434-440. 10.1016/S0926-6410(03)00058-2CrossRefPubMed
33.
Zurück zum Zitat Kang HG, Lipsitz LA: Stiffness control of balance during quiet standing and dual task in older adults: the MOBILIZE Boston Study. J Neurophysiol 2010, 104: 3510-3517. 10.1152/jn.00820.2009CrossRefPubMedPubMedCentral Kang HG, Lipsitz LA: Stiffness control of balance during quiet standing and dual task in older adults: the MOBILIZE Boston Study. J Neurophysiol 2010, 104: 3510-3517. 10.1152/jn.00820.2009CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Maki BE, McIlroy WE: Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm 2007, 114: 1279-1296. 10.1007/s00702-007-0764-yCrossRefPubMed Maki BE, McIlroy WE: Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm 2007, 114: 1279-1296. 10.1007/s00702-007-0764-yCrossRefPubMed
35.
Zurück zum Zitat Daffner KR, Mesulam MM, Scinto LF, Acar D, Calvo V, Faust R, Chabrerie A, Kennedy B, Holcomb P: The central role of the prefrontal cortex in directing attention to novel events. Brain 2000,123(Pt 5):927-939.CrossRefPubMed Daffner KR, Mesulam MM, Scinto LF, Acar D, Calvo V, Faust R, Chabrerie A, Kennedy B, Holcomb P: The central role of the prefrontal cortex in directing attention to novel events. Brain 2000,123(Pt 5):927-939.CrossRefPubMed
36.
Zurück zum Zitat Anguera JA, Boccanfuso J, Rintoul JL, Al-Hashimi O, Faraji F, Janowich J, Kong E, Larraburo Y, Rolle C, Johnston E, Gazzaley A: Video game training enhances cognitive control in older adults. Nature 2013, 501: 97-101. 10.1038/nature12486CrossRefPubMedPubMedCentral Anguera JA, Boccanfuso J, Rintoul JL, Al-Hashimi O, Faraji F, Janowich J, Kong E, Larraburo Y, Rolle C, Johnston E, Gazzaley A: Video game training enhances cognitive control in older adults. Nature 2013, 501: 97-101. 10.1038/nature12486CrossRefPubMedPubMedCentral
Metadaten
Titel
Increased frontal brain activation during walking while dual tasking: an fNIRS study in healthy young adults
verfasst von
Anat Mirelman
Inbal Maidan
Hagar Bernad-Elazari
Freek Nieuwhof
Miriam Reelick
Nir Giladi
Jeffrey M Hausdorff
Publikationsdatum
01.12.2014
Verlag
BioMed Central
Erschienen in
Journal of NeuroEngineering and Rehabilitation / Ausgabe 1/2014
Elektronische ISSN: 1743-0003
DOI
https://doi.org/10.1186/1743-0003-11-85

Weitere Artikel der Ausgabe 1/2014

Journal of NeuroEngineering and Rehabilitation 1/2014 Zur Ausgabe