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The contribution of postural control and bilateral coordination to the impact of dual tasking on gait

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Abstract

The simultaneous performance of a cognitive task while walking typically alters the gait pattern. In some populations, these alterations have been associated with an increased risk of falls, motivating study of this response from the clinical perspective. The mechanisms responsible for these effects are not fully understood. The concurrent requirement to control upright posture and stepping, a bilaterally coordinated rhythmic task, may be the cause of this so-called dual-tasking effect. To evaluate this possibility, the present study was designed to isolate the individual contribution of these two demands by assessing the effects of cognitive loading on standing (i.e., postural control without bilateral coordination of stepping), cycling (i.e., bilateral coordination similar to stepping, but with minimal postural demands), and walking. We also investigated the effects of aging and parkinsonism on the performance of these three tasks in response to cognitive loading, also referred to as a dual task. Twenty-one healthy young adults, 15 healthy older adults, and 18 patients with Parkinson’s disease were assessed while walking, standing, and cycling, with and without an additional cognitive load. In the young adults, the performance on the two motor tasks that involved bilateral coordination deteriorated significantly in response to the dual task, while standing was not impacted. Similar results, although less robust, were observed among the healthy older adults. In contrast, among the patients with Parkinson’s disease, the dual-task costs, i.e., the impact of the simultaneously performed cognitive task on the gait pattern, were high in all motor tasks. These findings suggest that walking is especially vulnerable to cognitive loading, in part, because of the unique sensitivity of bilateral coordination of limb movements to the effects of dual tasking.

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Abbreviations

CV:

Coefficient of variation

FAB:

Frontal assessment battery

TMT:

Trail making test

UPDRS:

Unified Parkinson’s Disease Rating Scale

References

  • Bakker M, Verstappen CC, Bloem BR, Toni I (2007) Recent advances in functional neuroimaging of gait. J Neural Transm 114:1323–1331

    Article  PubMed  CAS  Google Scholar 

  • Beauchet O, Dubost V, Aminian K, Gonthier R, Kressig RW (2005a) Dual-task-related gait changes in the elderly: does the type of cognitive task matter? J Mot Behav 37:259–264

    PubMed  CAS  Google Scholar 

  • Beauchet O, Dubost V, Herrmann FR, Kressig RW (2005b) Stride-to-stride variability while backward counting among healthy young adults. J Neuroeng Rehabil 2:26

    Article  PubMed  Google Scholar 

  • Ble A, Volpato S, Zuliani G, Guralnik JM, Bandinelli S, Lauretani F, Bartali B, Maraldi C, Fellin R, Ferrucci L (2005) Executive function correlates with walking speed in older persons: the InCHIANTI study. J Am Geriatr Soc 53:410–415

    Article  PubMed  Google Scholar 

  • Bloem BR, Valkenburg VV, Slabbekoorn M, van Dijk JG (2001a) The multiple tasks test. Strategies in Parkinson’s disease. Exp Brain Res 137:478–486

    Article  PubMed  CAS  Google Scholar 

  • Bloem BR, Valkenburg VV, Slabbekoorn M, Willemsen MD (2001b) The Multiple Tasks Test: development and normal strategies. Gait Posture 14:191–202

    Article  PubMed  CAS  Google Scholar 

  • Bloem BR, Grimbergen YA, van Dijk JG, Munneke M (2006) The “posture second” strategy: a review of wrong priorities in Parkinson’s disease. J Neurol Sci 251:87–90

    Article  PubMed  Google Scholar 

  • Bond JM, Morris M (2000) Goal-directed secondary motor tasks: their effects on gait in subjects with Parkinson disease. Arch Phys Med Rehabil 81:110–116

    PubMed  CAS  Google Scholar 

  • Bootsma-van der Wiel A, Gussekloo J, de Craen AJ, van Exel E, Bloem BR, Westendorp RG (2003) Walking and talking as predictors of falls in the general population: the Leiden 85-Plus Study. J Am Geriatr Soc 51:1466–1471

    Article  PubMed  Google Scholar 

  • Camicioli R, Oken BS, Sexton G, Kaye JA, Nutt JG (1998) Verbal fluency task affects gait in Parkinson’s disease with motor freezing. J Geriatr Psychiatry Neurol 11:181–185

    PubMed  CAS  Google Scholar 

  • Christensen LO, Johannsen P, Sinkjaer T, Petersen N, Pyndt HS, Nielsen JB (2000) Cerebral activation during bicycle movements in man. Exp Brain Res 135:66–72

    Article  PubMed  CAS  Google Scholar 

  • Dault MC, Frank JS, Allard F (2001) Influence of a visuo-spatial, verbal and central executive working memory task on postural control. Gait Posture 14:110–116

    Article  PubMed  CAS  Google Scholar 

  • de Bruin ED, Schmidt A (2010) Walking behaviour of healthy elderly: attention should be paid. Behav Brain Funct 6:59

    Article  PubMed  Google Scholar 

  • Donoghue OA, Cronin H, Savva GM, O’Regan C, Kenny RA (2012) Effects of fear of falling and activity restriction on normal and dual task walking in community dwelling older adults. Gait Posture. http://dx.doi.org/10.1016/j.gaitpost.2012.10.023

  • Dubois B, Slachevsky A, Litvan I, Pillon B (2000) The FAB: a frontal assessment battery at bedside. Neurology 55:1621–1626

    Article  PubMed  CAS  Google Scholar 

  • Ebersbach G, Dimitrijevic MR, Poewe W (1995) Influence of concurrent tasks on gait: a dual-task approach. Percept Mot Skills 81:107–113

    Article  PubMed  CAS  Google Scholar 

  • Fahn S (1987) Members of the UPDRS Developmental Committee. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Health Care Information, Florham Park, pp 153–163 (Elton R)

  • Frenkel-Toledo S, Giladi N, Peretz C, Herman T, Gruendlinger L, Hausdorff JM (2005) Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson’s disease. Mov Disord 20:1109–1114

    Article  PubMed  Google Scholar 

  • Galletly R, Brauer SG (2005) Does the type of concurrent task affect preferred and cued gait in people with Parkinson’s disease? Aust J Physiother 51:175–180

    Article  PubMed  Google Scholar 

  • Gelb DJ, Oliver E, Gilman S (1999) Diagnostic criteria for Parkinson disease. Arch Neurol 56:33–39

    Article  PubMed  CAS  Google Scholar 

  • Goldberger AL, Amaral LA, Hausdorff JM, Ivanov PC, Peng CK, Stanley HE (2002) Fractal dynamics in physiology: alterations with disease and aging. Proc Natl Acad Sci USA 99(Suppl 1):2466–2472

    Article  PubMed  Google Scholar 

  • Hausdorff JM, Mitchell SL, Firtion R, Peng CK, Cudkowicz ME, Wei JY, Goldberger AL (1997) Altered fractal dynamics of gait: reduced stride-interval correlations with aging and Huntington’s disease. J Appl Physiol 82:262–269

    PubMed  CAS  Google Scholar 

  • Hausdorff JM, Lertratanakul A, Cudkowicz ME, Peterson AL, Kaliton D, Goldberger AL (2000) Dynamic markers of altered gait rhythm in amyotrophic lateral sclerosis. J Appl Physiol 88:2045–2053

    PubMed  CAS  Google Scholar 

  • Hausdorff JM, Rios DA, Edelberg HK (2001) Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 82:1050–1056

    Article  PubMed  CAS  Google Scholar 

  • Hausdorff JM, Lowenthal J, Herman T, Gruendlinger L, Peretz C, Giladi N (2007) Rhythmic auditory stimulation modulates gait variability in Parkinson’s disease. Eur J Neurosci 26:2369–2375

    Article  PubMed  Google Scholar 

  • Hausdorff JM, Schweiger A, Herman T, Yogev-Seligmann G, Giladi N (2008) Dual-task decrements in gait: contributing factors among healthy older adults. J Gerontol A Biol Sci Med Sci 63:1335–1343

    Article  PubMed  Google Scholar 

  • Herman T, Mirelman A, Giladi N, Schweiger A, Hausdorff JM (2010) Executive control deficits as a prodrome to falls in healthy older adults: a prospective study linking thinking, walking, and falling. J Gerontol A Biol Sci Med Sci 65:1086–1092

    Article  PubMed  Google Scholar 

  • Kave G (2005a) Phonemic fluency, semantic fluency, and difference scores: normative data for adult Hebrew speakers. J Clin Exp Neuropsychol 27:690–699

    Article  PubMed  Google Scholar 

  • Kave G (2005b) Standardization and norms for a Hebrew naming test. Brain Lang 92:204–211

    Article  PubMed  Google Scholar 

  • Kelly VE, Eusterbrock AJ, Shumway-Cook A (2012) A review of dual-task walking deficits in people with Parkinson’s disease: motor and cognitive contributions, mechanisms, and clinical implications. Parkinsons Dis 2012:918719

    PubMed  Google Scholar 

  • Kerr B, Condon SM, McDonald LA (1985) Cognitive spatial processing and the regulation of posture. J Exp Psychol Hum Percept Perform 11:617–622

    Article  PubMed  CAS  Google Scholar 

  • Lezak MD (1995) Neuropsychological assessment. Oxford University Press, Inc., New York

    Google Scholar 

  • Li KZ, Lindenberger U, Freund AM, Baltes PB (2001) Walking while memorizing: age-related differences in compensatory behavior. Psychol Sci 12:230–237

    Article  PubMed  CAS  Google Scholar 

  • Li KZ, Abbud GA, Fraser SA, Demont RG (2012) Successful adaptation of gait in healthy older adults during dual-task treadmill walking. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 19:150–167

    Article  PubMed  Google Scholar 

  • Lindenberger U, Marsiske M, Baltes PB (2000) Memorizing while walking: increase in dual-task costs from young adulthood to old age. Psychol Aging 15:417–436

    Article  PubMed  CAS  Google Scholar 

  • Lundin-Olsson L, Nyberg L, Gustafson Y (1997) “Stops walking when talking” as a predictor of falls in elderly people. Lancet 349:617

    Article  PubMed  CAS  Google Scholar 

  • Maylor EA, Wing AM (1996) Age differences in postural stability are increased by additional cognitive demands. J Gerontol B Psychol Sci Soc Sci 51:143–154

    Article  Google Scholar 

  • McNevin NH, Wulf G, Carlson C (2000) Effects of attentional focus, self-control, and dyad training on motor learning: implications for physical rehabilitation. Phys Ther 80:373–385

    PubMed  CAS  Google Scholar 

  • Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N, Hausdorff JM (2011) Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci 66:234–240

    Article  PubMed  Google Scholar 

  • Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, Tsunazawa Y, Suzuki T, Yanagida T, Kubota K (2001) Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 14:1186–1192

    Article  PubMed  CAS  Google Scholar 

  • 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 53:695–699

    Article  PubMed  Google Scholar 

  • Nieuwboer A, Kwakkel G, Rochester L, Jones D, van Wegen E, Willems AM, Chavret F, Hetherington V, Baker K, Lim I (2007) Cueing training in the home improves gait-related mobility in Parkinson’s disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 78:134–140

    Article  PubMed  CAS  Google Scholar 

  • O’Shea S, Morris ME, Iansek R (2002) Dual task interference during gait in people with Parkinson disease: effects of motor versus cognitive secondary tasks. Phys Ther 82:888–897

    PubMed  Google Scholar 

  • Perry J (1992) Gait analysis: normal and pathological function. SLACK Incorporate, Thorofare

    Google Scholar 

  • Pichierri G, Wolf P, Murer K, de Bruin ED (2011) Cognitive and cognitive-motor interventions affecting physical functioning: a systematic review. BMC Geriatr 11:29

    Article  PubMed  Google Scholar 

  • Pichierri G, Coppe A, Lorenzetti S, Murer K, de Bruin ED (2012) The effect of a cognitive-motor intervention on voluntary step execution under single and dual task conditions in older adults: a randomized controlled pilot study. Clin Interv Aging 7:175–184

    Article  PubMed  Google Scholar 

  • Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148

    PubMed  CAS  Google Scholar 

  • Rochester L, Hetherington V, Jones D, Nieuwboer A, Willems AM, Kwakkel G, Van WE (2005) The effect of external rhythmic cues (auditory and visual) on walking during a functional task in homes of people with Parkinson’s disease. Arch Phys Med Rehabil 86:999–1006

    Article  PubMed  Google Scholar 

  • Segev-Jacubovski O, Herman T, Yogev-Seligmann G, Mirelman A, Giladi N, Hausdorff JM (2011) The interplay between gait, falls and cognition: can cognitive therapy reduce fall risk? Expert Rev Neurother 11:1057–1075

    Article  PubMed  Google Scholar 

  • Silsupadol P, Shumway-Cook A, Lugade V, van Donkelaar P, Chou LS, Mayr U, Woollacott MH (2009) Effects of single-task versus dual-task training on balance performance in older adults: a double-blind, randomized controlled trial. Arch Phys Med Rehabil 90:381–387

    Article  PubMed  Google Scholar 

  • Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM (2005) Dual tasking effects on gait variability: the role of aging, falls and executive function. Mov Disord 21:950–957

    Article  Google Scholar 

  • Stuss DT, Levine B (2002) Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol 53:401–433

    Article  PubMed  Google Scholar 

  • Toledo-Frankel S, Giladi N, Gruendlinger L, Baltadjieva R, Herman T, Hausdorff JM (2004) Treadmill walking as an external cue to improve gait rhythm and stability in Parkinson’s disease. Mov Disord 19:S138–S139

    Google Scholar 

  • Verghese J, Kuslansky G, Holtzer R, Katz M, Xue X, Buschke H, Pahor M (2007) Walking while talking: effect of task prioritization in the elderly. Arch Phys Med Rehabil 88:50–53

    Article  PubMed  Google Scholar 

  • Verghese J, Mahoney J, Ambrose AF, Wang C, Holtzer R (2010) Effect of cognitive remediation on gait in sedentary seniors. J Gerontol A Biol Sci Med Sci 65:1338–1343

    Article  PubMed  Google Scholar 

  • Wang C, Wai Y, Kuo B, Yeh YY, Wang J (2008) Cortical control of gait in healthy humans: an fMRI study. J Neural Transm 115:1149–1158

    Article  PubMed  Google Scholar 

  • Woollacott M, Shumway-Cook A (2002) Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16:1–14

    Article  PubMed  Google Scholar 

  • Wulf G, McNevin NH, Fuchs T, Ritter F, Toole T (2000) Attentional focus in complex skill learning. Res Q Exerc Sport 71:229–239

    Article  PubMed  CAS  Google Scholar 

  • Yang YR, Chen YC, Lee CS, Cheng SJ, Wang RY (2007) Dual-task-related gait changes in individuals with stroke. Gait Posture 25:185–190

    Article  PubMed  Google Scholar 

  • Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM (2005) Dual tasking, gait rhythmicity, and Parkinson’s disease: which aspects of gait are attention demanding? Eur J Neurosci 22:1248–1256

    Article  PubMed  Google Scholar 

  • Yogev G, Plotnik M, Peretz C, Giladi N, Hausdorff JM (2006) Gait asymmetry in patients with Parkinson’s disease and elderly fallers: when does the bilateral coordination of gait require attention? Exp Brain Res 177:336–346

    Article  Google Scholar 

  • Yogev-Seligmann G, Hausdorff JM, Giladi N (2008) The role of executive function and attention in gait. Mov Disord 23:329–342

    Article  PubMed  Google Scholar 

  • Yogev-Seligmann G, Rotem-Galili Y, Mirelman A, Dickstein R, Giladi N, Hausdorff JM (2010) How does explicit prioritization alter walking during dual-task performance? Effects of age and sex on gait speed and variability. Phys Ther 90:177–186

    Article  PubMed  Google Scholar 

  • Yogev-Seligmann G, Giladi N, Brozgol M, Hausdorff JM (2012) A training program to improve gait while dual tasking in patients with Parkinson’s disease: a pilot study. Arch Phys Med Rehabil 93:176–181

    Article  PubMed  Google Scholar 

  • Zanone PG, Monno A, Temprado JJ, Laurent M (2001) Shared dynamics of attentional cost and pattern stability. Hum Mov Sci 20:765–789

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory for Gait Analysis and Neurodynamics, Movement Disorders Unit, Department of Neurology, Tel Aviv Sourasky Medical Center, 6 Weizman Street, 64239, Tel Aviv, Israel

    Galit Yogev-Seligmann, Nir Giladi, Leor Gruendlinger & Jeffrey M. Hausdorff

  2. Faculty of Medicine, The Dr. Miriam and Sheldon G. Adelson Graduate School of Medicine Sackler, Tel-Aviv University, Tel Aviv, Israel

    Galit Yogev-Seligmann

  3. Department of Physical Therapy, Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Jeffrey M. Hausdorff

  4. Department of Medicine, Harvard Medical School, Boston, MA, USA

    Jeffrey M. Hausdorff

  5. Department of Neurology, Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Nir Giladi

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  1. Galit Yogev-Seligmann
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  2. Nir Giladi
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  3. Leor Gruendlinger
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  4. Jeffrey M. Hausdorff
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Correspondence to Jeffrey M. Hausdorff.

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Yogev-Seligmann, G., Giladi, N., Gruendlinger, L. et al. The contribution of postural control and bilateral coordination to the impact of dual tasking on gait. Exp Brain Res 226, 81–93 (2013). https://doi.org/10.1007/s00221-013-3412-9

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