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Effects of aging on the relationship between cognitive demand and step variability during dual-task walking

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An Erratum to this article was published on 10 May 2017

Abstract

A U-shaped relationship between cognitive demand and gait control may exist in dual-task situations, reflecting opposing effects of external focus of attention and attentional resource competition. The purpose of the study was twofold: to examine whether gait control, as evaluated from step-to-step variability, is related to cognitive task difficulty in a U-shaped manner and to determine whether age modifies this relationship. Young and older adults walked on a treadmill without attentional requirement and while performing a dichotic listening task under three attention conditions: non-forced (NF), forced-right (FR), and forced-left (FL). The conditions increased in their attentional demand and requirement for inhibitory control. Gait control was evaluated by the variability of step parameters related to balance control (step width) and rhythmic stepping pattern (step length and step time). A U-shaped relationship was found for step width variability in both young and older adults and for step time variability in older adults only. Cognitive performance during dual tasking was maintained in both young and older adults. The U-shaped relationship, which presumably results from a trade-off between an external focus of attention and competition for attentional resources, implies that higher-level cognitive processes are involved in walking in young and older adults. Specifically, while these processes are initially involved only in the control of (lateral) balance during gait, they become necessary for the control of (fore-aft) rhythmic stepping pattern in older adults, suggesting that attentional resources turn out to be needed in all facets of walking with aging. Finally, despite the cognitive resources required by walking, both young and older adults spontaneously adopted a “posture second” strategy, prioritizing the cognitive task over the gait task.

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References

  • Andersson M, Reinvang I, Wehling E, Hugdhal K, Lundervold AJ (2008) A dichotic listening study of attention control in older adults. Scand J Psychol 49:299–304

    Article  PubMed  Google Scholar 

  • Asbjørnsen A, Hugdahl K (1995) Attentional effects in dichotic listening. Brain Lang 49:189–201

    Article  PubMed  Google Scholar 

  • Asbjørnsen A, Holmefjord A, Reisaeter S, Møller P, Klausen O, Prytz B, Boliek C, Obrzut JE (2000) Lasting auditory attention impairment after persistent middle ear infections: a dichotic listening study. Dev Med Child Neurol 42:481–486

    Article  PubMed  Google Scholar 

  • Aylward GP, Gordon M, Verhulst SJ (1997) Relationships between continuous performance task scores and other cognitive measures: causality or commonality. Assessment 4:325–336

    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

    CAS  PubMed  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  PubMed Central  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 248:196–204

    Article  PubMed  Google Scholar 

  • Bouma A, Gootjes L (2011) Effects of attention on dichotic listening in elderly and patients with dementia of the Alzheimer type. Brain Cogn 76:286–293. doi:10.1016/j.bandc.2011.02.008

    Article  PubMed  Google Scholar 

  • Brach JS, Berlin JE, VanSwearingen JM, Newman AB, Studenski SA (2005) Too much or too little step width variability is associated with a fall history in older persons who walk at or near normal gait speed. J Neuroeng Rehabil 2:21. doi:10.1186/1743-0003-2-21

    Article  PubMed  PubMed Central  Google Scholar 

  • Braver TS, Cohen JD (2000) On the control of control: the role of dopamine in regulating prefrontal function and working memory. In: Monsell S, Driver J (eds) Attention and performance XVIII. MIT Press, Cambridge, MA, pp 713–737

    Google Scholar 

  • Braver TS, Cohen JD, Barch DM (2002) The role of prefrontal cortex in normal and disordered cognitive control: a cognitive neuroscience perspective. In: Stuss DT, Knight RT (eds) Principles of frontal lobe function. Oxford University Press, New York, pp 428–448

    Chapter  Google Scholar 

  • Bryden MP (1988) An overview of the dichotic listening procedure and its relation to cerebral organization. In: Hugdahl K (ed) Handbook of dichotic listening: theory, methods, and research. Wiley & Sons, Chichester, UK, pp 1–44

    Google Scholar 

  • Bryden MP, Munhall K, Allard F (1983) Attentional biases and the right-ear effect in dichotic listening. Brain Lang 18:236–248

    Article  CAS  PubMed  Google Scholar 

  • Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in the anterior cingulate cortex. Trends Cogn Sci 4:215–222

    Article  CAS  PubMed  Google Scholar 

  • Buzzi UH, Stergiou N, Kurz MJ, Hageman PA, Heidel J (2003) Nonlinear dynamics indicates aging affects variability during gait. Clin Biomech 18:435–443

    Article  Google Scholar 

  • Cherry EC (1953) Some experiments on the recognition of speech, with one and with two ears. J Acoust Soc Am 25:975–979

    Article  Google Scholar 

  • Cignetti F, Decker LM, Stergiou N (2012) Sensitivity of the Wolf’s and Rosenstein’s algorithms to evaluate local dynamic stability from small gait data sets: response to commentaries by Bruijn et al. Ann Biomed Eng 40:2507–2509. doi:10.1007/s10439-012-0665-6

    Article  Google Scholar 

  • Decker LM, Cignetti F, Potter JF, Studenski SA, Stergiou N (2012) Use of motor abundance in young and older adults during dual-task treadmill walking. PLoS One 7, e41306. doi:10.1371/journal.pone.0041306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Decker LM, Cignetti F, Stergiou N (2013) Executive function orchestrates regulation of task-relevant gait fluctuations. Gait Posture 38:537–540. doi:10.1016/j.gaitpost.2012.12.018

    Article  PubMed  PubMed Central  Google Scholar 

  • Della Penna S, Brancucci A, Babiloni C, Franciotti R, Pizzella V, Rossi D, Torquati K, Rossini PM, Romani GL (2007) Lateralization of dichotic speech stimuli is based on specific auditory pathway interactions: neuromagnetic evidence. Cereb Cortex 17:2303–2311

    Article  PubMed  Google Scholar 

  • Diamond A (2013) Executive functions. Annu Rev Psychol 64:135–168. doi:10.1146/annurev-psych-113011-143750

    Article  PubMed  Google Scholar 

  • Dingwell JB, Cusumano JP (2015) Identifying stride-to-stride control strategies in human treadmill walking. PLoS One 10, e0124879. doi:10.1371/journal.pone.0124879

    Article  PubMed  PubMed Central  Google Scholar 

  • Dingwell JB, Cusumano JP, Cavanagh PR, Sternad D (2001) Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. J Biomech Eng 123:27–32

    Article  CAS  PubMed  Google Scholar 

  • Dingwell JB, John J, Cusumano JP (2010) Do humans optimally exploit redundancy to control step variability in walking? PLoS Comput Biol 6, e1000856. doi:10.1371/journal.pcbi.1000856

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubost V, Kressig RW, Gonthier R, Herrmann FR, Aminian K, Najafi B, Beauchet O (2006) Relationships between dual-task related changes in stride velocity and stride time variability in healthy older adults. Hum Movement Sci 25:372–382

    Article  Google Scholar 

  • Dubost V, Annweiler C, Aminian K, Najafi B, Herrmann FR, Beauchet O (2008) Stride-to-stride variability while enumerating animal names among healthy young adults: result of stride velocity or effect of attention-demanding task? Gait Posture 27:138–143

    Article  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Foundas AL, Corey DM, Hurley MM, Heilman KM (2006) Verbal dichotic listening in right and left-handed adults: laterality effects of directed attention. Cortex 42:79–86

    Article  PubMed  Google Scholar 

  • Gabell A, Nayak US (1984) The effect of age on variability in gait. J Gerontol 39:662–666

    Article  CAS  PubMed  Google Scholar 

  • Grabiner MD, Troy KL (2005) Attention demanding tasks during treadmill walking reduce step width variability in young adults. J Neuroeng Rehabil 2:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Griggs RA, Platt RD, Newstead SE, Jackson SL (1998) Attentional factors in a disjunctive reasoning task. Think Reason 4:1–14

    Article  Google Scholar 

  • Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J Neuroeng Rehabil 2:19

    Article  PubMed  PubMed Central  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  CAS  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. doi:10.1093/gerona/glq077

    Article  PubMed  Google Scholar 

  • Hill KD, Schwarz JA, Kalogeropoulos AJ, Gibson SJ (1996) Fear of falling revisited. Arch Phys Med Rehabil 77:1025–1029

    Article  CAS  PubMed  Google Scholar 

  • Hollman JH, Kovash FM, Kubik JJ, Linbo RA (2007) Age-related differences in spatiotemporal markers of gait stability during dual task walking. Gait Posture 26:113–119

    Article  PubMed  Google Scholar 

  • Holtzer R, Wang C, Verghese J (2014) Performance variance on walking while talking tasks: theory, findings, and clinical implications. Age (Dordr) 36:373–381. doi:10.1007/s11357-013-9570-7

    Article  Google Scholar 

  • Hugdahl K (2003) Dichotic listening in the study of auditory laterality. In: Hugdahl K, Davidson RJ (eds) The asymmetrical brain. MIT Press, Cambridge, MA, pp 441–476

    Google Scholar 

  • Hugdahl K, Andersson L (1986) The “forced-attention paradigm” in dichotic listening to CV-syllables: a comparison between adults and children. Cortex 22:417–432

    Article  CAS  PubMed  Google Scholar 

  • Hugdahl K, Westerhausen R, Alho K, Medvedev S, Laine M, Hämäläinen H (2009) Attention and cognitive control: unfolding the dichotic listening story. Scand J Psychol 50:11–22. doi:10.1111/j.1467-9450.2008.00676.x

    Article  PubMed  Google Scholar 

  • Hunt E, Lansman M (1986) Unified model of attention and problem solving. Psychol Rev 93:446–461

    Article  Google Scholar 

  • Huxhold O, Li SC, Schmiedek F, Lindenberger U (2006) Dual tasking postural control. Aging and the effects of cognitive demand in conjunction with focus of attention. Brain Res Bull 69:294–305

    Article  PubMed  Google Scholar 

  • Jordan K, Challis JH, Newell KM (2007) Walking speed influences on gait cycle variability. Gait Posture 26:128–134

    Article  PubMed  Google Scholar 

  • Kang HG, Dingwell JB (2008) Separating the effects of age and walking speed on gait variability. Gait Posture 27:572–577

    Article  PubMed  Google Scholar 

  • Kimura D (1961) Cerebral dominance and the perception of verbal stimuli. Can J Psychol 15:166–171

    Article  Google Scholar 

  • Kinsbourne M (1970) The cerebral basis of lateral asymmetries in attention. Acta Psychol (Amst) 33:193–201

    Article  CAS  Google Scholar 

  • Kinsbourne M (1975) The mechanism of hemispheric control of the lateral gradient of attention. In: Rabbitt PMA, Dornic S (eds) Attention and performance V. Academic, London, New York

    Google Scholar 

  • Kressig RW, Herrmann FR, Grandjean R, Michel JP, Beauchet O (2008) Gait variability while dual-tasking: fall predictor in older inpatients? Aging Clin Exp Res 20:123–130

    Article  PubMed  Google Scholar 

  • Li KZ, Lindenberger U (2002) Relations between aging sensory/sensorimotor and cognitive functions. Neurosci Biobehav Rev 26:777–783

    Article  PubMed  Google Scholar 

  • Lindenberger U, Baltes PB (1994) Sensory functioning and intelligence in old age: a strong connection. Psychol Aging 9:339–355

    Article  CAS  PubMed  Google Scholar 

  • Lövdén M, Schaefer S, Pohlmeyer AE, Lindenberger U (2008) Walking variability and working memory load in aging: a dual-process account relating cognitive control to motor control performance. J Gerontol B Psychol Sci Soc Sci 63:P121–P128

    Article  PubMed  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–212

    Article  CAS  PubMed  Google Scholar 

  • Monaco M, Costa A, Caltagirone C, Carlesimo GA (2013) Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci 34:749–754. doi:10.1007/s10072-012-1130-x

    Article  PubMed  Google Scholar 

  • Montero-Odasso M, Muir SW, Hall M, Doherty TJ, Kloseck M, Beauchet O, Speechley M (2011) Gait variability is associated with frailty in community-dwelling older adults. J Gerontol A Biol Sci Med Sci 66:568–576. doi:10.1093/gerona/glr007

    Article  PubMed  Google Scholar 

  • Newell KM, Corcos DM (1993) Issues in variability and motor control. In: Newell KM, Corcos DM (eds) Variability and motor control. Human Kinetics, Champaign, IL, pp 1–12

    Google Scholar 

  • Nigg BM, Cole GK, Nachbauer W (1993) Effects of arch height of the foot on angular motion of the lower extremities in running. J Biomech 26:909–916

    Article  CAS  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Owings TM, Grabiner MD (2004) Variability of step kinematics in young and older adults. Gait Posture 20:26–29

    Article  PubMed  Google Scholar 

  • Redfern MS, Jennings JR, Martin C, Furman JM (2001) Attention influences sensory integration for postural control in older adults. Gait Posture 14:211–216

    Article  CAS  PubMed  Google Scholar 

  • Redfern MS, Jennings JR, Mendelson D, Nebes RD (2009) Perceptual inhibition is associated with sensory integration in standing postural control among older adults. J Gerontol B Psychol Sci Soc Sci 64:P569–P576. doi:10.1093/geronb/gbp060

    Article  Google Scholar 

  • Schaefer S, Huxhold O, Lindenberger U (2006) Healthy mind in healthy body? A review of sensorimotor-cognitive interdependencies in old age. Eur Rev Aging Phys Act 3:45–54

    Article  Google Scholar 

  • Schaefer S, Lövdén M, Wieckhorst B, Lindenberger U (2010) Cognitive performance is improved while walking: differences in cognitive-sensorimotor couplings between children and young adults. Eur J Dev Psychol 7:371–389

    Article  Google Scholar 

  • Schaefer S, Jagenow D, Verrel J, Lindenberger U (2015) The influence of cognitive load and walking speed on gait regularity in children and young adults. Gait Posture 41:258–262. doi:10.1016/j.gaitpost.2014.10.013

    Article  PubMed  Google Scholar 

  • Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34:721–733. doi:10.1016/j.neubiorev.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  • Sheikh JI, Yesavage JA (1986) Geriatric Depression Scale (GDS) (1986): recent evidence and development of a shorter version. In: Brink TL (ed) Clinical gerontology: a guide to assessment and intervention. The Haworth Press, Binghamton, NY, pp 165–173

    Google Scholar 

  • Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM (2006) Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Movement Disord 21:950–957

    Article  PubMed  Google Scholar 

  • Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–661

    Article  Google Scholar 

  • Tervaniemi M, Hugdahl K (2003) Lateralization of auditory-cortex functions. Brain Res Brain Res Rev 43:231–246

    Article  PubMed  Google Scholar 

  • Thomsen T, Rimol LM, Ersland L, Hugdahl K (2004) Dichotic listening reveals functional specificity in prefrontal cortex: an fMRI study. Neuroimage 21:211–218

    Article  PubMed  Google Scholar 

  • Vaughan C, Davis B, O’Connor J (1999) Dynamics of human gait. Kiboho Publishers, Cape Town, South Africa

    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  PubMed Central  Google Scholar 

  • Verghese J, Holtzer R, Lipton RB, Wang C (2009) Quantitative gait markers and incident fall risk in older adults. J Gerontol Med Sci 64:896–901. doi:10.1093/gerona/glp033

    Article  Google Scholar 

  • Verrel J, Lövdén M, Schellenbach M, Schaefer S, Lindenberger U (2009) Interacting effects of cognitive load and adult age on the regularity of whole-body motion during treadmill walking. Psychol Aging 24:75–81. doi:10.1037/a0014272

    Article  PubMed  Google Scholar 

  • Wechsler D (1981) Wechsler Adult Intelligence Scale—3rd edition. Psychological Corporation, San Antonio, TX

    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-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. doi:10.2522/ptj.20090043

    Article  PubMed  PubMed Central  Google Scholar 

  • Yogev-Seligmann G, Hausdorff JM, Giladi N (2012a) Do we always prioritize balance when walking? Towards an integrated model of task prioritization. Mov Disord 27:765–770. doi:10.1002/mds.24963

    Article  PubMed  Google Scholar 

  • Yogev-Seligmann G, Rotem-Galili Y, Dickstein R, Giladi N, Hausdorff JM (2012b) Effects of explicit prioritization on dual task walking in patients with Parkinson’s disease. Gait Posture 35:641–646. doi:10.1016/j.gaitpost.2011.12.016

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the National Institute on Aging at the National Institutes of Health (1K99AG033684). The authors are very grateful to Sharon Lynn Salhi, Ph.D., for presubmission editorial assistance.

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Authors and Affiliations

  1. UMR-S 1075 COMETE (Mobilités: Attention, Orientation, Chronobiologie) INSERM and Université de Caen Normandie, Pôle des Formations et de Recherche en Santé, 2 rue des Rochambelles, 14032, Caen Cedex 5, France

    Leslie M. Decker

  2. University of Nebraska at Omaha, Biomechanics Research Building, 6160 University Drive, Omaha, NE, 68182-0860, USA

    Leslie M. Decker & Nicholas Stergiou

  3. UMR 7291 CNRS and Aix-Marseille Université, 3 place Victor-Hugo, 13331, Marseille Cedex 3, France

    Fabien Cignetti

  4. Department of Integrative Biology, University of California, Berkeley, 3040 Valley Life Sciences Building #3140, Berkeley, CA, 94720-3140, USA

    Nathaniel Hunt

  5. Division of Geriatrics and Gerontology, University of Nebraska Medical Center, 986155 Nebraska Medical Center, Omaha, NE, 68198-6155, USA

    Jane F. Potter

  6. Translational Gerontology Branch, Longitudinal Studies Section, National Institute on Aging, 251 Bayview Blvd., Suite 100, Rm 04B316, Baltimore, MD, 21224, USA

    Stephanie A. Studenski

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  1. Leslie M. Decker
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  2. Fabien Cignetti
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  3. Nathaniel Hunt
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  6. Stephanie A. Studenski
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Correspondence to Leslie M. Decker.

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An erratum to this article is available at http://dx.doi.org/10.1007/s11357-017-9974-x.

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Decker, L.M., Cignetti, F., Hunt, N. et al. Effects of aging on the relationship between cognitive demand and step variability during dual-task walking. AGE 38, 363–375 (2016). https://doi.org/10.1007/s11357-016-9941-y

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