Skip to main content

Advertisement

SpringerLink
Log in

Older but not younger adults rely on multijoint coordination to stabilize the swinging limb when performing a novel cued walking task

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Motor flexibility, the ability to employ multiple motor strategies to meet task demands, may facilitate ambulation in complex environments that constrain movements; loss of motor flexibility may impair mobility. The purpose of this study was to determine the effects of obesity (a specific model of mobility impairment) and advanced age on motor flexibility during a task that constrained foot placement while walking. Twenty-one community-dwelling obese (OB) and 25 normal weight (NW) older adults (46 total older adults—OA) and 10 younger adults (YA) walked normally on a treadmill (baseline) then walked while stepping on lighted cues projected onto the treadmill at locations corresponding to average foot placement during normal walking (cued). The uncontrolled manifold (UCM) analysis was used to partition total variance in a set of seven lower-limb segment angles into components that did (“bad” variance) and did not (“good” variance) affect step-to-step variance in the trajectory of the swing foot. Motor flexibility was operationalized as an increase (baseline to cued) in total variance with an increase in good variance that exceeded the change in bad variance. There was no significant group × walking task interaction for total and good variance for OB vs NW, but there was a strong and significant interaction effect for OA vs YA (p < 0.01; Cohen’s d > 1.0). Whereas YA reduced both good and bad variance, OA increased good variance beyond the change in bad variance. In OA, these changes were associated with several functional measures of mobility. Cued walking may place greater demands on OA requiring greater reliance on motor flexibility, although otherwise healthy older obese adults may be able to compensate for functional and cognitive declines associated with obesity by increasing motor flexibility under such tasks. The extent to which motor flexibility is employed during novel or constrained tasks may be a biomarker of healthy aging and a target for (re)habilitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arvin M, Hoozemans M, Pijnappels M, Duysens J, Verschueren SMP, Van Dieen J (2018) Where to step? Contributions of stance leg muscle spindle afference to planning of mediolateral foot placement for balance control in young and older adults. Front Physiol 9:1134

    Article  PubMed  PubMed Central  Google Scholar 

  • Auyang AG, Chang Y-H (2013) Effects of a foot placement constraint on use of motor equivalence during human hopping. PLoS ONE 8:e69429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bauby CE, Kuo AD (2000) Active control of lateral balance in human walking. J Biomech 33:1433–1440

    Article  CAS  PubMed  Google Scholar 

  • Berg WP, Murdock LA (2011) Age-related differences in locomotor targeting performance under structural interference. Age Ageing 40:324–329

    Article  PubMed  Google Scholar 

  • Bernstein N (1966) The co-ordination and regulation of movements. The co-ordination and regulation of movements.

  • Bischof GN, Park DC (2015) Obesity and aging: consequences for cognition, brain structure, and brain function. Psychosom Med 77:697–709

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruijn SM, Van Dieën JH (2018) Control of human gait stability through foot placement. J R Soc Interface 15:20170816

    Article  PubMed  PubMed Central  Google Scholar 

  • Chien J, Yentes J, Stergiou N, and Siu K-C (2015) The effect of walking speed on gait variability in healthy young, middle-aged and elderly individuals. J Phys Activity Nutr Rehabilit 2015.

  • Christou EA (2011) Aging and variability of voluntary contractions. Exerc Sport Sci Rev 39:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Christou EA, Shinohara M, Enoka RM (2003) Fluctuations in acceleration during voluntary contractions lead to greater impairment of movement accuracy in old adults. J Appl Physiol 95:373–384

    Article  PubMed  Google Scholar 

  • Davis RB III, Ounpuu S, Tyburski D, Gage JR (1991) A gait analysis data collection and reduction technique. Hum Mov Sci 10:575–587

    Article  Google Scholar 

  • De Stefano F, Zambon S, Giacometti L, Sergi G, Corti M, Manzato E, Busetto L (2015) Obesity, muscular strength, muscle composition and physical performance in an elderly population. J Nutr Health Aging 19:785–791

    Article  PubMed  Google Scholar 

  • Dite W, Temple VA (2002) A clinical test of stepping and change of direction to identify multiple falling older adults. Arch Phys Med Rehabil 83:1566–1571

    Article  PubMed  Google Scholar 

  • Donelan JM, Shipman DW, Kram R, Kuo AD (2004) Mechanical and metabolic requirements for active lateral stabilization in human walking. J Biomech 37:827–835

    Article  PubMed  Google Scholar 

  • Durgin FH, Gigone K, Scott R (2005) Perception of visual speed while moving. J Exp Psychol Hum Percept Perform 31:339

    Article  PubMed  Google Scholar 

  • Dutta GG, Freitas SMSF, Scholz JP (2013) Diminished joint coordination with aging leads to more variable hand paths. Hum Mov Sci 32:768–784

    Article  PubMed  PubMed Central  Google Scholar 

  • Eckardt N, Rosenblatt NJ (2018) Healthy aging does not impair lower extremity motor flexibility while walking across an uneven surface. Hum Mov Sci 62:67–80

    Article  PubMed  Google Scholar 

  • Eckardt N, Rosenblatt NJ (2019) Instability resistance training decreases motor noise during challenging walking tasks in older adults: a 10-week double-blinded RCT. Front Aging Neurosci 11:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Freitas SM, Scholz JP, Latash ML (2010) Analyses of joint variance related to voluntary whole-body movements performed in standing. J Neurosci Methods 188:89–96

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedman J, Varadhan S, Zatsiorsky VM, Latash ML (2009) The sources of two components of variance: an example of multifinger cyclic force production tasks at different frequencies. Exp Brain Res 196:263–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Fritz S, Lusardi M (2009) White paper: “walking speed: the sixth vital sign”. J Geriat Phys Ther 32:2–5

    Article  Google Scholar 

  • Gaul D, Mat A, O'Shea D, Issartel J (2016) Impaired visual motor coordination in obese adults. J Obes 2016:6178575

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaul D, Fernandez L, Issartel J (2018) "It ain't what you do, it's the way that you do it": does obesity affect perceptual motor control ability of adults on the speed and accuracy of a discrete aiming task? Exp Brain Res 236:2703–2711

    Article  PubMed  Google Scholar 

  • Gera G, Freitas S, Latash M, Monahan K, Schoner G, Scholz J (2010) Motor abundance contributes to resolving multiple kinematic task constraints. Mot Control 14:83–115

    Article  Google Scholar 

  • Goble DJ, Coxon JP, Wenderoth N, Van Impe A, Swinnen SP (2009) Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33:271–278

    Article  PubMed  Google Scholar 

  • Gonzalez M, Gates DH, Rosenblatt NJ (2020) The impact of obesity on gait stability in older adults. J Biomech 100:109585

    Article  PubMed  Google Scholar 

  • Goodman SR, Shim JK, Zatsiorsky VM, Latash ML (2005) Motor variability within a multi-effector system: experimental and analytical studies of multi-finger production of quick force pulses. Exp Brain Res 163:75–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Greve C, Zijlstra W, Hortobágyi T, Bongers RM (2013) Not all is lost: old adults retain flexibility in motor behaviour during sit-to-stand. PLoS ONE 8:e77760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greve C, Hortobágyi T, Bongers RM (2017) Old adults preserve motor flexibility during rapid reaching. Eur J Appl Physiol 117:955–967

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamer M, Batty GD (2019) Association of body mass index and waist-to-hip ratio with brain structure: UK biobank study. Neurology 92:e594–e600

    Article  PubMed  Google Scholar 

  • Herrmann MJ, Tesar AK, Beier J, Berg M, Warrings B (2019) Grey matter alterations in obesity: a meta-analysis of whole-brain studies. Obes Rev 20:464–471

    Article  PubMed  Google Scholar 

  • Hess RJ, Brach JS, Piva SR, VanSwearingen JM (2010) Walking skill can be assessed in older adults: validity of the Figure-of-8 Walk Test. Phys Ther 90:89–99

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsu W-L, Scholz JP (2012) Motor abundance supports multitasking while standing. Hum Mov Sci 31:844–862

    Article  PubMed  Google Scholar 

  • Hsu W-L, Chou L-S, Woollacott M (2013) Age-related changes in joint coordination during balance recovery. Age 35:1299–1309

    Article  PubMed  Google Scholar 

  • Hsu W-L, Lin K-H, Yang R-S, Cheng C-H (2014) Use of motor abundance in old adults in the regulation of a narrow-based stance. Eur J Appl Physiol 114:261–271

    Article  PubMed  Google Scholar 

  • Jonsson E, Seiger Å, Hirschfeld H (2004) One-leg stance in healthy young and elderly adults: a measure of postural steadiness? Clin Biomech 19:688–694

    Article  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 

  • Kang HG, Dingwell JB (2009) Dynamics and stability of muscle activations during walking in healthy young and older adults. J Biomech 42:2231–2237

    Article  PubMed  PubMed Central  Google Scholar 

  • Krishnan V, Rosenblatt NJ, Latash ML, Grabiner MD (2013) The effects of age on stabilization of the mediolateral trajectory of the swing foot. Gait Posture 38:923–928

    Article  PubMed  Google Scholar 

  • Kubinski SN, McQueen CA, Sittloh KA, Dean JC (2015) Walking with wider steps increases stance phase gluteus medius activity. Gait Posture 41:130–135

    Article  PubMed  Google Scholar 

  • Kuhman D, Hammond KG, Hurt CP (2018a) Altered joint kinetic strategies of healthy older adults and individuals with Parkinson’s disease to walk at faster speeds. J Biomech 79:112–118

    Article  PubMed  Google Scholar 

  • Kuhman D, Willson J, Mizelle J, DeVita P (2018b) The relationships between physical capacity and biomechanical plasticity in old adults during level and incline walking. J Biomech 69:90–96

    Article  PubMed  Google Scholar 

  • Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5

    Article  PubMed  PubMed Central  Google Scholar 

  • Latash ML (2018) Abundant degrees of freedom are not a problem. Kinesiol Rev 7:64–72

    Article  Google Scholar 

  • Latash ML, Shim JK, Smilga AV, Zatsiorsky VM (2005) A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model. Biol Cybern 92:186–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Latash ML, Scholz JP, Schoner G (2007) Toward a new theory of motor synergies. Mot Control 11:276–308

    Article  Google Scholar 

  • Lerner ZF, Board WJ, Browning RC (2014) Effects of an obesity-specific marker set on estimated muscle and joint forces in walking. Med Sci Sports Exerc 46:1261–1267

    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 

  • Liu ZQ, Yang F (2017) Obesity may not induce dynamic stability disadvantage during overground walking among young adults. PLoS ONE 12:e0169766

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Madigan M, Rosenblatt NJ, Grabiner MD (2014) Obesity as a factor contributing to falls by older adults. Curr Obes Rep 3:348–354

    Article  PubMed  Google Scholar 

  • Martin V, Reimann H, Schöner G (2019) A process account of the uncontrolled manifold structure of joint space variance in pointing movements. Biol Cybern 113:293–307

    Article  PubMed  PubMed Central  Google Scholar 

  • Mattos DJ, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106:1424–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCrum C, Willems P, Karamanidis K, Meijer K (2019) Stability-normalised walking speed: a new approach for human gait perturbation research. J Biomech 87:48–53

    Article  PubMed  Google Scholar 

  • Oshita K, Yano S (2010) Relationship between force fluctuation in the plantar flexor and sustainable time for single-leg standing. J Physiol Anthropol 29:89–93

    Article  PubMed  Google Scholar 

  • Owings TM, Grabiner MD (2004) Step width variability, but not step length variability or step time variability, discriminates gait of healthy young and older adults during treadmill locomotion. J Biomech 37:935–938

    Article  PubMed  Google Scholar 

  • Park E, Reimann H, Schoner G (2016) Coordination of muscle torques stabilizes upright standing posture: an UCM analysis. Exp Brain Res 234:1757–1767

    Article  PubMed  Google Scholar 

  • Peper CL, Oorthuizen JK, Roerdink M (2012) Attentional demands of cued walking in healthy young and elderly adults. Gait Posture 36:378–382

    Article  PubMed  Google Scholar 

  • Poston B, Enoka JA, Enoka RM (2008) Endpoint accuracy for a small and a large hand muscle in young and old adults during rapid, goal-directed isometric contractions. Exp Brain Res 187:373–385

    Article  PubMed  Google Scholar 

  • Qu X (2012) Uncontrolled manifold analysis of gait variability: effects of load carriage and fatigue. Gait Posture 36:325–329

    Article  PubMed  Google Scholar 

  • Raji CA, Ho AJ, Parikshak NN, Becker JT, Lopez OL, Kuller LH, Hua X, Leow AD, Toga AW, Thompson PM (2010) Brain structure and obesity. Hum Brain Mapp 31:353–364

    PubMed  PubMed Central  Google Scholar 

  • Rankin BL, Buffo SK, Dean JC (2014) A neuromechanical strategy for mediolateral foot placement in walking humans. J Neurophysiol 112:374–383

    Article  PubMed  PubMed Central  Google Scholar 

  • Reimann H, Schoner G (2017) A multi-joint model of quiet, upright stance accounts for the "uncontrolled manifold" structure of joint variance. Biol Cybern 111:389–403

    Article  PubMed  PubMed Central  Google Scholar 

  • Robert T, Zatsiorsky VM, Latash ML (2008) Multi-muscle synergies in an unusual postural task: quick shear force production. Exp Brain Res 187:237–253

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenblatt NJ, Hurt CP (2019) Recommendation for the minimum number of steps to analyze when performing the uncontrolled manifold analysis on walking data. J Biomech 85:218–223

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenblatt NJ, Bauer A, Rotter D, Grabiner MD (2014a) Active dorsiflexing prostheses may reduce trip-related fall risk in people with transtibial amputation. J Rehabil Res Dev 51:1229–1242

    Article  PubMed  Google Scholar 

  • Rosenblatt NJ, Hurt CP, Latash ML, Grabiner MD (2014b) An apparent contradiction: increasing variability to achieve greater precision? Exp Brain Res 232:403–413

    Article  PubMed  Google Scholar 

  • Rosenblatt NJ, Latash ML, Hurt CP, Grabiner MD (2015) Challenging gait leads to stronger lower-limb kinematic synergies: the effects of walking within a more narrow pathway. Neurosci Lett 600:110–114

    Article  CAS  PubMed  Google Scholar 

  • Scarpina F, Migliorati D, Marzullo P, Mauro A, Scacchi M, Costantini M (2016) Altered multisensory temporal integration in obesity. Sci Rep 6:28382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholz JP, Schoner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306

    Article  CAS  PubMed  Google Scholar 

  • Shumway-Cook A, Woollacott M, Kerns KA, Baldwin M (1997) The effects of two types of cognitive tasks on postural stability in older adults with and without a history of falls. J Gerontol A Biol Sci Med Sci 52:M232–240

    Article  CAS  PubMed  Google Scholar 

  • Shumway-Cook A, Brauer S, Woollacott M (2000) Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther 80:896–903

    Article  CAS  PubMed  Google Scholar 

  • Stergiou N, Harbourne R, Cavanaugh J (2006) Optimal movement variability: a new theoretical perspective for neurologic physical therapy. J Neurol Phys Ther 30:120–129

    Article  PubMed  Google Scholar 

  • Studenski S, Perera S, Patel K, Rosano C, Faulkner K, Inzitari M, Brach J, Chandler J, Cawthon P, Connor EB, Nevitt M, Visser M, Kritchevsky S, Badinelli S, Harris T, Newman AB, Cauley J, Ferrucci L, Guralnik J (2011) Gait speed and survival in older adults. JAMA 305:50–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Yoshida H, Kim H, Yukawa H, Sugiura M, Furuna T, Nishizawa S, Kumagai S, Shinkai S, Ishizaki T (2003) Walking speed as a good predictor for maintenance of I-ADL among the rural community elderly in Japan: a 5-year follow-up study from TMIG-LISA. Geriatr Gerontol Int 3:S6–S14

    Article  Google Scholar 

  • Teasdale N, Simoneau M, Corbeil P, Handrigan G, Tremblay A, Hue O (2013) Obesity alters balance and movement control. Curr Obes Rep 2:235–240

    Article  Google Scholar 

  • Verrel J (2010) Distributional properties and variance-stabilizing transformations for measures of uncontrolled manifold effects. J Neurosci Methods 191:166–170

    Article  PubMed  Google Scholar 

  • Wang C, Chan JS, Ren L, Yan JH (2016) Obesity reduces cognitive and motor functions across the lifespan. Neural Plast 2016:2473081

    PubMed  PubMed Central  Google Scholar 

  • Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3(Suppl):1212–1217

    Article  CAS  PubMed  Google Scholar 

  • Yabe Y, Taga G (2008) Treadmill locomotion captures visual perception of apparent motion. Exp Brain Res 191:487–494

    Article  PubMed  Google Scholar 

  • Yamada M, Higuchi T, Tanaka B, Nagai K, Uemura K, Aoyama T, Ichihashi N (2011) Measurements of stepping accuracy in a multitarget stepping task as a potential indicator of fall risk in elderly individuals. J Gerontol Series A 66:994–1000

    Article  Google Scholar 

  • Yamagata M, Tateuchi H, Shimizu I, Ichihashi N (2019) The effects of fall history on kinematic synergy during walking. J Biomech 82:204–210

    Article  PubMed  Google Scholar 

  • Zhang W, Scholz JP, Zatsiorsky VM, Latash ML (2008) What do synergies do? Effects of secondary constraints on multidigit synergies in accurate force-production tasks. J Neurophysiol 99:500–513

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Michael Hurt, Gon Saman and Clarisse Pelaez for their assistance in recruiting young participants and collecting and processing the data.

Funding

Research reported in this publication was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases under Award Number 1R03AR066326-01A1 and the National Institute of Diabetes and Digestive and Kidney under Award Number 2T35DK07439. The content in this publication is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Dr. William M. Scholl College of Podiatric Medicine’s Center for Lower Extremity Ambulatory Research (CLEAR), Rosalind Franklin University of Medicine and Science, 3333 Green Bay Road, North Chicago, IL, 60064, USA

    Noah J. Rosenblatt

  2. Department of Sport and Movement Science, Institute of Sport Science, Carl Von Ossietzky University of Oldenburg, Oldenburg, Germany

    Nils Eckardt

  3. Department for Exercise and Health, Institute of Sport Science, Leibniz University Hannover, Hannover, Germany

    Nils Eckardt

  4. Rehabilitation Science, The University of Alabama at Birmingham, Birmingham, AL, USA

    Daniel Kuhman & Christopher P. Hurt

  5. Department of Physical Therapy, The University of Alabama at Birmingham, Birmingham, AL, USA

    Christopher P. Hurt

Authors
  1. Noah J. Rosenblatt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nils Eckardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Kuhman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher P. Hurt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Noah J. Rosenblatt.

Ethics declarations

Conflict of interest

There are no conflicts of interest to declare.

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent to publish

The authors affirm that human research participants provided informed consent for publication of the images in Fig. 1.

Additional information

Communicated by Francesco Lacquaniti.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rosenblatt, N.J., Eckardt, N., Kuhman, D. et al. Older but not younger adults rely on multijoint coordination to stabilize the swinging limb when performing a novel cued walking task. Exp Brain Res 238, 1441–1454 (2020). https://doi.org/10.1007/s00221-020-05822-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-020-05822-x

Keywords

Search

Navigation