Predictive and Reactive Locomotor Adaptability in Healthy Elderly: A Systematic Review and Meta-Analysis

Sebastian Bohm, Lida Mademli, Falk Mersmann, Adamantios Arampatzis, Sebastian Bohm, Lida Mademli, Falk Mersmann, Adamantios Arampatzis

Abstract

Background: Locomotor adaptability is based on the implementation of error-feedback information from previous perturbations to predictively adapt to expected perturbations (feedforward) and to facilitate reactive responses in recurring unexpected perturbations ('savings'). The effect of aging on predictive and reactive adaptability is yet unclear. However, such understanding is fundamental for the design and application of effective interventions targeting fall prevention.

Methods: We systematically searched the Web of Science, MEDLINE, Embase and Science Direct databases as well as the reference lists of the eligible articles. A study was included if it addressed an investigation of the locomotor adaptability in response to repeated mechanical movement perturbations of healthy older adults (≥60 years). The weighted average effect size (WAES) of the general adaptability (adaptive motor responses to repeated perturbations) as well as predictive (after-effects) and reactive adaptation (feedback responses to a recurring unexpected perturbation) was calculated and tested for an overall effect. A subgroup analysis was performed regarding the factor age group [i.e., young (≤35 years) vs. older adults]. Furthermore, the methodological study quality was assessed.

Results: The review process yielded 18 studies [1009 participants, 613 older adults (70 ± 4 years)], which used various kinds of locomotor tasks and perturbations. The WAES for the general locomotor adaptability was 1.21 [95% confidence interval (CI) 0.68-1.74, n = 11] for the older and 1.39 (95% CI 0.90-1.89, n = 10) for the young adults with a significant (p < 0.05) overall effect for both age groups and no significant subgroup differences. Similar results were found for the predictive (older: WAES 1.10, 95% CI 0.37-1.83, n = 8; young: WAES 1.54, 95% CI 0.11-2.97, n = 7) and reactive (older: WAES 1.09, 95% CI 0.22-1.96, n = 5; young: WAES 1.35, 95% CI 0.60-2.09, n = 5) adaptation featuring significant (p < 0.05) overall effects without subgroup differences. The average score of the methodological quality was 67 ± 8 %.

Conclusions: The present meta-analysis provides elaborate statistical evidence that locomotor adaptability in general and predictive and reactive adaptation in particular remain highly effective in the elderly, showing only minor, not statistically significant age-related deficits. Consequently, interventions which use adaptation and learning paradigms including the application of the mechanisms responsible for an effective predictive and reactive dynamic stability control may progressively improve older adults' recovery performance and, thus, reduce their risk of falling.

Figures

Fig. 1
Fig. 1
Flowchart of the systematic review process
Fig. 2
Fig. 2
Forest plots for the meta-analysis of human locomotor adaptability in response to repeated perturbations. The general adaptive potential displayed here includes the predictive and reactive components. The footnotes explain the data from the original study used for the present analysis. CI confidence interval, IV inverse variance, SMD standardized mean difference, TD touchdown
Fig. 3
Fig. 3
Forest plot of the effect of predictive adaptation on locomotion. The footnotes explain the data from the original study used for the present analysis. CI confidence interval, H hard surface (unperturbed), IV inverse variance, NS-1 non-slip trial (unperturbed), SD standard deviation, SMD standardized mean difference, TD touchdown
Fig. 4
Fig. 4
Forest plot of the effect of reactive adaptation on the response to repeated unexpected locomotor perturbations. The footnotes explain the data from the original study used for the present analysis. CI confidence interval, IV inverse variance, SMD standardized mean difference, TD touchdown

References

    1. Patla AE. Strategies for dynamic stability during adaptive human locomotion. IEEE Eng Med Biol Mag. 2003;22:48–52. doi: 10.1109/MEMB.2003.1195695.
    1. Massion J. Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol. 1992;38:35–56. doi: 10.1016/0301-0082(92)90034-C.
    1. Talbot LA, Musiol RJ, Witham EK, et al. Falls in young, middle-aged and older community dwelling adults: perceived cause, environmental factors and injury. BMC Public Health. 2005;5:86. doi: 10.1186/1471-2458-5-86.
    1. Berg WP, Alessio HM, Mills EM, et al. Circumstances and consequences of falls in independent community-dwelling older adults. Age Ageing. 1997;26:261–268. doi: 10.1093/ageing/26.4.261.
    1. Blake AJ. Falls by elderly people at home: prevalence and associated factors. Age Ageing. 1988;17:365–372. doi: 10.1093/ageing/17.6.365.
    1. Tinetti ME, Speechley M, Ginter SF. Risk-factors for falls among elderly persons living in the community. N Engl J Med. 1988;319:1701–1707. doi: 10.1056/NEJM198812293192604.
    1. Formiga F, Ferrer A, Duaso E, et al. Falls in nonagenarians living in their own homes: the NonaSantfeliu study. J Nutr Health Aging. 2008;12:273–276. doi: 10.1007/BF02982633.
    1. Shumway-Cook A, Woollacott M. Motor control. Philadelphia: Lippincott Williams & Wilkins; 2007.
    1. Heinrich S, Rapp K, Rissmann U, et al. Cost of falls in old age: a systematic review. Osteoporos Int. 2010;21:891–902. doi: 10.1007/s00198-009-1100-1.
    1. Bunn F, Dickinson A, Simpson C, et al. Preventing falls among older people with mental health problems: a systematic review. BMC Nurs. 2014;13:4. doi: 10.1186/1472-6955-13-4.
    1. Marks R. Falls Injuries: causes, consequences, and prevention. Open Longev Sci. 2011;5:1–2.
    1. Miall RC, Wolpert DM. Forward models for physiological motor control. Neural Netw. 1996;9:1265–1279. doi: 10.1016/S0893-6080(96)00035-4.
    1. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108. doi: 10.1146/annurev-neuro-060909-153135.
    1. Hof AL. The equations of motion for a standing human reveal three mechanisms for balance. J Biomech. 2007;40:451–457. doi: 10.1016/j.jbiomech.2005.12.016.
    1. Marigold DS, Patla AE. Strategies for dynamic stability during locomotion on a slippery surface: effects of prior experience and knowledge. J Neurophysiol. 2002;88:339–353.
    1. Bierbaum S, Peper A, Karamanidis K, et al. Adaptational responses in dynamic stability during disturbed walking in the elderly. J Biomech. 2010;43:2362–2368. doi: 10.1016/j.jbiomech.2010.04.025.
    1. Bierbaum S, Peper A, Karamanidis K, et al. Adaptive feedback potential in dynamic stability during disturbed walking in the elderly. J Biomech. 2011;44:1921–1926. doi: 10.1016/j.jbiomech.2011.04.027.
    1. Jacobs JV, Horak FB. Cortical control of postural responses. J Neural Transm. 2007;114:1339–1348. doi: 10.1007/s00702-007-0657-0.
    1. Seidler RD, Bernard JA, Burutolu TB, et al. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev. 2010;34:721–733. doi: 10.1016/j.neubiorev.2009.10.005.
    1. Bishop NA, Lu T, Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature. 2010;464:529–535. doi: 10.1038/nature08983.
    1. Kennedy R, Clemis J. The geriatric auditory and vestibular systems. Otolaryngol Clin N Am. 1990;23:1075–1082.
    1. Sloane P, Baloh R, Honrubia V. The vestibular system in the elderly—clinical implications. Am J Otolaryngol. 1989;10:422–429. doi: 10.1016/0196-0709(89)90038-0.
    1. Robbins S, Waked E, McClaran J. Proprioception and stability: foot position awareness as a function of age and footwear. Age Ageing. 1995;24:67–72. doi: 10.1093/ageing/24.1.67.
    1. Stelmach GE, Worringham CJ. Sensorimotor deficits related to postural stability. Implications for falling in the elderly. Clin Geriatr Med. 1985;1:679–694.
    1. Karamanidis K, Arampatzis A. Mechanical and morphological properties of different muscle-tendon units in the lower extremity and running mechanics: effect of aging and physical activity. J Exp Biol. 2005;208:3907–3923. doi: 10.1242/jeb.01830.
    1. Mademli L, Arampatzis A. Mechanical and morphological properties of the triceps surae muscle-tendon unit in old and young adults and their interaction with a submaximal fatiguing contraction. J Electromyogr Kinesiol. 2008;18:89–98. doi: 10.1016/j.jelekin.2006.09.008.
    1. Mademli L, Arampatzis A. Effect of voluntary activation on age-related muscle fatigue resistance. J Biomech. 2008;41:1229–1235. doi: 10.1016/j.jbiomech.2008.01.019.
    1. Yue GH, Ranganathan VK, Siemionow V, et al. Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A Biol Sci Med Sci. 1999;54:M249–M253. doi: 10.1093/gerona/54.5.M249.
    1. Hortobágyi T, Zheng D, Weidner M, et al. The influence of aging on muscle strength and muscle fiber characteristics with special reference to eccentric strength. J Gerontol A Biol Sci Med Sci. 1995;50A:B399–B406. doi: 10.1093/gerona/50A.6.B399.
    1. Thelen DG, Wojcik LA, Schultz AB, et al. Age differences in using a rapid step to regain balance during a forward fall. J Gerontol A Biol Sci Med Sci. 1997;52A:M8–M13. doi: 10.1093/gerona/52A.1.M8.
    1. Mademli L, Arampatzis A, Karamanidis K. Dynamic stability control in forward falls: postural corrections after muscle fatigue in young and older adults. Eur J Appl Physiol. 2008;103:295–306. doi: 10.1007/s00421-008-0704-z.
    1. Karamanidis K, Arampatzis A. Age-related degeneration in leg-extensor muscle–tendon units decreases recovery performance after a forward fall: compensation with running experience. Eur J Appl Physiol. 2006;99:73–85. doi: 10.1007/s00421-006-0318-2.
    1. Shadmehr R, Mussa-Ivaldi F. Adaptive representation of dynamics during learning of a motor task. J Neurosci. 1994;14:3208–3224.
    1. Morton SM, Bastian AJ. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci. 2006;26:9107–9116. doi: 10.1523/JNEUROSCI.2622-06.2006.
    1. Lackner JR, DiZio P. Visual stimulation affects the perception of voluntary leg movements during walking. Perception. 1988;17:71–80. doi: 10.1068/p170071.
    1. Bohm S, Mersmann F, Bierbaum S, et al. Cognitive demand and predictive adaptational responses in dynamic stability control. J Biomech. 2012;45:2330–2336. doi: 10.1016/j.jbiomech.2012.07.009.
    1. Pai YC, Wening JD, Runtz EF, et al. Role of feedforward control of movement stability in reducing slip-related balance loss and falls among older adults. J Neurophysiol. 2003;90:755–762. doi: 10.1152/jn.01118.2002.
    1. Pavol MJ, Pai YC. Feedforward adaptations are used to compensate for a potential loss of balance. Exp Brain Res. 2002;145:528–538. doi: 10.1007/s00221-002-1143-4.
    1. Pai YC, Iqbal K. Simulated movement termination for balance recovery: can movement strategies be sought to maintain stability in the presence of slipping or forced sliding? J Biomech. 1999;32:779–786. doi: 10.1016/S0021-9290(99)00074-3.
    1. Pavol MJ, Runtz EF, Pai Y-C. Young and older adults exhibit proactive and reactive adaptations to repeated slip exposure. J Gerontol A Biol Sci Med Sci. 2004;59:494–502. doi: 10.1093/gerona/59.5.M494.
    1. van der Linden MH, Marigold DS, Gabreels FJM, et al. Muscle reflexes and synergies triggered by an unexpected support surface height during walking. J Neurophysiol. 2007;97:3639–3650. doi: 10.1152/jn.01272.2006.
    1. Hussain SJ, Hanson AS, Tseng S-C, et al. A locomotor adaptation including explicit knowledge and removal of postadaptation errors induces complete 24-hour retention. J Neurophysiol. 2013;110:916–925. doi: 10.1152/jn.00770.2012.
    1. Kojima Y, Iwamoto Y, Yoshida K. Memory of learning facilitates saccadic adaptation in the monkey. J Neurosci. 2004;24:7531–7539. doi: 10.1523/JNEUROSCI.1741-04.2004.
    1. Smith MA, Ghazizadeh A, Shadmehr R. Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol. 2006;4:e179. doi: 10.1371/journal.pbio.0040179.
    1. Herzfeld DJ, Vaswani PA, Marko MK, et al. A memory of errors in sensorimotor learning. Science. 2014;345:1349–1353. doi: 10.1126/science.1253138.
    1. Pavol MJ, Runtz EF, Edwards BJ, et al. Age influences the outcome of a slipping perturbation during initial but not repeated exposures. J Gerontol A Biol Sci Med Sci. 2002;57:M496–M503. doi: 10.1093/gerona/57.8.M496.
    1. Tseng Y, Diedrichsen J, Krakauer JW, et al. Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol. 2007;98:54–62. doi: 10.1152/jn.00266.2007.
    1. Jayaram G, Tang B, Pallegadda R, et al. Modulating locomotor adaptation with cerebellar stimulation. J Neurophysiol. 2012;107:2950–2957. doi: 10.1152/jn.00645.2011.
    1. Jayaram G, Galea JM, Bastian AJ, et al. Human locomotor adaptive learning is proportional to depression of cerebellar excitability. Cereb Cortex N Y N. 1991;2011(21):1901–1909.
    1. Weiner MJ, Hallett M, Funkenstein HH. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology. 1983;33:766–772. doi: 10.1212/WNL.33.6.766.
    1. Scheidt RA, Zimbelman JL, Salowitz NMG, et al. Remembering forward: neural correlates of memory and prediction in human motor adaptation. NeuroImage. 2012;59:582–600. doi: 10.1016/j.neuroimage.2011.07.072.
    1. Diedrichsen J, Hashambhoy Y, Rane T, et al. Neural correlates of reach errors. J Neurosci. 2005;25:9919–9931. doi: 10.1523/JNEUROSCI.1874-05.2005.
    1. Herzfeld DJ, Pastor D, Haith AM, et al. Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. Neuroimage. 2014;98:147–158. doi: 10.1016/j.neuroimage.2014.04.076.
    1. Seidler RD, Noll DC, Chintalapati P. Bilateral basal ganglia activation associated with sensorimotor adaptation. Exp Brain Res. 2006;175:544–555. doi: 10.1007/s00221-006-0571-y.
    1. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia. 2003;41:252–262. doi: 10.1016/S0028-3932(02)00158-6.
    1. Raz N, Lindenberger U, Rodrigue KM, et al. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex. 2005;15:1676–1689. doi: 10.1093/cercor/bhi044.
    1. Luft AR, Skalej M, Schulz JB, et al. Patterns of age-related shrinkage in cerebellum and brainstem observed in vivo using three-dimensional MRI volumetry. Cereb Cortex. 1999;9:712–721. doi: 10.1093/cercor/9.7.712.
    1. Hogan MJ. The cerebellum in thought and action: a fronto-cerebellar aging hypothesis. New Ideas Psychol. 2004;22:97–125. doi: 10.1016/j.newideapsych.2004.09.002.
    1. Raz N, Rodrigue KM, Kennedy KM, et al. Differential aging of the human striatum: longitudinal evidence. AJNR Am J Neuroradiol. 2003;24:1849–1856.
    1. Bäckman L, Lindenberger U, Li S-C, Nyberg L. Linking cognitive aging to alterations in dopamine neurotransmitter functioning: recent data and future avenues. Neurosci Biobehav Rev. 2010;34:670–677. doi: 10.1016/j.neubiorev.2009.12.008.
    1. Yang F, Pai Y-C. Alteration in community-dwelling older adults’ level walking following perturbation training. J Biomech. 2013;46:2463–2468. doi: 10.1016/j.jbiomech.2013.07.025.
    1. Roemmich RT, Nocera JR, Stegemöller EL, et al. Locomotor adaptation and locomotor adaptive learning in Parkinson’s disease and normal aging. Clin Neurophysiol. 2014;125:313–319. doi: 10.1016/j.clinph.2013.07.003.
    1. Bruijn SM, Impe AV, Duysens J, et al. Split-belt walking: adaptation differences between young and older adults. J Neurophysiol. 2012;108:1149–1157. doi: 10.1152/jn.00018.2012.
    1. Chambers AJ, Cham R. Slip-related muscle activation patterns in the stance leg during walking. Gait Posture. 2007;25:565–572. doi: 10.1016/j.gaitpost.2006.06.007.
    1. Cohen J. Statistical power analysis for the behavioral sciences. Psychology Press; 1988.
    1. Deeks JJ, Higgins JP, Altman DG. Analysing Data and Undertaking Meta-Analyses. In: Fellow JPHSSV, Director SGF, editors. Cochrane Handbook for Systematic Reviews of Interventions. Hoboken: John Wiley & Sons; 2008. p. 243–96.
    1. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to meta-analysis. Hoboken: Wiley; 2011.
    1. Cooper H. Research synthesis and meta-analysis: a step-by-step approach. 4. Thousand Oaks: Sage Publications, Inc; 2010.
    1. Deeks JJ, Altman DG, Bradburn MJ. Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger M, Smith GD, Altman DG, editors. Systematic reviews in healthcare. Chichester: BMJ Publishing Group; 2001. pp. 285–312.
    1. Deeks J, Higgins J. Statistical algorithms in Review Manager 5. Statistical Methods Group of The Cochrane Collaboration; 2010. Available from: . Accessed 25 June 2015.
    1. Pai Y-C, Bhatt T, Wang E, et al. Inoculation against falls: rapid adaptation by young and older adults to slips during daily activities. Arch Phys Med Rehabil. 2010;91:452–459. doi: 10.1016/j.apmr.2009.10.032.
    1. Bhatt T, Yang F, Pai Y-C. Learning to resist gait-slip falls: long-term retention in community-dwelling older adults. Arch Phys Med Rehabil. 2012;93:557–564. doi: 10.1016/j.apmr.2011.10.027.
    1. Pai Y-C, Yang F, Bhatt T, et al. Learning from laboratory-induced falling: long-term motor retention among older adults. Age. 2014;36:1367–1376. doi: 10.1007/s11357-014-9640-5.
    1. Pai Y-C, Bhatt T, Yang F, et al. Perturbation training can reduce community-dwelling older adults’ annual fall risk: a randomized controlled trial. J Gerontol A Biol Sci Med Sci. 2014;69:1586–1594. doi: 10.1093/gerona/glu087.
    1. Higgins JPT, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560. doi: 10.1136/bmj.327.7414.557.
    1. The Cochrane Collaboration . Review manager (RevMan) Copenhagen: The Nordic Cochrane Centre; 2012.
    1. Higgins JP, Green S, editors. Cochrane handbook for systematic reviews of interventions. Hoboken: Wiley; 2008.
    1. Oates AR, Van Ooteghem K, Frank JS, et al. Adaptation of gait termination on a slippery surface in Parkinson’s disease. Gait Posture. 2013;37:516–520. doi: 10.1016/j.gaitpost.2012.09.002.
    1. Smeesters C, Hayes WC, McMahon TA. Disturbance type and gait speed affect fall direction and impact location. J Biomech. 2001;34:309–317. doi: 10.1016/S0021-9290(00)00200-1.
    1. Hatada Y, Miall RC, Rossetti Y. Two waves of a long-lasting aftereffect of prism adaptation measured over 7 days. Exp Brain Res. 2006;169:417–426. doi: 10.1007/s00221-005-0159-y.
    1. Karamanidis K, Sueptitz F, Catala MM, et al. Reactive response and adaptive modifications in dynamic stability to changes in lower limb dynamics in the elderly while walking. In: Dremstrup K, Rees S, Jensen O, editors. 15th Nord.-Balt. Conf. Biomed. Eng. Med. Phys. Nbc 2011. New York: Springer; 2011. p. 268–70.
    1. Karamanidis K, Arampatzis A, Mademli L. Age-related deficit in dynamic stability control after forward falls is affected by muscle strength and tendon stiffness. J Electromyogr Kinesiol. 2008;18:980–989. doi: 10.1016/j.jelekin.2007.04.003.
    1. Grabiner MD, Owings TA, Pavol MJ. Lower extremity strength plays only a small role in determining the maximum recoverable lean angle in older adults. J Gerontol Ser Biol Sci Med Sci. 2005;60:1447–1450. doi: 10.1093/gerona/60.11.1447.
    1. Pavol MJ, Owings TM, Foley KT, et al. Influence of lower extremity strength of healthy older adults on the outcome of an induced trip. J Am Geriatr Soc. 2002;50:256–262. doi: 10.1046/j.1532-5415.2002.50056.x.
    1. Arampatzis A, Karamanidis K, Mademli L. Deficits in the way to achieve balance related to mechanisms of dynamic stability control in the elderly. J Biomech. 2008;41:1754–1761. doi: 10.1016/j.jbiomech.2008.02.022.
    1. Vandervoort AA, Chesworth BM, Cunningham DA, et al. An outcome measure to quantify passive stiffness of the ankle. Can J Public Health Rev Can Santé Publique. 1992;83(Suppl 2):S19–S23.
    1. Verrillo RT. Age-related-changes in the sensitivity to vibration. J Gerontol. 1980;35:185–193. doi: 10.1093/geronj/35.2.185.
    1. Rankin JK, Woollacott MH, Shumway-Cook A, et al. Cognitive influence on postural stability. J Gerontol A Biol Sci Med Sci. 2000;55:M112–M119. doi: 10.1093/gerona/55.3.M112.
    1. Brown LA, Shumway-Cook A, Woollacott MH. Attentional demands and postural recovery: the effects of aging. J Gerontol A Biol Sci Med Sci. 1999;54:M165–M171. doi: 10.1093/gerona/54.4.M165.
    1. Martin TA, Keating JG, Goodkin HP, et al. Throwing while looking through prisms. Brain. 1996;119:1199–1211. doi: 10.1093/brain/119.4.1199.
    1. Thoroughman KA, Shadmehr R. Electromyographic correlates of learning an internal model of reaching movements. J Neurosci. 1999;19:8573–8588.
    1. Miall RC, Christensen LOD, Cain O, et al. Disruption of state estimation in the human lateral cerebellum. PLoS Biol. 2007;5:e316. doi: 10.1371/journal.pbio.0050316.
    1. Tanaka H, Sejnowski TJ, Krakauer JW. Adaptation to visuomotor rotation through interaction between posterior parietal and motor cortical areas. J Neurophysiol. 2009;102:2921–2932. doi: 10.1152/jn.90834.2008.
    1. King BR, Fogel SM, Albouy G, et al. Neural correlates of the age-related changes in motor sequence learning and motor adaptation in older adults. Front Hum Neurosci. 2013;7:142. doi: 10.3389/fnhum.2013.00142.
    1. Shadmehr R, Holcomb HH. Inhibitory control of competing motor memories. Exp Brain Res. 1999;126:235–251. doi: 10.1007/s002210050733.
    1. Kaasinen V, Rinne JO. Functional imaging studies of dopamine system and cognition in normal aging and Parkinson’s disease. Neurosci Biobehav Rev. 2002;26:785–793. doi: 10.1016/S0149-7634(02)00065-9.
    1. Swanson LR, Lee TD. Effects of aging and schedules of knowledge of results on motor learning. J Gerontol. 1992;47:P406–P411. doi: 10.1093/geronj/47.6.P406.
    1. Carnahan HC, Vandervoort AA, Swanson LR. The influence of summary knowledge of results and aging on motor learning. Res Q Exerc Sport. 1996;67:280–287. doi: 10.1080/02701367.1996.10607955.
    1. Wishart LR, Lee TD. Effects of aging and reduced relative frequency of knowledge of results on learning a motor skill. Percept Mot Skills. 1997;84:1107–1122. doi: 10.2466/pms.1997.84.3.1107.
    1. Schiffman JM, Luchies CW, Richards LG, et al. The effects of age and feedback on isometric knee extensor force control abilities. Clin Biomech. 2002;17:486–493. doi: 10.1016/S0268-0033(02)00041-4.
    1. Berghuis KMM, Veldman MP, Solnik S, et al. Neuronal mechanisms of motor learning and motor memory consolidation in healthy old adults. Age. 2015;37:1–18. doi: 10.1007/s11357-015-9779-8.
    1. Ooteghem KV, Frank JS, Allard F, et al. Aging does not affect generalized postural motor learning in response to variable amplitude oscillations of the support surface. Exp Brain Res. 2010;204:505–514. doi: 10.1007/s00221-010-2316-1.
    1. Cai L, Chan JSY, Yan JH, et al. Brain plasticity and motor practice in cognitive aging. Front Aging Neurosci. 2014;6:31. doi: 10.3389/fnagi.2014.00031.
    1. Arampatzis A, Peper A, Bierbaum S. Exercise of mechanisms for dynamic stability control increases stability performance in the elderly. J Biomech. 2011;44:52–58. doi: 10.1016/j.jbiomech.2010.08.023.
    1. Aragão FA, Karamanidis K, Vaz MA, et al. Mini-trampoline exercise related to mechanisms of dynamic stability improves the ability to regain balance in elderly. J Electromyogr Kinesiol. 2011;21:512–518. doi: 10.1016/j.jelekin.2011.01.003.
    1. Bierbaum S, Peper A, Arampatzis A. Exercise of mechanisms of dynamic stability improves the stability state after an unexpected gait perturbation in elderly. Age. 2013;35:1905–1915. doi: 10.1007/s11357-012-9481-z.
    1. Lindemann U, Najafi B, Zijlstra W, et al. Distance to achieve steady state walking speed in frail elderly persons. Gait Posture. 2008;27:91–96. doi: 10.1016/j.gaitpost.2007.02.005.
    1. Moreno Catalá M, Woitalla D, Arampatzis A. Recovery performance and factors that classify young fallers and non-fallers in Parkinson’s disease. Hum Mov Sci. 2015;41:136–46.
    1. Fernández-Ruiz J, Díaz R. Prism adaptation and aftereffect: specifying the properties of a procedural memory system. Learn Mem. 1999;6:47–53.
    1. Lindemann U, Klenk J, Becker C, et al. Assessment of adaptive walking performance. Med Eng Phys. 2013;35:217–220. doi: 10.1016/j.medengphy.2012.11.005.
    1. Sturnieks DL, Menant J, Vanrenterghem J, et al. Sensorimotor and neuropsychological correlates of force perturbations that induce stepping in older adults. Gait Posture. 2012;36:356–360. doi: 10.1016/j.gaitpost.2012.03.007.
    1. van Hedel HJA, Dietz V. The influence of age on learning a locomotor task. Clin Neurophysiol. 2004;115:2134–2143. doi: 10.1016/j.clinph.2004.03.029.
    1. Sakai M, Shiba Y, Sato H, et al. Motor adaptation during slip-perturbed gait in older adults. J Phys Ther Sci. 2008;20:109–115. doi: 10.1589/jpts.20.109.
    1. Tseng S-C, Stanhope SJ, Morton SM. Visuomotor adaptation of voluntary step initiation in older adults. Gait Posture. 2010;31:180–184. doi: 10.1016/j.gaitpost.2009.10.001.

Source: PubMed

3
S'abonner