Neural Correlates of Balance Skill Learning in Young and Older Individuals: A Systematic Review and Meta-analysis

. 2024 Jan 07 ; 10 (1) : 3. [epub] 20240107

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu systematický přehled, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38185708
Odkazy

PubMed 38185708
PubMed Central PMC10772137
DOI 10.1186/s40798-023-00668-3
PII: 10.1186/s40798-023-00668-3
Knihovny.cz E-zdroje

BACKGROUND: Despite the increasing number of research studies examining the effects of age on the control of posture, the number of annual fall-related injuries and deaths continues to increase. A better understanding of how old age affects the neural mechanisms of postural control and how countermeasures such as balance training could improve the neural control of posture to reduce falls in older individuals is therefore necessary. The aim of this review is to determine the effects of age on the neural correlates of balance skill learning measured during static (standing) and dynamic (walking) balance tasks in healthy individuals. METHODS: We determined the effects of acute (1-3 sessions) and chronic (> 3 sessions) balance skill training on balance in the trained and in untrained, transfer balance tasks through a systematic review and quantified these effects by robust variance estimation meta-analysis in combination with meta-regression. We systematically searched PubMed, Web of Science, and Cochrane databases. Balance performance and neural plasticity outcomes were extracted and included in the systematic synthesis and meta-analysis. RESULTS: Forty-two studies (n = 622 young, n = 699 older individuals) were included in the systematic synthesis. Seventeen studies with 508 in-analysis participants were eligible for a meta-analysis. The overall analysis revealed that acute and chronic balance training had a large effect on the neural correlates of balance skill learning in the two age groups combined (g = 0.79, p < 0.01). Both age groups similarly improved balance skill performance in 1-3 training sessions and showed little further improvements with additional sessions. Improvements in balance performance mainly occurred in the trained and less so in the non-trained (i.e., transfer) balance tasks. The systematic synthesis and meta-analysis suggested little correspondence between improved balance skills and changes in spinal, cortical, and corticospinal excitability measures in the two age groups and between the time courses of changes in balance skills and neural correlates. CONCLUSIONS: Balance skill learning and the accompanying neural adaptations occur rapidly and independently of age with little to no training dose-dependence or correspondence between behavioral and neural adaptations. Of the five types of neural correlates examined, changes in only spinal excitability seemed to differ between age groups. However, age or training dose in terms of duration did not moderate the effects of balance training on the changes in any of the neural correlates. The behavioral and neural mechanisms of strong task-specificity and the time course of skill retention remain unclear and require further studies in young and older individuals. REGISTRATION: PROSPERO registration number: CRD42022349573.

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

Papegaaij S, Taube W, Baudry S, Otten E, Hortobágyi T. Aging causes a reorganization of cortical and spinal control of posture. Front Aging Neurosci. 2014;6:28. PubMed PMC

Taube W, Gollhofer A. Postural control and balance training. Handb Mot Control Mot Learn. 2013;252–80.

Granacher U, Gollhofer A, Strass D. Training induced adaptations in characteristics of postural reflexes in elderly men. Gait Posture. 2006;24:459–66. PubMed

Hortobágyi T, Teixeira LA, Duysens J, Granacher U, Van Dieën J, Moraes R. Is standing sway an accurate measure of fall risk and predictor of future falls in older adults? Braz J Mot Behav. 2020;14:1–3.

Lesinski M, Hortobágyi T, Muehlbauer T, Gollhofer A, Granacher U. Dose-response relationships of balance training in healthy young adults: a systematic review and meta-analysis. Sport Med. 2015;45:557–76. PubMed

Granacher U, Zahner L, Gollhofer A. Strength, power, and postural control in seniors: considerations for functional adaptations and for fall prevention. Eur J Sport Sci. 2008;8:325–40.

Sherrington C, Fairhall N, Wallbank G, Tiedemann A, Michaleff ZA, Howard K, et al. Exercise for preventing falls in older people living in the community: an abridged Cochrane systematic review. Br J Sports Med. 2020;54:885–91. PubMed

Rapp K, Freiberger E, Todd C, Klenk J, Becker C, Denkinger M, et al. Fall incidence in Germany: results of two population-based studies, and comparison of retrospective and prospective falls data collection methods. BMC Geriatr. 2014;14:4–11. PubMed PMC

Bergen G, Stevens MR, Burns ER. Falls and fall injuries among adults aged ≥ 65 years—United States, 2014. MMWR Morb Mortal Wkly Rep. 2016;65:993–8. PubMed

Granacher U, Muehlbaue T, Zahner L, Gollhofer A, Kressig RW, Muehlbauer T, et al. Comparison of traditional and recent approaches in the promotion of balance and strength in older adults. Sport Med. 2011;41:377–400. PubMed

Granacher U, Gollhofer A, Hortobágyi T, Kressig RW, Muehlbauer T. The importance of trunk muscle strength for balance, functional performance, and fall prevention in seniors: a systematic review. Sport Med. 2013;43:627–41. PubMed

Horak FB. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age Ageing. 2006;35:7–11. PubMed

Dayan E, Cohen LG. Neuroplasticity subserving motor skill learning. Neuron. 2011;72:443–54. PubMed PMC

van Dieën JH, van Leeuwen M, Faber GS. Learning to balance on one leg: motor strategy and sensory weighting. J Neurophysiol. 2015;114:2967–82. PubMed PMC

Alizadehsaravi L, Koster RAJJ, Muijres W, Maas H, Bruijn SM, van Dieën JH, et al. The underlying mechanisms of improved balance after one and ten sessions of balance training in older adults. Hum Mov Sci. 2022;81:1–14. PubMed

Sehm B, Taubert M, Conde V, Weise D, Classen J, Dukart J, et al. Structural brain plasticity in Parkinson’s disease induced by balance training. Neurobiol Aging. 2014;35:232–9. PubMed

Kümmel J, Kramer A, Giboin LS, Gruber M. Specificity of balance training in healthy individuals: a systematic review and meta-analysis. Sport Med. 2016;46:1261–71. PubMed

Egger S, Wälchli M, Rüeger E, Taube W. Interference of balance tasks revisited: consolidation of a novel balance task is impaired by subsequent learning of a similar postural task. Gait Posture. 2021;84:182–6. PubMed

Berghuis KMM, Fagioli S, Maurits NM, Zijdewind I, Marsman JBC, Hortobágyi T, et al. Age-related changes in brain deactivation but not in activation after motor learning. Neuroimage. 2019;186:358–68. PubMed

Bootsma JM, Caljouw SR, Veldman MP, Maurits NM, Rothwell JC, Hortobágyi T. Neural correlates of motor skill learning are dependent on both age and task difficulty. Front Aging Neurosci. 2021;13:1–17. PubMed PMC

Taubert M, Mehnert J, Pleger B, Villringer A. Rapid and specific gray matter changes in M1 induced by balance training. Neuroimage. 2016;133:399–407. PubMed

Schmidt R, Lee T. Motor control and learning: a behavioral emphasis, 6th ed. 2011.

Mellow ML, Goldsworthy MR, Coussens S, Smith AE. Acute aerobic exercise and neuroplasticity of the motor cortex: a systematic review. J Sci Med Sport. 2020;23:408–14. PubMed

Lin T-W, Tsai S-F, Kuo Y-M. Physical exercise enhances neuroplasticity and delays Alzheimer’s disease. Brain Plast. 2018;4:95–110. PubMed PMC

Herold F, Törpel A, Schega L, Müller NG. Functional and/or structural brain changes in response to resistance exercises and resistance training lead to cognitive improvements—a systematic review. Eur Rev Aging Phys Act. 2019;16:1–33. PubMed PMC

Freyler K, Weltin E, Gollhofer A, Ritzmann R. Improved postural control in response to a 4-week balance training with partially unloaded bodyweight. Gait Posture. 2014;40:291–6. PubMed

Gruber M, Taube W, Gollhofer A, Beck S, Amtage F, Schubert M. Training-specific adaptations of H- and stretch reflexes in human soleus muscle. J Mot Behav. 2007;39:68–78. PubMed

Taube W, Gruber M, Beck S, Faist M, Gollhofer A, Schubert M. Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiol (Oxf). 2007;189:347–58. PubMed

Beck S, Taube W, Gruber M, Amtage F, Gollhofer A, Schubert M. Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Res. 2007;1179:51–60. PubMed

Schubert M, Beck S, Taube W, Amtage F, Faist M, Gruber M. Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci. 2008;27:2007–18. PubMed

Esculier JF, Vaudrin J, Tremblay LE. Corticomotor excitability in Parkinson’s disease during observation, imagery and imitation of action: effects of rehabilitation using wii fit and comparison to healthy controls. J Parkinsons Dis. 2014;4:67–75. PubMed

Taubert M, Lohmann G, Margulies DS, Villringer A, Ragert P. Long-term effects of motor training on resting-state networks and underlying brain structure. Neuroimage. 2011;57:1492–8. PubMed

Kubica J, Szymura J, Domagalik A, Golda S, Wiecek M, Fafrowicz M, et al. Systematic balance exercises influence cortical activation and serum BDNF levels in older adults. J Clin Med. 2019;8:1910. PubMed PMC

Magon S, Donath L, Gaetano L, Thoeni A, Radue EW, Faude O, et al. Striatal functional connectivity changes following specific balance training in elderly people: MRI results of a randomized controlled pilot study. Gait Posture. 2016;49:334–9. PubMed

Eggenberger P, Wolf M, Schumann M, de Bruin ED. Exergame and balance training modulate prefrontal brain activity during walking and enhance executive function in older adults. Front Aging Neurosci. 2016;8:1–16. PubMed PMC

Taubert M, Draganski B, Anwander A, Muller K, Horstmann A, Villringer A, et al. Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J Neurosci United States. 2010;30:11670–7. PubMed PMC

Mouthon A, Ruffieux J, Mouthon M, Hoogewoud HM, Annoni JM, Taube W. Age-related differences in cortical and subcortical activities during observation and motor imagery of dynamic postural tasks: an fMRI study. Neural Plast. 2018. PubMed PMC

Bakker LBM, Nandi T, Lamoth CJC, Hortobágyi T. Task specificity and neural adaptations after balance learning in young adults. Hum Mov Sci. 2021;78:102833. PubMed

Ruffieux J, Mouthon A, Keller M, Mouthon M, Annoni JM, Taube W. Balance training reduces brain activity during motor simulation of a challenging balance task in older adults: an fMRI study. Front Behav Neurosci. 2018;12:1–10. PubMed PMC

Rueda-Delgado LM, Solesio-Jofre E, Serrien DJ, Mantini D, Daffertshofer A, Swinnen SP. Understanding bimanual coordination across small time scales from an electrophysiological perspective. Neurosci Biobehav Rev. 2014;47:614–35. PubMed

Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10:1–11. PubMed PMC

Taube W, Gruber M, Gollhofer A. Spinal and supraspinal adaptations associated with balance training and their functional relevance. Acta Physiol. 2008;193:101–16. PubMed

Lesinski M, Hortobágyi T, Muehlbauer T, Gollhofer A, Granacher U. Effects of balance training on balance performance in healthy older adults: a systematic review and meta-analysis. Sport Med. 2015;45:1721–38. PubMed PMC

Gebel A, Lesinski M, Behm DG, Granacher U. Effects and dose-response relationship of balance training on balance performance in youth: a systematic review and meta-analysis. Sport Med. 2018;48:2067–89. PubMed

Shumway-Cook A, Woollacott H. Motor control: translating research into clinical practice. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2012.

Wittenberg E, Thompson J, Nam CS, Franz JR. Neuroimaging of human balance control: a systematic review. Front Hum Neurosci. 2017;11:1–25. PubMed PMC

Gebel A, Lehmann T, Granacher U. Balance task difficulty affects postural sway and cortical activity in healthy adolescents. Exp Brain Res. 2020;238:1323–33. PubMed PMC

Hedges LV, Tipton E, Johnson MC. Robust variance estimation in meta-regression with dependent effect size estimates. Res Synth Methods. 2010;1:39–65. PubMed

Tipton E. Small sample adjustments for robust variance estimation with meta-regression. Psychol Methods. 2015;20:375–93. PubMed

Viechtbauer W, Cheung MW-L. Outlier and influence diagnostics for meta-analysis. Res Synth Methods. 2010;1:112–25. PubMed

Sterne JA, Egger M. Regression methods to detect publication and other bias in meta-analysis. Publ Bias Meta-anal Prev Assess Adjust. 2005;99–110.

Brydges CR. Effect size guidelines, sample size calculations, and statistical power in gerontology. Innov Aging. 2019;3:1–8. PubMed PMC

Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Br Med J. 2003;327:557–60. PubMed PMC

Melsen WG, Bootsma MCJ, Rovers MM, Bonten MJM. The effects of clinical and statistical heterogeneity on the predictive values of results from meta-analyses. Clin Microbiol Infect. 2014;20:123–9. PubMed

Ueta K, Mizuguchi N, Sugiyama T, Isaka T, Otomo S. The motor engram of functional connectivity generated by acute whole-body dynamic balance training. Med Sci Sports Exerc. 2022;54:598–608. PubMed PMC

Im S, Oh J, Jun SY, Chang S, Kim Y. Evidence of lateralised white matter plasticity: a longitudinal study of balance performance in nonexpert healthy adults. Eur J Neurosci. 2023;57:1789–802. PubMed

Adcock M, Fankhauser M, Post J, Lutz K, Zizlsperger L, Luft AR, et al. Effects of an in-home multicomponent exergame training on physical functions, cognition, and brain volume of older adults: a randomized controlled trial. Front Med. 2020;6:321. PubMed PMC

Adcock M, Sonder F, Schättin A, Gennaro F, De Bruin ED. A usability study of a multicomponent video game-based training for older adults. Eur Rev Aging Phys Act. 2020;17:1–15. PubMed PMC

Burciu RG, Fritsche N, Granert O, Schmitz L, Spönemann N, Konczak J, et al. Brain changes associated with postural training in patients with cerebellar degeneration: a voxel-based morphometry study. J Neurosci. 2013;33:4594–604. PubMed PMC

Nagamatsu LS, Weinstein AM, Erickson KI, Fanning J, Awick EA, Kramer AF, et al. Exercise mode moderates the relationship between mobility and basal ganglia volume in healthy older adults. J Am Geriatr Soc. 2016;176:139–48. PubMed PMC

Szymura J, Kubica J, Wiecek M, Pera J. The immunomodulary effects of systematic exercise in older adults and people with Parkinson’s disease. J Clin Med. 2020;9:184. PubMed PMC

Giboin LS, Tokuno C, Kramer A, Henry M, Gruber M. Motor learning induces time-dependent plasticity that is observable at the spinal cord level. J Physiol. 2020;598:1943–63. PubMed

Behrens M, Mau-Moeller A, Wassermann F, Bader R, Bruhn S. Effect of balance training on neuromuscular function at rest and during isometric maximum voluntary contraction. Eur J Appl Physiol. 2015;115:1075–85. PubMed

Keller M, Pfusterschmied J, Buchecker M, Müller E, Taube W. Improved postural control after slackline training is accompanied by reduced H-reflexes. Scand J Med Sci Sports. 2012;22:471–7. PubMed

Ruffieux J, Mouthon A, Keller M, Walchli M, Taube W, Wälchli M, et al. Behavioral and neural adaptations in response to five weeks of balance training in older adults: a randomized controlled trial. J Negat Results Biomed. 2017;16:11. PubMed PMC

Penzer F, Duchateau J, Baudry S. Effects of short-term training combining strength and balance exercises on maximal strength and upright standing steadiness in elderly adults. Exp Gerontol. 2015;61:38–46. PubMed

Giboin LS, Loewe K, Hassa T, Kramer A, Dettmers C, Spiteri S, et al. Cortical, subcortical and spinal neural correlates of slackline training-induced balance performance improvements. Neuroimage. 2019;202: 116061. PubMed

Lauber B, Keller M, Gollhofer A, Müller E, Taube W, Muller E, et al. Spinal reflex plasticity in response to alpine skiing in the elderly. Scand J Med Sci Sports. 2011;21(Suppl 1):62–8. PubMed

Chen YS, Zhou S, Cartwright C. Effect of 12 weeks of Tai Chi training on Soleus Hoffmann reflex and control of static posture in older adults. Arch Phys Med Rehabil. 2011;92:886–91. PubMed

Taube W, Gollhofer A, Lauber B. Training-, muscle- and task-specific up- and downregulation of cortical inhibitory processes. Eur J Neurosci. 2020;51:1428–40. PubMed

Lauber B, Gollhofer A, Taube W. What to train first: Balance or explosive strength? Impact on performance and intracortical inhibition. Scand J Med Sci Sport. 2021;31:1301–12. PubMed

Mouthon A, Taube W. Intracortical inhibition increases during postural task execution in response to balance training. Neuroscience. 2019;401:35–42. PubMed

Zandvoort CS, van Dieën JH, Dominici N, Daffertshofer A. The human sensorimotor cortex fosters muscle synergies through cortico-synergy coherence. Neuroimage. 2019;199:30–7. PubMed

Peterson SM, Rios E, Ferris DP. Transient visual perturbations boost short-term balance learning in virtual reality by modulating electrocortical activity. J Neurophysiol. 2018;120:1998–2010. PubMed PMC

Patel PJ, Bhatt T, DelDonno SR, Langenecker SA, Dusane S. Examining neural plasticity for slip-perturbation training: an fMRI study. Front Neurol. 2019;10:1–13. PubMed PMC

Chen Y, Wan A, Mao M, Sun W, Song Q, Mao D. Tai Chi practice enables prefrontal cortex bilateral activation and gait performance prioritization during dual-task negotiating obstacle in older adults. Front Aging Neurosci. 2022;14:1000427. PubMed PMC

Rogge AK, Röder B, Zech A, Hötting K. Exercise-induced neuroplasticity: balance training increases cortical thickness in visual and vestibular cortical regions. Neuroimage. 2018;179:471–9. PubMed

Niemann C, Godde B, Voelcker-Rehage C. Not only cardiovascular, but also coordinative exercise increases hippocampal volume in older adults. Front Aging Neurosci. 2014;6:170. PubMed PMC

Solianik R, Brazaitis M, Cekanauskaite-Krušnauskien A. Tai chi effects on balance in older adults: the role of sustained attention and myokines. J Sports Med Phys Fitness. 2022;62:1512–8. PubMed

Cekanauskaite A, Skurvydas A, Zlibinaite L, Mickeviciene D, Kilikeviciene S, Solianik R, et al. A 10-week yoga practice has no effect on cognition, but improves balance and motor learning by attenuating brain-derived neurotrophic factor levels in older adults. Exp Gerontol. 2020;138:110998. PubMed

Berghuis KMM, Semmler JG, Opie GM, Post AK, Hortobágyi T. Age-related changes in corticospinal excitability and intracortical inhibition after upper extremity motor learning: a systematic review and meta-analysis. Neurobiol Aging. 2017;55:61–71. PubMed

Baudry S. Aging changes the contribution of spinal and corticospinal pathways to control balance. Exerc Sport Sci Rev. 2016;44:104–9. PubMed

Chen Y-SS, Zhou S. Soleus H-reflex and its relation to static postural control. Gait Posture. 2011;33:169–78. PubMed

Solopova IA, Kazennikov OV, Deniskina NB, Levik YS, Ivanenko YP. Postural instability enhances motor responses to transcranial magnetic stimulation in humans. Neurosci Lett. 2003;337:25–8. PubMed

Papegaaij S, Taube W, Hogenhout M, Baudry S, Hortobágyi T. Age-related decrease in motor cortical inhibition during standing under different sensory conditions. Front Aging Neurosci. 2014;6:1–8. PubMed PMC

Puttemans V. Changes in brain activation during the acquisition of a multifrequency bimanual coordination task: from the cognitive stage to advanced levels of automaticity. J Neurosci. 2005;25:4270–8. PubMed PMC

Floyer-Lea A, Matthews PM. Distinguishable brain activation networks for short- and long-term motor skill learning. J Neurophysiol. 2005;94:512–8. PubMed

Sampaio-Baptista C, Filippini N, Stagg CJ, Near J, Scholz J, Johansen-Berg H. Changes in functional connectivity and GABA levels with long-term motor learning. Neuroimage. 2015;106:15–20. PubMed PMC

Hvid LG, Harwood DL, Eskildsen SF, Dalgas U. A critical systematic review of current evidence on the effects of physical exercise on whole/regional grey matter brain volume in populations at risk of neurodegeneration. Sport Med. 2021;51:1651–71. PubMed

Nano PR, Bhaduri A. Mounting evidence suggests human adult neurogenesis is unlikely. Neuron. 2022;110:353–5. PubMed

Gogniat MA, Robinson TL, Miller LS. Exercise interventions do not impact brain volume change in older adults: a systematic review and meta-analysis. Neurobiol Aging. 2021;101:230–46. PubMed

Polacchini A, Metelli G, Francavilla R, Baj G, Florean M, Mascaretti LG, et al. A method for reproducible measurements of serum BDNF: comparison of the performance of six commercial assays. Sci Rep. 2015;5:1–10. PubMed PMC

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