Effects of an In-home Multicomponent Exergame Training on Physical Functions, Cognition, and Brain Volume of Older Adults: A Randomized Controlled Trial

Manuela Adcock, Mélanie Fankhauser, Jennifer Post, Kai Lutz, Leopold Zizlsperger, Andreas R Luft, Vânia Guimarães, Alexandra Schättin, Eling D de Bruin, Manuela Adcock, Mélanie Fankhauser, Jennifer Post, Kai Lutz, Leopold Zizlsperger, Andreas R Luft, Vânia Guimarães, Alexandra Schättin, Eling D de Bruin

Abstract

Aging is associated with a decline in physical functions, cognition and brain structure. Considering that human life is based on an inseparable physical-cognitive interplay, combined physical-cognitive training through exergames is a promising approach to counteract age-related impairments. The aim of this study was to assess the effects of an in-home multicomponent exergame training on [i] physical and cognitive functions and [ii] brain volume of older adults compared to a usual care control group. Thirty-seven healthy and independently living older adults aged 65 years and older were randomly assigned to an intervention (exergame training) or a control (usual care) group. Over 16 weeks, the participants of the intervention group absolved three home-based exergame sessions per week (à 30-40 min) including Tai Chi-inspired exercises, dancing and step-based cognitive games. The control participants continued with their normal daily living. Pre- and post-measurements included assessments of physical (gait parameters, functional muscle strength, balance, aerobic endurance) and cognitive (processing speed, short-term attention span, working memory, inhibition, mental flexibility) functions. T1-weighted magnetic resonance imaging was conducted to assess brain volume. Thirty-one participants (mean age = 73.9 ± 6.4 years, range = 65-90 years, 16 female) completed the study. Inhibition and working memory significantly improved post-intervention in favor of the intervention group [inhibition: F (1) = 2.537, p = 0.046, n p 2 = 0.11, working memory: F (1) = 5.872, p = 0.015, n p 2 = 0.02]. Two measures of short-term attentional span showed improvements after training in favor of the control group [F(1) = 4.309, p = 0.038, n p 2 = 0.03, F (1) = 8.504, p = 0.004, n p 2 = 0.04]. No significant training effects were evident for physical functions or brain volume. Both groups exhibited a significant decrease in gray matter volume of frontal areas and the hippocampus over time. The findings indicate a positive influence of exergame training on executive functioning. No improvements in physical functions or brain volume were evident in this study. Better adapted individualized training challenge and a longer training period are suggested. Further studies are needed that assess training-related structural brain plasticity and its effect on performance, daily life functioning and healthy aging.

Keywords: brain volume; cognition; exergame; healthy aging; physical functions; physical-cognitive training.

Copyright © 2020 Adcock, Fankhauser, Post, Lutz, Zizlsperger, Luft, Guimarães, Schättin and de Bruin.

Figures

Figure 1
Figure 1
Set up and navigation in the Active@Home exergame. The hardware of the Active@Home exergame consists of four inertial measurement units (IMUs). For movement evaluation, participants wore the sensors at wrists and ankles. Color and size of the bracelet helped to distinguish the position of each IMU. The IMUs were connected via Bluetooth to a HDMI dongle. This dongle was inserted into a television and provided the exergame software. The game interface was presented on the TV screen. By pointing the IMU on the right wrist horizontally to the TV screen, a “hand mouse” got activated for navigation through the game.
Figure 2
Figure 2
Study flow chart. Screening for eligibility included a health questionnaire and the Mini Mental Status Examination. Eligible participants were randomly assigned to either training or control group. The participants of the training group trained 3x/week à 30–40 min for 16 weeks while the participants of the control group continued with their normal daily living. Physical and cognitive functions as well as brain volume were assessed before and after the intervention period.

References

    1. He W, Goodkind D, Kowal P. An Aging World: 2015. International Publication Reports. Washington, DC: U.S. Census Bureau; (2016).
    1. Harada CN, Love MCN, Triebel KL. Normal cognitive aging. Clin Geriatr Med. (2013) 29:737–52. 10.1016/j.cger.2013.07.002
    1. Fjell AM, Walhovd KB. Structural brain changes in aging: courses, causes and cognitive consequences. Rev Neurosci. (2010) 21:187–222. 10.1515/REVNEURO.2010.21.3.187
    1. Reuter-Lorenz PA, Cooke KA. Neuropsychology of aging, past, present and future: contributions of Morris Moscovitch. Neuropsychologia. (2016) 90:117–24. 10.1016/j.neuropsychologia.2016.06.018
    1. Brehmer Y, Kalpouzos G, Wenger E, Lövdén M. Plasticity of brain and cognition in older adults. Psychol Res. (2014) 78:790–802. 10.1007/s00426-014-0587-z
    1. Hertzog C, Kramer AF, Wilson RS, Lindenberger U. Enrichment effects on adult cognitive development: can the functional capacity of older adults be preserved and enhanced? Psychol Sci Public Interest. (2008) 9:1–65. 10.1111/j.1539-6053.2009.01034.x
    1. Pascual-Leone A, Amedi A, Fregni F, Merabet LB. The plastic human brain cortex. Annu Rev Neurosci. (2005) 28:377–401. 10.1146/annurev.neuro.27.070203.144216
    1. Cai L, Chan JS, Yan JH, Peng K. Brain plasticity and motor practice in cognitive aging. Front. Aging Neurosci. (2014) 6:31. 10.3389/fnagi.2014.00031
    1. Warburton DE, Nicol CW, Bredin SS. Health benefits of physical activity: the evidence. Can Med Assoc J. (2006) 174:801–9. 10.1503/cmaj.051351
    1. Chang Y-K, Pan C-Y, Chen F-T, Tsai C-L, Huang C-C. Effect of resistance-exercise training on cognitive function in healthy older adults: a review. J Aging Phys Act. (2012) 20:497–517. 10.1123/japa.20.4.497
    1. Netz Y, Wu M-J, Becker BJ, Tenenbaum G. Physical activity and psychological well-being in advanced age: a meta-analysis of intervention studies. Psychol Aging. (2005) 20:272. 10.1037/0882-7974.20.2.272
    1. Kramer AF, Colcombe S. Fitness effects on the cognitive function of older adults: a meta-analytic study—revisited. Perspect. Psychol. Sci. (2018) 13:213–7. 10.1177/1745691617707316
    1. Erickson KI, Voss MW, Prakash RS, Basak C, Szabo A, Chaddock L, et al. . Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA. (2011) 108:3017–22. 10.1073/pnas.1015950108
    1. Bherer L, Erickson KI, Liu-Ambrose T. A review of the effects of physical activity and exercise on cognitive and brain functions in older adults. J Aging Res. (2013) 2013:657508. 10.1155/2013/657508
    1. Best JR, Chiu BK, Hsu CL, Nagamatsu LS, Liu-Ambrose T. Long-term effects of resistance exercise training on cognition and brain volume in older women: results from a randomized controlled trial. J Int Neuropsychol Soc. (2015) 21:745–56. 10.1017/S1355617715000673
    1. Voss MW, Nagamatsu LS, Liu-Ambrose T, Kramer AF. Exercise, brain, and cognition across the life span. J Appl Physiol. (2011) 111:1505–13. 10.1152/japplphysiol.00210.2011
    1. Thomas A, Dennis A, Bandettini PA, Johansen-Berg H. The effects of aerobic activity on brain structure. Front Psychol. (2012) 3:86. 10.3389/fpsyg.2012.00086
    1. Cotman CW, Berchtold NC, Christie L-A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci. (2007) 30:464–72. 10.1016/j.tins.2007.06.011
    1. Lista I, Sorrentino G. Biological mechanisms of physical activity in preventing cognitive decline. Cell Mol Neurobiol. (2010) 30:493–503. 10.1007/s10571-009-9488-x
    1. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity—exercise-induced response of peripheral brain-derived neurotrophic factor. Sports Med. (2010) 40:765–801. 10.2165/11534530-000000000-00000
    1. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA. (1990) 87:5568–72. 10.1073/pnas.87.14.5568
    1. Van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. (1999) 2:266. 10.1038/6368
    1. Eadie BD, Redila VA, Christie BR. Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J Comp Neurol. (2005) 486:39–47. 10.1002/cne.20493
    1. Van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. (2005) 25:8680–5. 10.1523/JNEUROSCI.1731-05.2005
    1. Pereira AC, Huddleston DE, Brickman AM, Sosunov AA, Hen R, McKhann GM, et al. . An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA. (2007) 104:5638–43. 10.1073/pnas.0611721104
    1. Bediou B, Adams DM, Mayer RE, Tipton E, Green CS, Bavelier D. Meta-analysis of action video game impact on perceptual, attentional, and cognitive skills. Psychol Bull. (2018) 144:77. 10.1037/bul0000130
    1. Nguyen L, Murphy K, Andrews G. Cognitive and neural plasticity in old age: a systematic review of evidence from executive functions cognitive training. Ageing Res Rev. (2019) 53:100912. 10.1016/j.arr.2019.100912
    1. Reijnders J, van Heugten C, van Boxtel M. Cognitive interventions in healthy older adults and people with mild cognitive impairment: a systematic review. Ageing Res Rev. (2013) 12:263–75. 10.1016/j.arr.2012.07.003
    1. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth Ø, Larsen VA, et al. . Effects of memory training on cortical thickness in the elderly. Neuroimage. (2010) 52:1667–76. 10.1016/j.neuroimage.2010.05.041
    1. Lövdén M, Bodammer NC, Kühn S, Kaufmann J, Schütze H, Tempelmann C, et al. . Experience-dependent plasticity of white-matter microstructure extends into old age. Neuropsychologia. (2010) 48:3878–83. 10.1016/j.neuropsychologia.2010.08.026
    1. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth Ø, Larsen VA, et al. . Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study. Hum Brain Mapp. (2012) 33:2390–406. 10.1002/hbm.21370
    1. Lampit A, Hallock H, Suo C, Naismith SL, Valenzuela M. Cognitive training-induced short-term functional and long-term structural plastic change is related to gains in global cognition in healthy older adults: a pilot study. Front Aging Neurosci. (2015) 7:14. 10.3389/fnagi.2015.00014
    1. Kühn S, Lorenz RC, Weichenberger M, Becker M, Haesner M, O'Sullivan J, et al. . Taking control! Structural and behavioural plasticity in response to game-based inhibition training in older adults. NeuroImage. (2017) 156:199–206. 10.1016/j.neuroimage.2017.05.026
    1. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, et al. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci. (2003) 17:2042–6. 10.1046/j.1460-9568.2003.02647.x
    1. Ehninger D, Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cerebral Cortex. (2003) 13:845–51. 10.1093/cercor/13.8.845
    1. Olson AK, Eadie BD, Ernst C, Christie BR. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus. (2006) 16:250–60. 10.1002/hipo.20157
    1. Wolf SA, Kronenberg G, Lehmann K, Blankenship A, Overall R, Staufenbiel M, et al. . Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol Psychiatry. (2006) 60:1314–23. 10.1016/j.biopsych.2006.04.004
    1. Korol DL, Gold PE, Scavuzzo CJ. Use it and boost it with physical and mental activity. Hippocampus. (2013) 23:1125–35. 10.1002/hipo.22197
    1. Law LL, Barnett F, Yau MK, Gray MA. Effects of combined cognitive and exercise interventions on cognition in older adults with and without cognitive impairment: a systematic review. Ageing Res Rev. (2014) 15:61–75. 10.1016/j.arr.2014.02.008
    1. Lauenroth A, Ioannidis AE, Teichmann B. Influence of combined physical and cognitive training on cognition: a systematic review. BMC Geriatr. (2016) 16:1. 10.1186/s12877-016-0315-1
    1. Levin O, Netz Y, Ziv G. The beneficial effects of different types of exercise interventions on motor and cognitive functions in older age: a systematic review. Eur Rev Aging Phys Activ. (2017) 14:20. 10.1186/s11556-017-0189-z
    1. Tait JL, Duckham RL, Milte CM, Main LC, Daly RM. Influence of sequential vs. simultaneous dual-task exercise training on cognitive function in older adults. Front Aging Neurosci. (2017) 9:368. 10.3389/fnagi.2017.00368
    1. Herold F, Hamacher D, Schega L, Mueller NG. Thinking while moving or moving while thinking–concepts of motor-cognitive training for cognitive performance enhancement. Front Aging Neurosci. (2018) 10:228. 10.3389/fnagi.2018.00228
    1. Joubert C, Chainay H. Aging brain: the effect of combined cognitive and physical training on cognition as compared to cognitive and physical training alone–a systematic review. Clin Interv Aging. (2018) 13:1267. 10.2147/CIA.S165399
    1. Schaefer S, Schumacher V. The interplay between cognitive and motor functioning in healthy older adults: findings from dual-task studies and suggestions for intervention. Gerontology. (2011) 57:239–46. 10.1159/000322197
    1. Fabel K, Kempermann G. Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromolecular Med. (2008) 10:59–66. 10.1007/s12017-008-8031-4
    1. Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, et al. . Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci. (2010) 4:189. 10.3389/fnins.2010.00189
    1. Benzing V, Schmidt M. Exergaming for children and adolescents: strengths, weaknesses, opportunities and threats. J Clin Med. (2018) 7:422. 10.3390/jcm7110422
    1. Brox E, Luque LF, Evertsen GJ, Hernández JEG. Exergames for elderly: social exergames to persuade seniors to increase physical activity. In Pervasive Computing Technologies for Healthcare (PervasiveHealth), 5th International Conference on: IEEE. Dublin: (2011). p. 546–9.
    1. Pirovano M, Surer E, Mainetti R, Lanzi PL, Borghese NA. Exergaming and rehabilitation: a methodology for the design of effective and safe therapeutic exergames. Entertain Comput. (2016) 14:55–65. 10.1016/j.entcom.2015.10.002
    1. Schutzer KA, Graves BS. Barriers and motivations to exercise in older adults. Prev Med. (2004) 39:1056–61. 10.1016/j.ypmed.2004.04.003
    1. Stanmore E, Stubbs B, Vancampfort D, de Bruin ED, Firth J. The effect of active video games on cognitive functioning in clinical and non-clinical populations: a meta-analysis of randomized controlled trials. Neurosci Biobehav Rev. (2017) 78:34–43. 10.1016/j.neubiorev.2017.04.011
    1. Stojan R, Voelcker-Rehage C. A systematic review on the cognitive benefits and neurophysiological correlates of exergaming in healthy older adults. J Clin Med. (2019) 8:734. 10.3390/jcm8050734
    1. Larsen LH, Schou L, Lund HH, Langberg H. The physical effect of exergames in healthy elderly—a systematic review. Games Health J. (2013) 2:205–12. 10.1089/g4h.2013.0036
    1. Street TD, Lacey SJ, Langdon RR. Gaming your way to health: a systematic review of exergaming programs to increase health and exercise behaviors in adults. Games Health J. (2017) 6:136–46. 10.1089/g4h.2016.0102
    1. Kappen DL, Mirza-Babaei P, Nacke LE. Older Adults' physical activity and exergames: a systematic review. Int J Hum Comput Interact. (2019) 35:1–28. 10.1080/10447318.2018.1441253
    1. Ji L, Zhang H, Potter GG, Zang Y-F, Steffens DC, Guo H, et al. . Multiple neuroimaging measures for examining exercise-induced neuroplasticity in older adults: a quasi-experimental study. Front Aging Neurosci. (2017) 9:102. 10.3389/fnagi.2017.00102
    1. Anderson-Hanley C, Barcelos NM, Zimmerman EA, Gillen RW, Dunnam M, Cohen BD, et al. . The Aerobic and Cognitive Exercise Study (ACES) for community-dwelling older adults with or at-risk for mild cognitive impairment (MCI): neuropsychological, neurobiological and neuroimaging outcomes of a randomized clinical trial. Front Aging Neurosci. (2018) 10:76. 10.3389/fnagi.2018.00076
    1. Adcock M, Thalmann M, Schättin A, Gennaro F, de Bruin ED. A pilot study of an in-home multicomponent exergame training for older adults: feasibility, usability and pre-post evaluation. Front. Aging Neurosci. (2019) 11:304. 10.3389/fnagi.2019.00304
    1. Campbell M, Fitzpatrick R, Haines A, Kinmonth AL, Sandercock P, Spiegelhalter D, et al. . Framework for design and evaluation of complex interventions to improve health. BMJ. (2000) 321:694–6. 10.1136/bmj.321.7262.694
    1. Beller EM, Gebski V, Keech AC. Randomisation in clinical trials. Med J Aust. (2002) 177:565–7. 10.5694/j.1326-5377.2002.tb04955.x
    1. American Geriatrics Society BGS American Academy of Orthopaedic Surgeons Panel on Falls Prevention Summary of the Updated American Geriatrics Society/British Geriatrics Society clinical practice guideline for prevention of falls in older persons. J Am Geriatr Soc. (2011) 59:148–57. 10.1111/j.1532-5415.2010.03234.x
    1. Sherrington C, Tiedemann A, Fairhall N, Close JC, Lord SR. Exercise to prevent falls in older adults: an updated meta-analysis and best practice recommendations. NSW Public Health Bull. (2011) 22:78–83. 10.1071/NB10056
    1. Brach M, Hauer K, Rotter L, Werres C, Korn O, Konrad R, et al. Modern principles of training in exergames for sedentary seniors: requirements and approaches for sport and exercise sciences. Int J Comput Sci Sport. (2011) 11:86–99. 10.13140/RG.2.1.3762.2647
    1. Shigematsu R, Chang M, Yabushita N, Sakai T, Nakagaichi M, Nho H, et al. . Dance-based aerobic exercise may improve indices of falling risk in older women. Age Ageing. (2002) 31:261–6. 10.1093/ageing/31.4.261
    1. Wayne PM, Walsh JN, Taylor-Piliae RE, Wells RE, Papp KV, Donovan NJ, et al. . Effect of Tai Chi on cognitive performance in older adults: systematic review and meta-analysis. J Am Geriatr Soc. (2014) 62:25–39. 10.1111/jgs.12611
    1. Dhami P, Moreno S, DeSouza JF. New framework for rehabilitation–fusion of cognitive and physical rehabilitation: the hope for dancing. Front Psychol. (2015) 5:1478. 10.3389/fpsyg.2014.01478
    1. Nelson ME, Rejeski WJ, Blair SN, Duncan PW, Judge JO, King AC, et al. . Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association. Circulation. (2007) 116:1094. 10.1249/mss.0b013e3180616aa2
    1. Chodzko-Zajko WJ, Proctor DN, Singh MAF, Minson CT, Nigg CR, Salem GJ, et al. . Exercise and physical activity for older adults. Med Sci Sports Exerc. (2009) 41:1510–30. 10.1249/MSS.0b013e3181a0c95c
    1. Bamidis P, Vivas A, Styliadis C, Frantzidis C, Klados M, Schlee W, et al. . A review of physical and cognitive interventions in aging. Neurosci Biobehav Rev. (2014) 44:206–20. 10.1016/j.neubiorev.2014.03.019
    1. Tabei KI, Satoh M, Ogawa JI, Tokita T, Nakaguchi N, Nakao K, et al. . Physical exercise with music reduces gray and white matter loss in the frontal cortex of elderly people: the Mihama-Kiho scan project. Front Aging Neurosci. (2017) 9:174. 10.3389/fnagi.2017.00174
    1. Healy AF, Kole JA, Bourne LE, Jr. Training principles to advance expertise. Front Psychol. 5:131. 10.3389/fpsyg.2014.00131
    1. Dubost V, Kressig RW, Gonthier R, Herrmann FR, Aminian K, Najafi B, et al. . Relationships between dual-task related changes in stride velocity and stride time variability in healthy older adults. Hum Mov Sci. (2006) 25:372–82. 10.1016/j.humov.2006.03.004
    1. Lindemann U, Najafi B, Zijlstra W, Hauer K, Muche R, Becker C, et al. . Distance to achieve steady state walking speed in frail elderly persons. Gait Posture. (2008) 27:91–6. 10.1016/j.gaitpost.2007.02.005
    1. Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, Ostir GV, et al. . Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci. (2000) 55:M221–31. 10.1093/gerona/55.4.M221
    1. Ostir GV, Volpato S, Fried LP, Chaves P, Guralnik JM. Reliability and sensitivity to change assessed for a summary measure of lower body function: results from the Women's Health and Aging Study. J Clin Epidemiol. (2002) 55:916–21. 10.1016/S0895-4356(02)00436-5
    1. 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) 8:66. 10.3389/fnagi.2016.00066
    1. Rikli RE, Jones CJ. Development and validation of a functional fitness test for community-residing older adults. J Aging Phys Act. (1999) 7:129–61. 10.1123/japa.7.2.129
    1. Hesseberg K, Bentzen H, Bergland A. Reliability of the senior fitness test in community-dwelling older people with cognitive impairment. Physiother Res Int. (2015) 20:37–44. 10.1002/pri.1594
    1. Strauss E, Sherman EM, Spreen O. A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. (2006). American Chemical Society.
    1. Bowie CR, Harvey PD. Administration and interpretation of the Trail Making Test. Nat Protoc. (2006) 1:2277–81. 10.1038/nprot.2006.390
    1. Wechsler D. Wechsler Memory Scale-Revised (WMS-R). (1987). Psychological Corporation.
    1. Ashburner J, Friston KJ. Voxel-based morphometry—the methods. Neuroimage. (2000) 11:805–21. 10.1006/nimg.2000.0582
    1. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. (2007) 38:95–113. 10.1016/j.neuroimage.2007.07.007
    1. Suppa P, Anker U, Spies L, Bopp I, Rüegger-Frey B, Klaghofer R, et al. . Fully automated atlas-based hippocampal volumetry for detection of Alzheimer's disease in a memory clinic setting. J Alzheimer's Dis. (2015) 44:183–93. 10.3233/JAD-141446
    1. Noguchi K, Gel YR, Brunner E, Konietschke F. nparLD: an R software package for the nonparametric analysis of longitudinal data in factorial experiments. J Stat Softw. (2012) 50:1–23. 10.18637/jss.v050.i12
    1. Team RC. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna (2017) Available online at:
    1. Brunner EDS, Langer F. Nonparametric Analysis of Longitudinal Data in Factorial Experiments. New York, NY: Wiley; (2002).
    1. Brunner E, Puri ML. Nonparametric methods in factorial designs. Stat Papers. (2001) 42:1–52. 10.1007/s003620000039
    1. Lakens D. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol. (2013) 4:863. 10.3389/fpsyg.2013.00863
    1. Cohen J. Statistical Analysis for the Behavioral Sciences. Hillsdale, MI: Lawrance Erlbaum; (1988).
    1. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. . Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. (2002) 15:273–89. 10.1006/nimg.2001.0978
    1. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol. (2000) 41:49–100. 10.1006/cogp.1999.0734
    1. Delbaere K, Close JC, Heim J, Sachdev PS, Brodaty H, Slavin MJ, et al. . A multifactorial approach to understanding fall risk in older people. J Am Geriatr Soc. (2010) 58:1679–85. 10.1111/j.1532-5415.2010.03017.x
    1. Schoene D, Smith ST, Davies TA, Delbaere K, Lord SR. A Stroop Stepping Test (SST) using low-cost computer game technology discriminates between older fallers and non-fallers. Age Ageing. (2014) 43:285–9. 10.1093/ageing/aft157
    1. Blackwood J, Shubert T, Forgarty K, Chase C. Relationships between performance on assessments of executive function and fall risk screening measures in community-dwelling older adults. J Geriatr Phys Ther. (2016) 39:89–96. 10.1519/JPT.0000000000000056
    1. Caetano MJD, Menant JC, Schoene D, Pelicioni PHS, Sturnieks DL, Lord SR. Sensorimotor and cognitive predictors of impaired gait adaptability in older people. J Gerontol A Biol Sci Med Sci. (2017) 72:1257–63. 10.1093/gerona/glw171
    1. Mateen BA, Bussas M, Doogan C, Waller D, Saverino A, Kiraly FJ, et al. . The Trail Making test: a study of its ability to predict falls in the acute neurological in-patient population. Clin Rehabil. (2018) 32:1396–405. 10.1177/0269215518771127
    1. Anderson-Hanley C, Arciero PJ, Brickman AM, Nimon JP, Okuma N, Westen SC, et al. . Exergaming and older adult cognition a cluster randomized clinical trial. Am J Prev Med. (2012) 42:109–19. 10.1016/j.amepre.2011.10.016
    1. Maillot P, Perrot A, Hartley A. Effects of interactive physical-activity video-game training on physical and cognitive function in older adults. Psychol Aging. (2012) 27:589. 10.1037/a0026268
    1. Schoene D, Lord SR, Delbaere K, Severino C, Davies TA, Smith ST. A randomized controlled pilot study of home-based step training in older people using videogame technology. PLoS ONE. (2013) 8:e57734. 10.1371/journal.pone.0057734
    1. Eggenberger P, Schumacher V, Angst M, Theill N, de Bruin ED. Does multicomponent physical exercise with simultaneous cognitive training boost cognitive performance in older adults? A 6-month randomized controlled trial with a 1-year follow-up. Clin Interv Aging. (2015) 10:1335–49. 10.2147/CIA.S87732
    1. Gschwind YJ, Eichberg S, Ejupi A, de Rosario H, Kroll M, Marston HR, et al. . ICT-based system to predict and prevent falls (iStoppFalls): results from an international multicenter randomized controlled trial. Eur Rev Aging Phys Act. (2015) 12:10. 10.1186/s11556-015-0155-6
    1. Ogawa EF, You T, Leveille SG. Potential benefits of exergaming for cognition and dual-task function in older adults: a systematic review. J Aging Phys Act. (2016) 24:332–6. 10.1123/japa.2014-0267
    1. Cassilhas RC, Viana VA, Grassmann V, Santos RT, Santos RF, Tufik S, et al. . The impact of resistance exercise on the cognitive function of the elderly. Med Sci Sports Exerc. (2007) 39:1401–7. 10.1249/mss.0b013e318060111f
    1. Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci. (2008) 9:58. 10.1038/nrn2298
    1. Anderson-Hanley C, Nimon JP, Westen SC. Cognitive health benefits of strengthening exercise for community-dwelling older adults. J Clin Exp Neuropsychol. (2010) 32:996–1001. 10.1080/13803391003662702
    1. Smith PJ, Blumenthal JA, Hoffman BM, Cooper H, Strauman TA, Welsh-Bohmer K, et al. . Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med. (2010) 72:239–52. 10.1097/PSY.0b013e3181d14633
    1. Voelcker-Rehage C, Godde B, Staudinger UM. Cardiovascular and coordination training differentially improve cognitive performance and neural processing in older adults. Front Hum Neurosci. (2011) 5:26. 10.3389/fnhum.2011.00026
    1. Nagamatsu LS, Handy TC, Hsu CL, Voss M, Liu-Ambrose T. Resistance training promotes cognitive and functional brain plasticity in seniors with probable mild cognitive impairment. Arch Intern Med. (2012) 172:666–8. 10.1001/archinternmed.2012.379
    1. Rehfeld K, Lüders A, Hökelmann A, Lessmann V, Kaufmann J, Brigadski T, et al. . Dance training is superior to repetitive physical exercise in inducing brain plasticity in the elderly. PLoS ONE. (2018) 13:e0196636. 10.1371/journal.pone.0196636
    1. Kent P. The evolution of the Wechsler Memory Scale: a selective review. Appl Neuropsychol Adult. (2013) 20:277–91. 10.1080/09084282.2012.689267
    1. Howes SC, Charles DK, Marley J, Pedlow K, McDonough SM. Gaming for health: systematic review and meta-analysis of the physical and cognitive effects of active computer gaming in older adults. Phys Ther. (2017) 97:1122–37. 10.1093/ptj/pzx088
    1. Pichierri G, Murer K, de Bruin ED. A cognitive-motor intervention using a dance video game to enhance foot placement accuracy and gait under dual task conditions in older adults: a randomized controlled trial. BMC Geriatr. (2012) 12:74. 10.1186/1471-2318-12-74
    1. Schättin A, Arner R, Gennaro F, de Bruin ED. Adaptations of prefrontal brain activity, executive functions, and gait in healthy elderly following exergame and balance training: a randomized-controlled study. Front Aging Neurosci. (2016) 8:278. 10.3389/fnagi.2016.00278
    1. Segev-Jacubovski O, Herman T, Yogev-Seligmann G, Mirelman A, Giladi N, Hausdorff JM. The interplay between gait, falls and cognition: can cognitive therapy reduce fall risk? Expert Rev Neurother. (2011) 11:1057–75. 10.1586/ern.11.69
    1. Beurskens R, Bock O. Age-related deficits of dual-task walking: a review. Neural Plast. (2012) 2012:131608. 10.1155/2012/131608
    1. Bohannon RW, Andrews AW, Thomas MW. Walking speed: reference values and correlates for older adults. J Orthopaedic Sports Phys Ther. (1996) 24:86–90. 10.2519/jospt.1996.24.2.86
    1. Kattenstroth J-C, Kalisch T, Holt S, Tegenthoff M, Dinse HR. Six months of dance intervention enhances postural, sensorimotor, and cognitive performance in elderly without affecting cardio-respiratory functions. Front Aging Neurosci. (2013) 5:5. 10.3389/fnagi.2013.00005
    1. Hamacher D, Hamacher D, Rehfeld K, Hökelmann A, Schega L. The effect of a six-month dancing program on motor-cognitive dual-task performance in older adults. J Aging Phys Act. (2015) 23:647–52. 10.1123/japa.2014-0067
    1. Rehfeld K, Müller P, Aye N, Schmicker M, Dordevic M, Kaufmann J, et al. . Dancing or fitness sport? The effects of two training programs on hippocampal plasticity and balance abilities in healthy seniors. Front. Hum Neurosci. (2017) 11:305. 10.3389/fnhum.2017.00305
    1. Liao Y-Y, Chen I-H, Wang R-Y. Effects of Kinect-based exergaming on frailty status and physical performance in prefrail and frail elderly: a randomized controlled trial. Sci Rep. (2019) 9:9353. 10.1038/s41598-019-45767-y
    1. Schoene D, Valenzuela T, Toson B, Delbaere K, Severino C, Garcia J, et al. . Interactive cognitive-motor step training improves cognitive risk factors of falling in older adults - a randomized controlled trial. PLoS ONE. (2015) 10:e0145161. 10.1371/journal.pone.0145161
    1. Okubo Y, Schoene D, Lord SR. Step training improves reaction time, gait and balance and reduces falls in older people: a systematic review and meta-analysis. Br J Sports Med. (2016) 51:586–93. 10.1136/bjsports-2015-095452
    1. Jones CJ, Rikli RE. Measuring functional fitness in older adults. J Active Aging. (2002) 1:24–30.
    1. Cress ME, Buchner DM, Prohaska T, Rimmer J, Brown M, Macera C, et al. . Best practices for physical activity programs and behavior counseling in older adult populations. J Aging Phys Act. (2005) 13:61–74. 10.1123/japa.13.1.61
    1. Paterson DH, Jones GR, Rice CL. Ageing and physical activity: evidence to develop exercise recommendations for older adults. Appl Physiol Nutr Metab. (2007) 32:S69–108. 10.1139/H07-111
    1. Van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA. (1999) 96:13427–31. 10.1073/pnas.96.23.13427
    1. Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, et al. . Aerobic exercise training increases brain volume in aging humans. J Gerontol Ser A Biol Sci Med Sci. (2006) 61:1166–70. 10.1093/gerona/61.11.1166
    1. Kleim JA, Barbay S, Cooper NR, Hogg TM, Reidel CN, Remple MS, et al. . Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem. (2002) 77:63–77. 10.1006/nlme.2000.4004
    1. Kleim JA, Markham JA, Vij K, Freese JL, Ballard DH, Greenough WT. Motor learning induces astrocytic hypertrophy in the cerebellar cortex. Behav Brain Res. (2007) 178:244–9. 10.1016/j.bbr.2006.12.022
    1. Blumenfeld-Katzir T, Pasternak O, Dagan M, Assaf Y. Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS ONE. (2011) 6:e20678. 10.1371/journal.pone.0020678
    1. Niemann C, Godde B, Staudinger U, Voelcker-Rehage C. Exercise-induced changes in basal ganglia volume and cognition in older adults. Neuroscience. (2014) 281:147–63. 10.1016/j.neuroscience.2014.09.033
    1. 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. 10.3389/fnagi.2014.00170
    1. Müller P, Rehfeld K, Schmicker M, Hökelmann A, Dordevic M, Lessmann V, et al. . Evolution of neuroplasticity in response to physical activity in old age: the case for dancing. Front Aging Neurosci. (2017) 9:56. 10.3389/fnagi.2017.00056
    1. Mortimer JA, Ding D, Borenstein AR, DeCarli C, Guo Q, Wu Y, et al. . Changes in brain volume and cognition in a randomized trial of exercise and social interaction in a community-based sample of non-demented Chinese elders. J Alzheimer's Dis. (2012) 30:757–66. 10.3233/JAD-2012-120079
    1. Engvig A, Fjell AM, Westlye LT, Skaane NV, Dale AM, Holland D, et al. . Effects of cognitive training on gray matter volumes in memory clinic patients with subjective memory impairment. J Alzheimer's Dis. (2014) 41:779–91. 10.3233/JAD-131889
    1. Suo C, Singh MF, Gates N, Wen W, Sachdev P, Brodaty H, et al. Therapeutically relevant structural and functional mechanisms triggered by physical and cognitive exercise. Mol Psychiatry. (2016) 21:1633 10.1038/mp.2016.19
    1. Jessberger S, Gage FH. Stem-cell-associated structural and functional plasticity in the aging hippocampus. Psychol Aging. (2008) 23:684. 10.1037/a0014188
    1. Ferris LT, Williams JS, Shen C-L. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc. (2007) 39:728–34. 10.1249/mss.0b013e31802f04c7
    1. Vaynman S, Ying Z, Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci. (2004) 20:2580–90. 10.1111/j.1460-9568.2004.03720.x
    1. Ruscheweyh R, Willemer C, Krüger K, Duning T, Warnecke T, Sommer J, et al. . Physical activity and memory functions: an interventional study. Neurobiol Aging. (2011) 32:1304–19. 10.1016/j.neurobiolaging.2009.08.001
    1. Lövdén M, Schaefer S, Noack H, Bodammer NC, Kühn S, Heinze HJ, et al. . Spatial navigation training protects the hippocampus against age-related changes during early and late adulthood. Neurobiol Aging. (2012) 33:620.e9-22. 10.1016/j.neurobiolaging.2011.02.013
    1. Petersen AMW, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. (2005) 98:1154–62. 10.1152/japplphysiol.00164.2004
    1. Pervaiz N, Hoffman-Goetz L. Freewheel training alters mouse hippocampal cytokines. Int J Sports Med. (2011) 32:889–95. 10.1055/s-0031-1279780
    1. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. (2001) 14:21–36. 10.1006/nimg.2001.0786
    1. Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, et al. . Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cerebral Cortex. (2005) 15:1676–89. 10.1093/cercor/bhi044

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