Effects of Virtual Reality-Based Physical and Cognitive Training on Executive Function and Dual-Task Gait Performance in Older Adults With Mild Cognitive Impairment: A Randomized Control Trial

Ying-Yi Liao, I-Hsuan Chen, Yi-Jia Lin, Yue Chen, Wei-Chun Hsu, Ying-Yi Liao, I-Hsuan Chen, Yi-Jia Lin, Yue Chen, Wei-Chun Hsu

Abstract

Background: Walking while performing cognitive and motor tasks simultaneously interferes with gait performance and may lead to falls in older adults with mild cognitive impairment (MCI). Executive function, which seems to play a key role in dual-task gait performance, can be improved by combined physical and cognitive training. Virtual reality (VR) has the potential to assist rehabilitation, and its effect on physical and cognitive function requires further investigation. The purpose of this study was to assess the effects of VR-based physical and cognitive training on executive function and dual-task gait performance in older adults with MCI, as well as to compare VR-based physical and cognitive training with traditional combined physical and cognitive training. Method: Thirty-four community-dwelling older adults with MCI were randomly assigned into either a VR-based physical and cognitive training (VR) group or a combined traditional physical and cognitive training (CPC) group for 36 sessions over 12 weeks. Outcome measures included executive function [Stroop Color and Word Test (SCWT) and trail making test (TMT) A and B], gait performance (gait speed, stride length, and cadence) and dual-task costs (DTCs). Walking tasks were performed during single-task walking, walking while performing serial subtraction (cognitive dual task), and walking while carrying a tray (motor dual task). The GAIT Up system was used to evaluate gait parameters including speed, stride length, cadence and DTCs. DTC were defined as 100 * (single-task gait parameters - dual-task gait parameters)/single-task gait parameters. Results: Both groups showed significant improvements in the SCWT and single-task and motor dual-task gait performance measures. However, only the VR group showed improvements in cognitive dual-task gait performance and the DTC of cadence. Moreover, the VR group showed more improvements than the CPC group in the TMT-B and DTC of cadence with borderline significances. Conclusion: A 12-week VR-based physical and cognitive training program led to significant improvements in dual-task gait performance in older adults with MCI, which may be attributed to improvements in executive function.

Keywords: MCI; combined physical and cognitive training; dual-task gait; executive function; virtual reality.

Figures

Figure 1
Figure 1
Scenes from the VR-based training program. (A) Take the MRT. (B) Kitchen chef. (C) Convenience store clerk. (D) Tai Chi. (E) Football (running and stepping). (F) Subject wearing VR glasses and performing VR tasks. (B) and (C) are derived from “job simulator” created by Owlchemy Labs. Both the subject and trainer have provided written informed consent allowing the publication of this image.
Figure 2
Figure 2
Flowchart of the present study.

References

    1. Arnett J. A., Labovitz S. S. (1995). Effect of physical layout in performance of the trail making test. Psychol. Assess. 7, 220–221. 10.1037/1040-3590.7.2.220
    1. Abellan van Kan G., Rolland Y., Andrieu S., Bauer J., Beauchet O., Bonnefoy M., et al. . (2009). Gait speed at usual pace as a predictor of adverse outcomes in community-dwelling older people an international academy on nutrition and aging (IANA) task force. J. Nutr. Health Aging 13, 881–889. 10.1007/s12603-009-0246-z
    1. Anderson-Hanley C., Barcelos N. M., Zimmerman E. A., Gillen R. W., Dunnam M., Cohen B. D., et al. . (2018). 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. 10:76. 10.3389/fnagi.2018.00076
    1. Bahureksa L., Najafi B., Saleh A., Sabbagh M., Coon D., Mohler M. J., et al. . (2017). The impact of mild cognitive impairment on gait and balance: a systematic review and meta-analysis of studies using instrumented assessment. Gerontology 63, 67–83. 10.1159/000445831
    1. Barnes D. E., Santos-Modesitt W., Poelke G., Kramer A. F., Castro C., Middleton L. E., et al. . (2013). The Mental Activity and eXercise (MAX) trial: a randomized controlled trial to enhance cognitive function in older adults. JAMA Intern. Med. 173, 797–804. 10.1001/jamainternmed.2013.189
    1. Bruderer-Hofstetter M., Rausch-Osthoff A. K., Meichtry A., Munzer T., Niedermann K. (2018). Effective multicomponent interventions in comparison to active control and no interventions on physical capacity, cognitive function and instrumental activities of daily living in elderly people with and without mild impaired cognition—A systematic review and network meta-analysis. Ageing Res. Rev. 45, 1–14. 10.1016/j.arr.2018.04.002
    1. Chodzko-Zajko W. J., Proctor D. N., Fiatarone Singh M. A., Minson C. T., Nigg C. R., Salem G. J., et al. . (2009). American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med. Sci. Sports Exerc. 41, 1510–1530. 10.1249/MSS.0b013e3181a0c95c
    1. Coyle H., Traynor V., Solowij N. (2015). Computerized and virtual reality cognitive training for individuals at high risk of cognitive decline: systematic review of the literature. Am. J. Geriatr. Psychiatry 23, 335–359. 10.1016/j.jagp.2014.04.009
    1. Dadashi F., Mariani B., Rochat S., Büla C. J., Santos-Eggimann B., Aminian K. (2014). Gait and foot clearance parameters obtained using shoe-worn inertial sensors in a large-population sample of older adults. Sensors 14, 443–457. 10.3390/s140100443
    1. Damirchi A., Hosseini F., Babaei P. (2018). Mental training enhances cognitive function and BDNF more than either physical or combined training in elderly women with MCI: a small-scale study. Am. J. Alzheimers Dis. Other Demen. 33, 20–29. 10.1177/1533317517727068
    1. de Bruin E. D., Schmidt A. (2010). Walking behaviour of healthy elderly: attention should be paid. Behav. Brain Funct. 6:59. 10.1186/1744-9081-6-59
    1. Diamond A. (2013). Executive functions. Annu. Rev. Psychol. 64, 135–168. 10.1146/annurev-psych-113011-143750
    1. Doi T., Shimada H., Makizako H., Tsutsumimoto K., Uemura K., Anan Y., et al. . (2014). Cognitive function and gait speed under normal and dual-task walking among older adults with mild cognitive impairment. BMC Neurol. 14:67. 10.1186/1471-2377-14-67
    1. Eggenberger P., Theill N., Holenstein S., Schumacher V., De Bruin E. D. (2015). Multicomponent physical exercise with simultaneous cognitive training to enhance dual-task walking of older adults: a secondary analysis of a 6-month randomized controlled trial with 1-year follow-up. Clin. Interv. Aging 10, 1711–1732. 10.2147/cia.s91997
    1. Falbo S., Condello G., Capranica L., Forte R., Pesce C. (2016). Effects of physical-cognitive dual task training on executive function and gait performance in older adults: a randomized controlled trial. Biomed Res. Int. 2016:5812092. 10.1155/2016/5812092
    1. Garber C. E., Blissmer B., Deschenes M. R., Franklin B. A., Lamonte M. J., Lee I. M., et al. . (2011). American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med. Sci. Sports Exerc. 43, 1334–1359. 10.1249/mss.0b013e318213fefb
    1. García-Betances R. I., Jiménez-Mixco V., Arredondo M. T., Cabrera-Umpiérrez M. F. (2015). Using virtual reality for cognitive training of the elderly. Am. J. Alzheimers Dis. Other Demen. 30, 49–54. 10.1177/1533317514545866
    1. Hausdorff J. M., Yogev G., Springer S., Simon E. S., Giladi N. (2005). Walking is more like catching than tapping: gait in the elderly as a complex cognitive task. Exp. Brain Res. 164, 541–548. 10.1007/s00221-005-2280-3
    1. Herman T., Mirelman A., Giladi N., Schweiger A., Hausdorff J. M. (2010). Executive control deficits as a prodrome to falls in healthy older adults: a prospective study linking thinking, walking, and falling. J. Gerontol. A Biol. Sci. Med. Sci. 65, 1086–1092. 10.1093/gerona/glq077
    1. Hobert M. A., Meyer S. I., Hasmann S. E., Metzger F. G., Suenkel U., Eschweiler G. W., et al. . (2017). Gait is associated with cognitive flexibility: a dual-tasking study in healthy older people. Front. Aging Neurosci. 9:154. 10.3389/fnagi.2017.00154
    1. Hobert M. A., Niebler R., Meyer S. I., Brockmann K., Becker C., Huber H., et al. . (2011). Poor trail making test performance is directly associated with altered dual task prioritization in the elderly–baseline results from the TREND study. PLoS One 6:e27831. 10.1371/journal.pone.0027831
    1. Hunter S. W., Divine A., Frengopoulos C., Montero-Odasso M. (2018). A framework for secondary cognitive and motor tasks in dual-task gait testing in people with mild cognitive impairment. BMC Geriatr. 18:202. 10.1186/s12877-018-0894-0
    1. Johns E. K., Phillips N. A., Belleville S., Goupil D., Babins L., Kelner N., et al. . (2012). The profile of executive functioning in amnestic mild cognitive impairment: disproportionate deficits in inhibitory control. J. Int. Neuropsychol. Soc. 18, 541–555. 10.1017/s1355617712000069
    1. Johnson J. K., Lui L. Y., Yaffe K. (2007). Executive function, more than global cognition, predicts functional decline and mortality in elderly women. J. Gerontol. A Biol. Sci. Med. Sci. 62, 1134–1141. 10.1093/gerona/62.10.1134
    1. Kirova A. M., Bays R. B., Lagalwar S. (2015). Working memory and executive function decline across normal aging, mild cognitive impairment and Alzheimer’s disease. Biomed Res. Int. 2015:748212. 10.1155/2015/748212
    1. Liberman K., Forti L. N., Beyer I., Bautmans I. (2017). The effects of exercise on muscle strength, body composition, physical functioning and the inflammatory profile of older adults: a systematic review. Curr. Opin. Clin. Nutr. Metab. Care 20, 30–53. 10.1097/mco.0000000000000335
    1. Liu-Ambrose T. Y., Ashe M. C., Graf P., Beattie B. L., Khan K. M. (2008). Increased risk of falling in older community-dwelling women with mild cognitive impairment. Phys. Ther. 88, 1482–1491. 10.2522/ptj.20080117
    1. Makizako H., Doi T., Shimada H., Yoshida D., Tsutsumimoto K., Uemura K., et al. . (2012). Does a multicomponent exercise program improve dual-task performance in amnestic mild cognitive impairment? A randomized controlled trial. Aging Clin. Exp. Res. 24, 640–646. 10.3275/8760
    1. Mariani B., Hoskovec C., Rochat S., Büla C., Penders J., Aminian K. (2010). 3D gait assessment in young and elderly subjects using foot-worn inertial sensors. J. Biomech. 43, 2999–3006. 10.1016/j.jbiomech.2010.07.003
    1. McDowd J. M. (1986). The effects of age and extended practice on divided attention performance. J. Gerontol. 41, 764–769. 10.1093/geronj/41.6.764
    1. Mirelman A., Maidan I., Herman T., Deutsch J. E., Giladi N., Hausdorff J. M. (2011). Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J. Gerontol. A Biol. Sci. Med. Sci. 66, 234–240. 10.1093/gerona/glq201
    1. Montero-Odasso M. M., Sarquis-Adamson Y., Speechley M., Borrie M. J., Hachinski V. C., Wells J., et al. . (2017). Association of dual-task gait with incident dementia in mild cognitive impairment: results from the gait and brain study. JAMA Neurol. 74, 857–865. 10.1001/jamaneurol.2017.0643
    1. Mrakic-Sposta S., Di Santo S. G., Franchini F., Arlati S., Zangiacomi A., Greci L., et al. . (2018). Effects of combined physical and cognitive virtual reality-based training on cognitive impairment and oxidative stress in MCI patients: a pilot study. Front. Aging Neurosci. 10:282. 10.3389/fnagi.2018.00282
    1. Muir S. W., Speechley M., Wells J., Borrie M., Gopaul K., Montero-Odasso M. (2012). Gait assessment in mild cognitive impairment and Alzheimer’s disease: the effect of dual-task challenges across the cognitive spectrum. Gait Posture 35, 96–100. 10.1016/j.gaitpost.2011.08.014
    1. Parikh H. S. K., Shah C. (2017). Relationship between executive function and dual task physical performance among older adults-a cross sectional study. Int. J. Phys. Med. Rehabil. 5:421 10.4172/2329-9096.1000421
    1. Plummer P., Zukowski L. A., Giuliani C., Hall A. M., Zurakowski D. (2015). Effects of physical exercise interventions on gait-related dual-task interference in older adults: a systematic review and meta-analysis. Gerontology 62, 94–117. 10.1159/000371577
    1. Rosso A. L., Metti A. L., Faulkner K., Redfern M., Yaffe K., Launer L., et al. . (2019). Complex walking tasks and risk for cognitive decline in high functioning older adults. J. Alzheimers Dis. [Epub ahead of print]. 10.3233/jad-181140
    1. Ruthruff E., Pashler H. E., Klaassen A. (2001). Processing bottlenecks in dual-task performance: structural limitation or strategic postponement? Psychon. Bull. Rev. 8, 73–80. 10.3758/bf03196141
    1. Scarpina F., Tagini S. (2017). The stroop color and word test. Front. Psychol. 8:557. 10.3389/fpsyg.2017.00557
    1. Schweiger A., Yogev-Seligmann G., Hausdorff J. M., Giladi N., Herman T. (2008). Dual-task decrements in gait: contributing factors among healthy older adults. J. Gerontol. A Biol. Sci. Med. Sci. 63, 1335–1343. 10.1093/gerona/63.12.1335
    1. Simon S. S., Yokomizo J. E., Bottino C. M. (2012). Cognitive intervention in amnestic Mild Cognitive Impairment: a systematic review. Neurosci. Biobehav. Rev. 36, 1163–1178. 10.1016/j.neubiorev.2012.01.007
    1. Springer S., Giladi N., Peretz C., Yogev G., Simon E. S., Hausdorff J. M. (2006). Dual-tasking effects on gait variability: the role of aging, falls and executive function. Mov. Disord. 21, 950–957. 10.1002/mds.20848
    1. Stroop J. R. (1935). Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 643–662. 10.1037/h0054651
    1. Strouwen C., Molenaar E., Munks L., Keus S. H. J., Zijlmans J. C. M., Vandenberghe W., et al. . (2017). Training dual tasks together or apart in Parkinson’s disease: results from the DUALITY trial. Mov. Disord. 32, 1201–1210. 10.1002/mds.27014
    1. Suzuki T., Shimada H., Makizako H., Doi T., Yoshida D., Ito K., et al. . (2013). A randomized controlled trial of multicomponent exercise in older adults with mild cognitive impairment. PLoS One 8:e61483. 10.1371/journal.pone.0061483
    1. Suzuki T., Shimada H., Makizako H., Doi T., Yoshida D., Tsutsumimoto K., et al. . (2012). Effects of multicomponent exercise on cognitive function in older adults with amnestic mild cognitive impairment: a randomized controlled trial. BMC Neurol. 12:128. 10.1186/1471-2377-12-128
    1. Tay L., Lim W. S., Chan M., Ali N., Chong M. S. (2016). A combined cognitive stimulation and physical exercise programme (MINDVital) in early dementia: differential effects on single- and dual-task gait performance. Gerontology 62, 604–610. 10.1159/000444084
    1. Tsai C. F., Lee W. J., Wang S. J., Shia B. C., Nasreddine Z., Fuh J. L. (2012). Psychometrics of the Montreal Cognitive Assessment (MoCA) and its subscales: validation of the Taiwanese version of the MoCA and an item response theory analysis. Int. Psychogeriatr. 24, 651–658. 10.1017/s1041610211002298
    1. Wang R.-Y., Wang Y.-L., Cheng F.-Y., Chao Y.-H., Chen C.-L., Yang Y.-R. (2018a). Effects of a multicomponent exercise on dual-task performance and executive function among older adults. Int. J. Gerontol. 12, 133–138. 10.1016/j.ijge.2018.01.004
    1. Wang R.-Y., Zhou J.-H., Huang Y.-C., Yang Y.-R. (2018b). Reliability of the chinese version of the trail making test and stroop color and word test among older adults. Int. J. Gerontol. 12, 336–339. 10.1016/j.ijge.2018.06.003
    1. Woollacott M., Shumway-Cook A. (2002). Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16, 1–14. 10.1016/s0966-6362(01)00156-4
    1. Yogev-Seligmann G., Hausdorff J. M., Giladi N. (2008). The role of executive function and attention in gait. Mov. Disord. 23, 329–342; quiz 472. 10.1002/mds.21720

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