Abstract
The aim of this study was to examine the effects of 5 days of anodal-transcranial direct current stimulation (a-tDCS) over the primary motor cortex (M1) on lower extremity functional performance in healthy elderly people. This was a randomized, double-blinded, sham-controlled study whereby 32 healthy older individuals participated in two groups. The intervention group received 20 min of a-tDCS (1 mA) over the M1 on five consecutive days. The sham group received the same stimulation, but the tDCS device was turned off after 30 s of stimulation. Participants were asked to perform the Timed Up and Go (TUG), 30-s Chair Stand Test (30-s CST), and a Modified Figure of Eight Walk Test (MFEWT) on the first day before tDCS application, immediately, 30 min, and 1 week after the last session of stimulation. Results of the a-tDCS group showed that most of the test values had significant changes in post-test assessments compared to the pre-test (p < 0.05). When comparing the anodal and sham tDCS groups, the results showed a significant improvement in TUG and time-MFEWT immediately after (p = 0.02, p = 0.01), 30 min after (p = 0.04, p = 0.01) and 1 week after the last session of stimulation (p = 0.01, p = 0.01). Improvements in performance of the 30-s CST and the number of steps-MFEWT were not significant, except at 1 week after the last session for the steps-MFEWT (p = 0.04). The application of 20 min a-tDCS over the M1 for 5 consecutive days improves lower extremity functional performance in the healthy older participants.
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Data accessibility
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Abbreviations
- ADL:
-
Activity of daily life
- a-tDCS:
-
Anodal transcranial direct current stimulation
- ICC:
-
Intraclass correlation coefficient
- M1:
-
Primary motor cortex
- MDC:
-
Minimum detectable change
- SD:
-
Standard deviation
- SEM:
-
Standard error of mean
- TUG:
-
Timed up and go
- steps-MFEWTS:
-
Number of steps in Modified Figure of Eight Walk Test
- 30-s CST:
-
30-S Chair stand test
- time-MFEWT:
-
Time of Modified Figure of Eight Walk Test
References
Alexander BH, Rivara FP, Wolf ME (1992) The cost and frequency of hospitalization for fall-related injuries in older adults. Am J Public Health 82:1020–1023. https://doi.org/10.2105/AJPH.82.7.1020
Angius L, Pageaux B, Hopker J, Marcora SM, Mauger AR (2016) Transcranial direct current stimulation improves isometric time to exhaustion of the knee extensors. Neuroscience 339:363–375. https://doi.org/10.1016/j.neuroscience.2016.10.028
Angius L, Pascual-Leone A, Santarnecchi E (2018) Brain stimulation and physical performance. Prog Brain Res 240:317–339. https://doi.org/10.1016/bs.pbr.2018.07.010
Bastani A, Jaberzadeh S (2013) a-tDCS differential modulation of corticospinal excitability: the effects of electrode size. Brain Stimul 6:932–937. https://doi.org/10.1016/j.brs.2013.04.005
Beck S, Taube W, Gruber M, Amtage F, Gollhofer A, Schubert M (2007) Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Res 1179:51–60. https://doi.org/10.1016/j.brainres.2007.08.048
Been G, Ngo TT, Miller SM, Fitzgerald PB (2007) The use of tDCS and CVS as methods of non-invasive brain stimulation. Brain Res Rev 56:346–361. https://doi.org/10.1016/j.brainresrev.2007.08.001
Blankevoort CG, Van Heuvelen MJ, Scherder EJ (2013) Reliability of six physical performance tests in older people with dementia. Phys Ther 93:69–78. https://doi.org/10.2522/ptj.20110164
Boggio PS, Nunes A, Rigonatti SP, Nitsche MA, Pascual-Leone A, Fregni F (2007) Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restor Neurol Neurosci 25:123–129. https://doi.org/10.1016/j.brs.2015.01.411
Brunoni AR et al (2012) Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul 5:175–195. https://doi.org/10.1016/j.brs.2011.03.002
Chang MC, Kim DY, Park DH (2015) Enhancement of cortical excitability and lower limb motor function in patients with stroke by transcranial direct current stimulation. Brain Stimul 8:561–566. https://doi.org/10.1016/j.brs.2015.01.411
Ciccone AB, Deckert JA, Schlabs CR, Tilden MJ, Herda TJ, Gallagher PM, Weir JP (2019) Transcranial direct current stimulation of the temporal lobe does not affect high-intensity work capacity. J Strength Cond Res 33:2074–2086. https://doi.org/10.1519/JSC.0000000000002561
Craig CE, Doumas M (2017) Anodal transcranial direct current stimulation shows minimal, measure-specific effects on dynamic postural control in young and older adults: a double blind, sham-controlled study. PLoS One 12:e0170331. https://doi.org/10.1371/journal.pone.0170331
Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M (2009) Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul 2:201–207. https://doi.org/10.1016/j.brs.2009.03.005(e201)
Demain A et al (2014) High-level gait and balance disorders in the elderly: a midbrain disease? J Neurol 261:196–206. https://doi.org/10.1007/s00415-013-7174-x
Dumel G, Bourassa M-E, Charlebois-Plante C, Martine D, Doyon J, Saint-Amour D, De Beaumont L (2018) Motor learning improvement remains 3 months after a multisession anodal tDCS intervention in an aging population. Front Aging Neurosci 10:335. https://doi.org/10.3389/fnagi.2018.00335
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198. https://doi.org/10.1016/0022-3956(75)90026-6
Fregni F et al (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. NeuroReport 16:1551–1555. https://doi.org/10.1097/01.wnr.0000177010.44602.5e
Fregni F et al (2006) A randomized, sham-controlled, proof of principle study of transcranial direct current stimulation for the treatment of pain in fibromyalgia. Arthritis Rheum 54:3988–3998. https://doi.org/10.1002/art.22195
Frontera WR, Hughes VA, Lutz KJ, Evans WJ (1991) A cross-sectional study of muscle strength and mass in 45-to 78-year-old men and women. J Appl Physiol 71:644–650. https://doi.org/10.1152/jappl.1991.71.2.644
Fujiyama H, Hyde J, Hinder MR, Kim S-J, McCormack GH, Vickers JC, Summers JJ (2014) Delayed plastic responses to anodal tDCS in older adults. Aging Neurosci 6:115. https://doi.org/10.3389/fnagi.2014.00115
George MS, Aston-Jones G (2010) Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology 35:301. https://doi.org/10.1038/npp.2009.87
Gill TM, Williams CS, Tinetti ME (1995) Assessing risk for the onset of functional dependence among older adults: the role of physical performance. J Am Geriatr Soc 43:603–609. https://doi.org/10.1111/j.1532-5415.1995.tb07192.x
Goodwill AM, Reynolds J, Daly RM, Kidgell DJ (2013) Formation of cortical plasticity in older adults following tDCS and motor training. Front Aging Neurosci 5:87. https://doi.org/10.3389/fnagi.2013.00087
Goodwill AM, Daly RM, Kidgell DJ (2015) The effects of anodal-tDCS on cross-limb transfer in older adults. Clin Neurophysiol 126:2189–2197. https://doi.org/10.1016/j.clinph.2015.01.006
Herbert R (2019) Research note: significance testing and hypothesis testing: meaningless, misleading and mostly unnecessary. J Physiother 65:178. https://doi.org/10.1016/j.jphys.2019.05.001
Hess RJ, Brach JS, Piva SR, VanSwearingen JM (2010) Walking skill can be assessed in older adults: validity of the Figure-of-8 Walk Test. Phys Ther 90:89–99. https://doi.org/10.2522/ptj.20080121
Hummel FC, Heise K, Celnik P, Floel A, Gerloff C, Cohen LG (2010) Facilitating skilled right hand motor function in older subjects by anodal polarization over the left primary motor cortex. Neurobiol Aging 31:2160–2168. https://doi.org/10.1016/j.neurobiolaging.2008.12.008
Hunter S, White M, Thompson M (1998) Techniques to evaluate elderly human muscle function: a physiological basis. J Gerontol A Biol Sci Med Sci 53:B204–B216. https://doi.org/10.1093/gerona/53A.3.B204
Ishøi L, Hölmich P, Thorborg K (2019) Measures of hip muscle strength and rate of force development using a fixated handheld dynamometer: intra-tester intra-day reliability of a clinical set-up. Int J Sports Phys Thet 14:715 (PMID: 31598409)
Jarnlo G-B, Nordell E (2003) Reliability of the modified figure of eight—a balance performance test for elderly women. Physiother Theory Pract 19:35–43. https://doi.org/10.1080/09593980307969
Jones CJ, Rikli RE, Beam WC (1999) A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport 70:113–119. https://doi.org/10.1080/02701367.1999.10608028
Kaminski E et al (2017) Anodal transcranial direct current stimulation does not facilitate dynamic balance task learning in healthy old adults. Front Hum Neurosci 11:16. https://doi.org/10.3389/fnhum.2017.00016
Kaski D, Quadir S, Patel M, Yousif N, Bronstein AM (2012) Enhanced locomotor adaptation aftereffect in the “broken escalator” phenomenon using anodal tDCS. J Neurophysiol 107:2493–2505. https://doi.org/10.1152/jn.00223.2011
Keel JC, Smith MJ, Wassermann EM (2001) A safety screening questionnaire for transcranial magnetic stimulation. Clin Neurophysiol 112:720. https://doi.org/10.1016/S1388-2457(00)00518-6
Kinsella KG, Phillips DR (2005) Global aging: the challenge of success, vol 1. Population Reference Bureau, Washington DC
Lang N et al (2005) How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495–504. https://doi.org/10.1111/j.1460-9568.2005.04233.x
Lattari E, de Oliveira BS, Oliveira BRR, de Mello Pedreiro RC, Machado S, Neto GAM (2018) Effects of transcranial direct current stimulation on time limit and ratings of perceived exertion in physically active women. Neurosci Lett 662:12–16. https://doi.org/10.1016/j.neulet.2017.10.007
Lattari E et al (2020) Can transcranial direct current stimulation improve muscle power in individuals with advanced weight-training experience? J Strength Cond Res 34:97–103. https://doi.org/10.1519/jsc.0000000000001956
Lusardi MM, Pellecchia GL, Schulman M (2003) Functional performance in community living older adults. J Geriatr Phys Ther 26:14. https://doi.org/10.1123/japa.2012-0234
Madhavan S, Weber KA, Stinear JW (2011) Non-invasive brain stimulation enhances fine motor control of the hemiparetic ankle: implications for rehabilitation. Exp Brain Res 209:9–17. https://doi.org/10.1007/s00221-010-2511-0
Manenti R, Brambilla M, Rosini S, Orizio I, Ferrari C, Borroni B, Cotelli M (2014) Time up and go task performance improves after transcranial direct current stimulation in patient affected by Parkinson's disease. Neurosci Lett 580:74–77. https://doi.org/10.1016/j.neulet.2014.07.052
Mattay VS, Fera F, Tessitore A, Hariri A, Das S, Callicott J, Weinberger D (2002) Neurophysiological correlates of age-related changes in human motor function. Neurology 58:630–635. https://doi.org/10.1212/WNL.58.4.630
McCrimmon CM et al (2017) Electrocorticographic encoding of human gait in the leg primary motor cortex. Cereb Cortex 28:2752–2762. https://doi.org/10.1093/cercor/bhx155
McNeil CJ, Vandervoort AA, Rice CL (2007) Peripheral impairments cause a progressive age-related loss of strength and velocity-dependent power in the dorsiflexors. J Appl Physiol 102:1962–1968. https://doi.org/10.1152/japplphysiol.01166.2006
Monte-Silva K, Kuo M-F, Liebetanz D, Paulus W, Nitsche MA (2010) Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol 103:1735–1740. https://doi.org/10.1152/jn.00924.2009
Nakazono T, Kamide N, Ando M (2014) The reference values for the chair stand test in healthy Japanese older people: determination by meta-analysis. J Phys Ther Sci 26:1729–1731. https://doi.org/10.1589/jpts.26.1729
Nitsche M, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527:633–639. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x
Nitsche M et al (2003) Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 553:293–301. https://doi.org/10.1113/jphysiol.2003.049916
Nitsche MA et al (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1:206–223. https://doi.org/10.1016/j.brs.2008.06.004
Nordin E, Rosendahl E, Lundin-Olsson L (2006) Timed “Up & Go” Test: reliability in older people dependent in activities of daily living—focus on cognitive state. Phys Ther 86:646–655. https://doi.org/10.1093/ptj/86.5.646
Oki K, Mahato NK, Nakazawa M, Amano S, France CR, Russ DW, Clark BC (2016) Preliminary evidence that excitatory transcranial direct current stimulation extends time to task failure of a sustained, submaximal muscular contraction in older adults. J Gerontol A Biol Sci Med Sci 71:1109–1112. https://doi.org/10.1093/gerona/glw011
Parikh PJ, Cole KJ (2014) Effects of transcranial direct current stimulation in combination with motor practice on dexterous grasping and manipulation in healthy older adults. Physiol Rep 2:e00255. https://doi.org/10.1002/phy2.255
Parikh PJ, Cole KJ (2015) Effects of transcranial direct current stimulation on the control of finger force during dexterous manipulation in healthy older adults. PLoS One 10:e0124137. https://doi.org/10.1371/journal.pone.0124137
Penninx BW, Ferrucci L, Leveille SG, Rantanen T, Pahor M, Guralnik JM (2000) Lower extremity performance in nondisabled older persons as a predictor of subsequent hospitalization. J Gerontol A Biol Sci Med Sci 55:M691–M697. https://doi.org/10.1093/gerona/55.11.M691
Petersen TH, Willerslev-Olsen M, Conway BA, Nielsen JB (2012) The motor cortex drives the muscles during walking in human subjects. J Physiol 590:2443–2452. https://doi.org/10.1113/jphysiol.2012.227397
Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39:142–148. https://doi.org/10.1111/j.1532-5415.1991.tb01616.x
Radel R, Tempest G, Denis G, Besson P, Zory R (2017) Extending the limits of force endurance: stimulation of the motor or the frontal cortex? Cortex 97:96–108. https://doi.org/10.1016/j.nicl.2017.09.026
Reis J et al (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595. https://doi.org/10.1073/pnas.0805413106
Rikli RE, Jones CJ (1999) Functional fitness normative scores for community-residing older adults, ages 60–94. J Aging Phys Act 7:162–181. https://doi.org/10.1123/japa.7.2.162
Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415. https://doi.org/10.1146/annurev.neuro.23.1.393
Scahill RI, Frost C, Jenkins R, Whitwell JL, Rossor MN, Fox NC (2003) A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch Neurol 60:989–994. https://doi.org/10.1146/annurev.neuro.23.1.393
Schubert M, Beck S, Taube W, Amtage F, Faist M, Gruber M (2008) Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci 27:2007–2018. https://doi.org/10.1111/j.1460-9568.2008.06186.x
Seidler RD, Alberts JL, Stelmach GE (2002) Changes in multi-joint performance with age. Mot Control 6:19–31. https://doi.org/10.1123/mcj.6.1.19
Seidler RD et al (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34:721–733. https://doi.org/10.1016/j.neubiorev.2009.10.005
Shkuratova N, Morris ME, Huxham F (2004) Effects of age on balance control during walking. Arch Phys Med Rehabil 85:582–588. https://doi.org/10.1016/j.apmr.2003.06.021
Shumway-Cook A, Brauer S, Woollacott M (2000) Predicting the probability for falls in community-dwelling older adults using the timed up & go test. Phys Ther 80:896–903. https://doi.org/10.1093/ptj/80.9.896
Sohn MK, Jee SJ, Kim YW (2013) Effect of transcranial direct current stimulation on postural stability and lower extremity strength in hemiplegic stroke patients. Ann Rehabil Med 37:759. https://doi.org/10.5535/arm.2013.37.6.759
Sparing R, Mottaghy FM (2008) Noninvasive brain stimulation with transcranial magnetic or direct current stimulation (TMS/tDCS)—from insights into human memory to therapy of its dysfunction. Methods 44:329–337. https://doi.org/10.1016/j.ymeth.2007.02.001
Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17:37–53. https://doi.org/10.1177/1073858410386614
Tanaka S, Hanakawa T, Honda M, Watanabe K (2009) Enhancement of pinch force in the lower leg by anodal transcranial direct current stimulation. Exp Brain Res 196:459–465. https://doi.org/10.1007/s00221-009-1863-9
Tanaka S et al (2011) Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke. Neurorehabil Neural Repair 25:565–569. https://doi.org/10.1177/1545968311402091
Tang P-F, Woollacott MH (1996) Balance control in older adults: training effects on balance control and the integration of balance control into walking. Adv Psychol 114:339–367. https://doi.org/10.1016/S0166-4115(01)80015-7
Taube W, Schubert M, Gruber M, Beck S, Faist M, Gollhofer A (2006) Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. J Appl Physiol 101:420–429. https://doi.org/10.1152/japplphysiol.01447.2005
Taube W, Gruber M, Beck S, Faist M, Gollhofer A, Schubert M (2007) Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiol 189:347–358. https://doi.org/10.1111/j.1748-1716.2007.01665.x
Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707. https://doi.org/10.1056/NEJM198812293192604
Tokuno C, Taube W, Cresswell A (2009) An enhanced level of motor cortical excitability during the control of human standing. Acta Physiol 195:385–395. https://doi.org/10.1111/j.1748-1716.2008.01898.x
Valle A et al (2009) Efficacy of anodal transcranial direct current stimulation (tDCS) for the treatment of fibromyalgia: results of a randomized, sham-controlled longitudinal clinical trial. J Pain Manag 2:353 PMID: 21170277
Vargas VZ et al (2018) Modulation of isometric quadriceps strength in soccer players with transcranial direct current stimulation: a crossover study. J Strength Cond Res 32:1336–1341. https://doi.org/10.1519/jsc.0000000000001985
Vitor-Costa M, Okuno NM, Bortolotti H, Bertollo M, Boggio PS, Fregni F, Altimari LR (2015) Improving cycling performance: transcranial direct current stimulation increases time to exhaustion in cycling. PLoS One 10:e0144916. https://doi.org/10.1371/journal.pone.0144916
Wang C, Wai Y, Kuo B, Yeh Y-Y, Wang J (2008) Cortical control of gait in healthy humans: an fMRI study. J Neural Transm 115:1149. https://doi.org/10.1007/s00702-008-0058-z
Washabaugh EP, Santos L, Claflin ES, Krishnan C (2016) Low-level intermittent quadriceps activity during transcranial direct current stimulation facilitates knee extensor force-generating capacity. Neuroscience 329:93–97. https://doi.org/10.1016/j.neuroscience.2016.04.037
Woollacott MH (1993) 8 age-related changes in posture and movement. J Gerontol 48:56–60. https://doi.org/10.1093/geronj/48.Special_Issue.56
Yosephi MH, Ehsani F, Zoghi M, Jaberzadeh S (2018) Multi-session anodal tDCS enhances the effects of postural training on balance and postural stability in older adults with high fall risk: primary motor cortex versus cerebellar stimulation. Brain Stimul 11:1239–1250. https://doi.org/10.1016/j.brs.2018.07.044
Zhou J, Lo O-Y, Lipsitz LA, Zhang J, Fang J, Manor B (2018) Transcranial direct current stimulation enhances foot sole somatosensation when standing in older adults. Exp Brain Res 236:795–802. https://doi.org/10.1007/s00221-018-5178-6
Zimerman M, Hummel FC (2010) Non-invasive brain stimulation: enhancing motor and cognitive functions in healthy old subjects. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2010.00149
Zimerman M, Nitsch M, Giraux P, Gerloff C, Cohen LG, Hummel FC (2013) Neuroenhancement of the aging brain: restoring skill acquisition in old subjects. Ann Neurol 73:10–15. https://doi.org/10.1002/ana.23761
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The authors are thankful to the participants for their collaboration and the University of Social Welfare and Rehabilitation Sciences (USWR) for its support.
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All authors; MR, ZM, SA, FE, DK, MRN, EB and SJ substantially contributed to at least of the following aspects of preparing this research report: (i) developing study concept and design of the work; (ii) data acquisition, analysis, and interpretation; (iii) preparing and revising the final draft of the manuscript for publication. All contributors are accountable for the accuracy of the content of this manuscript.
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Clinical implications
Anodal tDCS can be considered as a potential intervention to improve gait speed, balance control and lower-body functional performance in healthy older adults. Perhaps, anodal-tDCS can be used to prevent age-related declined functional performance in elderly individuals.
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Communicated by Winston D. Byblow.
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Rostami, M., Mosallanezhad, Z., Ansari, S. et al. Multi-session anodal transcranial direct current stimulation enhances lower extremity functional performance in healthy older adults. Exp Brain Res 238, 1925–1936 (2020). https://doi.org/10.1007/s00221-020-05827-6
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DOI: https://doi.org/10.1007/s00221-020-05827-6