Advertisement

Experimental Brain Research

, Volume 233, Issue 8, pp 2401–2409 | Cite as

Effects of transcranial direct current stimulation (tDCS) on multiscale complexity of dual-task postural control in older adults

  • Diange Zhou
  • Junhong Zhou
  • Hu Chen
  • Brad Manor
  • Jianhao LinEmail author
  • Jue Zhang
Research Article

Abstract

Transcranial direct current stimulation (tDCS) targeting the prefrontal cortex reduces the size and speed of standing postural sway in younger adults, particularly when performing a cognitive dual task. Here, we hypothesized that tDCS would alter the complex dynamics of postural sway as quantified by multiscale entropy (MSE). Twenty healthy older adults completed two study visits. Center-of-pressure (COP) fluctuations were recorded during single-task (i.e., quiet standing) and dual-task (i.e., standing while performing serial subtractions) conditions, both before and after a 20-min session of real or sham tDCS. MSE was used to estimate COP complexity within each condition. The percentage change in complexity from single- to dual-task conditions (i.e., dual-task cost) was also calculated. Before tDCS, COP complexity was lower (p = 0.04) in the dual-task condition as compared to the single-task condition. Neither real nor sham tDCS altered complexity in the single-task condition. As compared to sham tDCS, real tDCS increased complexity in the dual-task condition (p = 0.02) and induced a trend toward improved serial subtraction performance (p = 0.09). Moreover, those subjects with lower dual-task COP complexity at baseline exhibited greater percentage increases in complexity following real tDCS (R = −0.39, p = 0.05). Real tDCS also reduced the dual-task cost to complexity (p = 0.02), while sham stimulation had no effect. A single session of tDCS targeting the prefrontal cortex increased standing postural sway complexity with concurrent non-postural cognitive task. This form of noninvasive brain stimulation may be a safe strategy to acutely improve postural control by enhancing the system’s capacity to adapt to stressors.

Keywords

Postural control Dual task tDCS Elderly Multiscale entropy 

Notes

Acknowledgments

This study was supported by grants from the National Natural Science Foundation of China (Grant Number 11372013) and the National Institute on Aging (1K01AG044543-01A1). We sincerely appreciate Dapeng Bao and the Beijing Sport University for providing the equipment needed to measure body postural sway.

Conflict of interest

All the authors declare that there is no further conflict of interest in this study.

Ethical standard

All procedures performed in studies involving human subjects were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

References

  1. Applegate C, Gandevia SC, Burke D (1988) Changes in muscle and cutaneous cerebral potentials during standing. Exp Brain Res 71:183–188PubMedCrossRefGoogle Scholar
  2. Ashkenazy Y, Hausdorff JM, Ivanov PC, Stanley HE (2002) A stochastic model of human gait dynamics. Phys A 316:662–670CrossRefGoogle Scholar
  3. Beauchet O, Annweiler C, Allali G, Berrut G, Herrmann FR, Dubost V (2008) Recurrent falls and dual task–related decrease in walking speed: is there a relationship? J Am Geriatr Soc 56(7):1265–1269PubMedCrossRefGoogle Scholar
  4. Blaszczyk JW, Klonowski W (2001) Postural stability and fractal dynamics. Acta Neurobiol Exp 61:105–112Google Scholar
  5. Boggio PS, Rigonatti SP, Ribeiro RB et al (2008) A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. Int J Neuropsychopharmacol 11:249–254PubMedCentralPubMedCrossRefGoogle Scholar
  6. Breakspear M, McIntosh AR (2011) Networks, noise and models: reconceptualizing the brain as a complex, distributed system. NeuroImage 58:293–295PubMedCrossRefGoogle Scholar
  7. Chesnokov YV (2008) Complexity and spectral analysis of the heart rate variability dynamics for distant prediction of paroxysmal atrial fibrillation with artificial intelligence methods. Artif Intell Med 43:151–165PubMedCrossRefGoogle Scholar
  8. Costa MD, Goldberger AL, Peng CK (2002) Multiscale entropy analysis of complex physiologic time series. Phys Rev Lett 89:068102–068104PubMedCrossRefGoogle Scholar
  9. Costa MD, Goldberger AL, Peng CK (2005) Multiscale entropy analysis of biological signals. Phys Rev E 71:021906CrossRefGoogle Scholar
  10. Costa MD, Priplata AA, Lipsitz LA et al (2007) Noise and poise: enhancement of postural complexity in the elderly with a stochastic-resonance–based therapy. Europhys Lett 77:68008PubMedCentralPubMedCrossRefGoogle Scholar
  11. Costa MD, Peng CK, Goldberger AL (2008) Multiscale analysis of heart rate dynamics: entropy and time irreversibility measures. Cardiovasc Eng 8(2):88–93PubMedCrossRefGoogle Scholar
  12. Davis NJ, Gold E, Pascual-Leone A, Bracewell RM (2013) Challenges of proper placebo control for non-invasive brain stimulation in clinical and experimental applications. Eur J Neurosci 38:2973–2977PubMedGoogle Scholar
  13. Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C (2009) Enhancement of planning ability by transcranial direct current stimulation. J Neurosci 29(22):7271–7277PubMedCrossRefGoogle Scholar
  14. Filmer HL, Mattingley JB, Dux PE (2013) Improved multitasking following prefrontal tDCS. Cortex 49(10):2845–2852PubMedCrossRefGoogle Scholar
  15. Fregni F, Boggio PS, Nitsche M et al (2005) Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 166:23–30PubMedCrossRefGoogle Scholar
  16. Gandiga PC, Hummel FC, Cohen LG (2006) Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 117:845–850PubMedCrossRefGoogle Scholar
  17. Goble DJ, Coxon JP, Van Impe A et al (2011) Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults. J Neurosci 31(45):16344–16352PubMedCrossRefGoogle Scholar
  18. Goldberger AL, Peng CK, Lipsitz LA (2002) What is physiologic complexity and how does it change with aging and disease? Neurobiol Aging 23:23–26PubMedCrossRefGoogle Scholar
  19. Gruber AH, Busa MA, Gorton GE III, Van Emmerik RE, Masso PD, Jl Hamil (2011) Time-to-contact and multiscale entropy identify differences in postural control in adolescent idiopathic scoliosis. Gait Posture 34:13–18PubMedCrossRefGoogle Scholar
  20. Hecht D, Walsh V, Lavidor M (2010) Transcranial direct current stimulation facilitates decision making in a probabilistic guessing task. J Neurosci 30:4241–4245PubMedCrossRefGoogle Scholar
  21. Herwig U, Satrapi P, Schonfeldt-Lecuona C (2003) Using the international 10–20 EEG system for positioning of transcranial magnetic stimulation. Brain Topogr 16:95–99PubMedCrossRefGoogle Scholar
  22. Huxhold O, Li SC, Schmiedek F, Lindenberger U (2006) Dual-tasking postural control: aging and the effects of cognitive demand in conjunction with focus of attention. Brain Res Bull 69:294–305PubMedCrossRefGoogle Scholar
  23. Ivanov PC, Amaral LN, Goldberger AL, Stanley HE (1998) Stochastic feedback and the regulation of biological rhythms. Europhys Lett 43(4):363PubMedCrossRefGoogle Scholar
  24. Javadi AH, Walsh V (2011) Transcranial direct current stimulation (tDCS) of the left dorsolateral prefrontal cortex modulates declarative memory. Brain Stimul 5:231–241PubMedCrossRefGoogle Scholar
  25. Javadi AH, Cheng P, Walsh V (2012) Short duration transcranial direct current stimulation (tDCS) modulates verbal memory. Brain Stimul 5(4):468–474PubMedCrossRefGoogle Scholar
  26. Kane MJ, Engle RW (2002) The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychon Bull Rev 9(4):637–671PubMedCrossRefGoogle Scholar
  27. Kang HG, Costa MD, Priplata AA et al (2009) Frailty and the degradation of complex balance dynamics during a dual-task protocol. J Gerontol A Biol Sci Med Sci 64:1304–1311PubMedCrossRefGoogle Scholar
  28. Knight RT, Grabowecky MF, Scabini D (1995) Role of human prefrontal cortex in attention control. Adv Neurol 66:21–34PubMedGoogle Scholar
  29. Liang WK, Lo MT, Yang AC et al (2014) Revealing the brain’s adaptability and the transcranial direct current stimulation facilitating effect in inhibitory control by multiscale entropy. Neuroimage 90:218–234PubMedCrossRefGoogle Scholar
  30. Lipsitz LA (2002) Dynamics of stability: the physiologic basis of functional health and frailty. J Gerontol A Biol Sci Med Sci 57:B115–B125PubMedCrossRefGoogle Scholar
  31. Lipsitz LA (2009) Physiological complexity, aging, and the path to frailty. Sci Aging Knowledge Environ 16:pe16Google Scholar
  32. Manor B, Lipsitz LA (2013) Physiologic complexity and aging: implications for physical function and rehabilitation. Prog Neuropsychopharmacol Biol Psychiatry 45:287–293PubMedCentralPubMedCrossRefGoogle Scholar
  33. Manor B, Costa MD, Hu K et al (2010a) Physiological complexity and system adaptability: evidence from postural control dynamics of older adults. J Appl Physiol 109:1786–1791PubMedCentralPubMedCrossRefGoogle Scholar
  34. Manor B, Hu K, Zhao P et al (2010b) Altered control of postural sway following cerebral infarction A cross-sectional analysis. Neurology 74(6):458–464PubMedCentralPubMedCrossRefGoogle Scholar
  35. Manor B, Hu K, Peng CK, Lipsitz LA, Novak V (2012a) Posturo-respiratory synchronization: effects of aging and stroke. Gait Posture 36(2):254–259PubMedCentralPubMedCrossRefGoogle Scholar
  36. Manor B, Newton E, Abduljalil A, Novak V (2012b) The relationship between brain volume and walking outcomes in older adults with and without diabetic peripheral neuropathy. Diabetes Care 35(9):1907–1912PubMedCentralPubMedCrossRefGoogle Scholar
  37. Marsh AP, Geel SE (2000) The effect of age on the attentional demands of postural control. Gait Posture 12:105–113PubMedCrossRefGoogle Scholar
  38. Metuki N, Sela T, Lavidor M (2012) Enhancing cognitive control components of insight problems solving by anodal tDCS of the left dorsolateral prefrontal cortex. Brain Stimul 5:110–115PubMedCrossRefGoogle Scholar
  39. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  40. Peng CK, Costa MD, Goldberger AL (2009) Adaptive data analysis of complex fluctuations in physiologic time series. Adv Adapt Data Anal 1(1):61–70PubMedCentralPubMedCrossRefGoogle Scholar
  41. Petersen RC, Smith GE, Waring SC (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56:303–308PubMedCrossRefGoogle Scholar
  42. Pincus SM (1991) Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 88:2297–2301PubMedCentralPubMedCrossRefGoogle Scholar
  43. Poreisz C, Boros K, Antal A, Paulus W (2007) Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull 72:208–214PubMedCrossRefGoogle Scholar
  44. Ragert P, Vandermeeren Y, Camus M, Cohen LG (2008) Improvement of spatial tactile acuity by transcranial direct current stimulation. Clin Neurophysiol 119:805–811PubMedCentralPubMedCrossRefGoogle Scholar
  45. Ramdani S, Seigle B, Lagarde J, Bouchara F, Bernard PL (2009) On the use of sample entropy to analyze human postural sway data. Med Eng Phys 31(8):1023–1031PubMedCrossRefGoogle Scholar
  46. Rankin JK, Woollacott MH, Cook AS, Brown LA (2000) Cognitive influence on postural stability: a neuromuscular analysis in young and older adults. J Gerontol A Biol 55A(3):M112–M119CrossRefGoogle Scholar
  47. Redfern MS, Jennings JR, Martin C, Furman JM (2001) Attention influences sensory integration for postural control in older adults. Gait Posture 14(3):211–216PubMedCrossRefGoogle Scholar
  48. Reis J, Fritsch B (2011) Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr Opin Neurol 24:590–596PubMedCrossRefGoogle Scholar
  49. Richman JS, Moorman JR (2000) Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 278:H2039–H2049PubMedGoogle Scholar
  50. Ruthruff E, Pashler HE, Klaassen A (2001) Processing bottlenecks in dual-task performance: structural limitation or strategic postponement? Psychon Bull Rev 8:73–80PubMedCrossRefGoogle Scholar
  51. Szameitat AJ, Schubert T, Müller K, Von Cramon DY (2002) Localization of executive functions in dual-task performance with fMRI. J Cogn Neurosci 14(8):1184–1199PubMedCrossRefGoogle Scholar
  52. Teasdale N, Lajoie Y, Bard C et al (1993) Cognitive processes involved for maintaining postural stability while standing and walking. In: Stelmach GE, Homberg V (eds) Sensorimotor Impairment in the Elderly. Kluwer Academic Publishers, Boston, pp 157–168Google Scholar
  53. Tombu M, Jolicoeur P (2003) A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform 29:3–18PubMedCrossRefGoogle Scholar
  54. Trunkvalterova Z, Javorka M, Tonhajzerova I (2008) Reduced short-term complexity of heart rate and blood pressure dynamics in patients with diabetes mellitus type 1: multiscale entropy analysis. Physiol Meas 29:817–828PubMedCrossRefGoogle Scholar
  55. Wang CH, Tsai CH, Tseng P et al (2014) The association of physical activity to neural adaptability during visuo-spatial processing in healthy elderly adults: a multiscale entropy analysis. Brain Cogn 92:73–83CrossRefGoogle Scholar
  56. Wayne PM, Gow BJ, Costa MD et al (2014) Complexity-based measures inform effect of Tai Chi training on standing postural control: cross-sectional and randomized trial studies PloS One 9(12):e114731Google Scholar
  57. Yang AC, Chu-Chung H, Heng-Liang Y et al (2013a) Complexity of spontaneous BOLD activity in default mode network is correlated with cognitive function in normal male elderly: a multiscale entropy analysis. Neurobiol Aging 34(2):428–438PubMedCrossRefGoogle Scholar
  58. Yang AC, Wang SJ, Lai KL et al (2013b) Cognitive and neuropsychiatric correlates of EEG dynamic complexity in patients with Alzheimer’s disease. Prog Neuropsychopharmacol Biol Psychiatry 47:52–61PubMedCrossRefGoogle Scholar
  59. Zhou J, Manor B, Liu D, Hu K, Zhang J, Fang J (2013) The complexity of standing postural control in older adults: a modified detrended fluctuation analysis based upon the empirical mode decomposition algorithm. PLoS One 8:e62585PubMedCentralPubMedCrossRefGoogle Scholar
  60. Zhou J, Bao D, Zhang J et al (2014a) Noise stimuli improve the accuracy of target aiming: possible involvement of noise-enhanced balance control. Exp Mech 54(1):95–100CrossRefGoogle Scholar
  61. Zhou J, Hao Y, Wang Y et al (2014b) Transcranial direct current stimulation (tDCS) reduces the cost of performing a cognitive task on gait and postural control. Eur J Neurosci 39(8):1343–1348PubMedCentralPubMedCrossRefGoogle Scholar
  62. Zimerman M, Heise KF, Hoppe J et al (2012) Modulation of training by single-session transcranial direct current stimulation to the intact motor cortex enhances motor skill acquisition of the paretic hand. Stroke 43(8):2185–2191PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Diange Zhou
    • 1
    • 2
  • Junhong Zhou
    • 2
  • Hu Chen
    • 3
  • Brad Manor
    • 4
    • 5
    • 6
  • Jianhao Lin
    • 1
    Email author
  • Jue Zhang
    • 2
  1. 1.Arthritis Clinic and Research CenterPeking University People’s HospitalBeijingChina
  2. 2.Academy for Advanced Interdisciplinary StudiesPeking UniversityBeijingChina
  3. 3.Office of Educational AdministrationPeking UniversityBeijingChina
  4. 4.Institute for Aging ResearchHebrew SeniorLifeRoslindaleUSA
  5. 5.Department of MedicineBeth Israel Deaconess Medical CenterBostonUSA
  6. 6.Harvard Medical SchoolBostonUSA

Personalised recommendations