The effect of transcranial alternating current stimulation over the supplementary motor area on bimanual coordination in elderly people

Document Type : Research Paper

Authors

1 Department of Motor Behavior, Ferdowsi University of Mashhad, Iran

2 Department of motor behavior, Faculty of sport sciences, Alzahra University, Tehran, Iran

3 Postdoctoral researcher- University of Sussex United-Kingdom

Abstract

Background: Transcranial alternating current stimulation (tACS) is a non-invasive method that offers a potential solution to reduce the effects of aging on brain function.
Aim: The aim of this study was to investigate the effect of offline tACS over the supplementary motor area on bimanual coordination in elderly people.
Materials and Methods: Thirty-one women aged of 60-75 years were selected as convenience. They were assigned to 2 conditions: tACS and Sham, in random order, with one-week interval between conditions. After pre-test, each participant completed four trials of 5 min using Purdue pegboard task. Concurrently, participants received beta tACS with a current intensity of 1 mA. Immediate retention test, transfer test, and delayed retention tests after 48 hours and 1 week were conducted. A 2(condition) x 4(test) ANOVA with repeated measures was performed on gain scores.
Results: The main effects of condition and test were significant (P<0.0001). The Bonferroni tests revealed the significant improvement of bimanual coordination in the tACS condition compared to the sham condition in all retention and transfer tests (P<0.05).
Conclusion: The findings highlights the potential use of offline beta tACS over the SMA as a modulatory factor for enhancing bimanual coordination in the elderly women.

Keywords

References

[1] Moghadam MF, Ardekani MK, Shamsi A. “The effects of transcranial Direct Current Stimulation on working memory in the elderly with normal cognitive impairments”. Archives of Psychiatry & Psychotherapy. 2020; 22(1). doi: 10.12740/APP/109146.

[2] Rudnicka E, Napierała P, Podfigurna A, Męczekalski B, Smolarczyk R, Grymowicz M. “The World Health Organization (WHO) approach to healthy ageing”. Maturitas. 2020; 139: 6-11. doi: 10.1016/j.maturitas.2020.05.018.

[3] World Health Organization. Ageing; 2023 July 27. https://www.who.int/health-topics/ageing.

[4] Akbari Kamrani AA, Azadi F, Foroughan M, Siadat S, Kaldi AR. “Characteristics of falls among institutionalized elderly people”. Iranian Journal of Ageing. 2007; 1(2): 101-5.

[5] Brayne C, Miller B. “Dementia and aging populations—A global priority for contextualized research and health policy”. Plos Medicine. 2017; 14(3): e1002275. doi: 10.1371/journal.pmed.1002275.

[6] Bowden JL, McNulty PA. “The magnitude and rate of reduction in strength, dexterity and sensation in the human hand vary with ageing”. Experimental Gerontology. 2013; 48(8): 756-65. doi: 10.1016/j.exger.2013.03.011.

[7] Mahncke HW, Bronstone A, Merzenich MM. “Brain plasticity and functional losses in the aged: scientific bases for a novel intervention”. Progress in Brain Research. 2006; 157: 81-109.

[8] Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB. “Motor control and aging: links to age-related brain structural, functional, and biochemical effects”. Neuroscience & Biobehavioral Reviews. 2010; 34(5): 721-33. doi: 10.1016/j.neubiorev.2009.10.005.

[9] Lin CH, Chou LW, Wei SH, Lieu FK, Chiang SL, Sung WH. “Influence of aging on bimanual coordination control”. Experimental Gerontology. 2014; 53: 40-7. doi: 10.1016/j.exger.2014.02.005.

[10] Loehrer PA, Nettersheim FS, Jung F, Weber I, Huber C, Dembek TA, Pelzer EA, Fink GR, Tittgemeyer M, Timmermann L. “Ageing changes effective connectivity of motor networks during bimanual finger coordination”. NeuroImage. 2016; 143: 325-42. doi: 10.1016/j.neuroimage.2016.09.014.

[11] Maes C, Gooijers J, de Xivry JJ, Swinnen SP, Boisgontier MP. “Two hands, one brain, and aging”. Neuroscience & Biobehavioral Reviews. 2017; 75: 234-56. doi: 10.1016/j.neubiorev.2017.01.052.

[12] Temprado JJ, Torre MM, Langeard A, Julien-Vintrou M, Devillers-Réolon L, Sleimen-Malkoun R, Berton E. “Intentional switching between bimanual coordination patterns in older adults: is it mediated by inhibition processes?”. Frontiers in Aging Neuroscience. 2020; 12: 29. doi: 10.3389/fnagi.2020.00029.

[13] Helfrich RF, Knepper H, Nolte G, Strüber D, Rach S, Herrmann CS, Schneider TR, Engel AK. “Selective modulation of interhemispheric functional connectivity by HD-tACS shapes perception”. PLoS biology. 2014; 12(12): e1002031. doi: 10.1371/journal.pbio.1002031.

[14] Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS. “Entrainment of brain oscillations by transcranial alternating current stimulation”. Current Biology. 2014; 24(3): 333-9. doi: 10.1016/j.cub.2013.12.041.

[15] Suzuki M, Tanaka S, Gomez-Tames J, Okabe T, Cho K, Iso N, Hirata A. “Nonequivalent after-effects of alternating current stimulation on motor cortex oscillation and inhibition: Simulation and experimental study”. Brain Sciences. 2022; 12(2): 195. doi: 10.3390/brainsci12020195.

[16] Fresnoza S, Christova M, Feil T, Gallasch E, Körner C, Zimmer U, Ischebeck A. “The effects of transcranial alternating current stimulation (tACS) at individual alpha peak frequency (iAPF) on motor cortex excitability in young and elderly adults”. Experimental Brain Research. 2018; 236: 2573-88. doi: 10.1007/s00221-018-5314-3.

[17] Nomura T, Kirimoto H. “Anodal transcranial direct current stimulation over the supplementary motor area improves anticipatory postural adjustments in older adults”. Frontiers in Human Neuroscience. 2018; 12: 317. doi: 10.3389/fnhum.2018.00317.

[18] Ganguly J, Murgai A, Sharma S, Aur D, Jog M. “Non-invasive transcranial electrical stimulation in movement disorders”. Frontiers in Neuroscience. 2020; 14: 522. doi: 10.3389/fnins.2020.00522.

[19] Nitsche MA, Paulus W. “Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation”. The Journal of Physiology. 2000; 527(Pt 3): 633.

[20] Polanía R, Paulus W, Nitsche MA. “Modulating cortico‐striatal and thalamo‐cortical functional connectivity with transcranial direct current stimulation”. Human Brain Mapping. 2012; 33(10): 2499-508. doi: 10.1002/hbm.21380.

[21] Toyokura M, Muro I, Komiya T, Obara M. “Activation of pre–supplementary motor area (SMA) and SMA proper during unimanual and bimanual complex sequences: an analysis using functional magnetic resonance imaging”. Journal of Neuroimaging. 2002; 12(2): 172-8.

[22] Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M. “Atlasing the frontal lobe connections and their variability due to age and education: A spherical deconvolution tractography study”. Brain Structure and Function. 2016; 221: 1751-66. doi: 10.1007/s00429-015-1001-3.

[23] Kasess CH, Windischberger C, Cunnington R, Lanzenberger R, Pezawas L, Moser E. “The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling”. Neuroimage. 2008; 40(2): 828-37.

[24] Pastor MA, Day BL, Macaluso E, Friston KJ, Frackowiak RS. “The functional neuroanatomy of temporal discrimination”. Journal of Neuroscience. 2004; 24(10): 2585-91.

[25] Miyaguchi S, Inukai Y, Takahashi R, Miyashita M, Matsumoto Y, Otsuru N, Onishi H. “Effects of stimulating the supplementary motor area with a transcranial alternating current for bimanual movement performance”. Behavioural Brain Research. 2020; 393: 112801. doi: 10.1016/j.bbr.2020.112801.

[26] Miyaguchi S, Inukai Y, Mitsumoto S, Otsuru N, Onishi H. “Gamma-transcranial alternating current stimulation on the cerebellum and supplementary motor area improves bimanual motor skill”. Behavioural Brain Research. 2022; 424: 113805. doi: 10.1016/j.bbr.2022.113805.

[27] Sikaroodi H, Majidi A, Samadi S, Shirzad H, Aghdam H, Azimi Kia A, Mohammadi Bakhsh L. “Evaluating reliability of the montreal cognitive assessment test and its agreement with neurologist diagnosed among patients with cognitive complaints”. Journal of Police Medicine. 2012; 1(1): 15-21. doi: 10.30505/1.1.15.

[28] Alipour A, Agah Haris M. “Reliability and validity of Edinburg handedness inventory in Iran”. Journal of Psychological Sciences. 2007; 22: 117-33.

[29] Manji A, Amimoto K, Matsuda T, Wada Y, Inaba A, Ko S. “Effects of transcranial direct current stimulation over the supplementary motor area body weight-supported treadmill gait training in hemiparetic patients after stroke”. Neuroscience Letters. 2018; 662: 302-5. doi: 10.1016/j.neulet.2017.10.049.

[30] Nguyen J, Deng Y, Reinhart RM. “Brain-state determines learning improvements after transcranial alternating-current stimulation to frontal cortex”. Brain Stimulation. 2018; 11(4): 723-6.

[31] Raco V, Bauer R, Olenik M, Brkic D, Gharabaghi A. “Neurosensory effects of transcranial alternating current stimulation”. Brain Stimulation. 2014; 7(6): 823-31. doi: 10.1016/j.brs.2014.08.005.

[32] Hu K, Wan R, Liu Y, Niu M, Guo J, Guo F. “Effects of transcranial alternating current stimulation on motor performance and motor learning for healthy individuals: A systematic review and meta-analysis”. Frontiers in Physiology. 2022; 13: 1064584. doi: 10.3389/fphys.2022.1064584.

[33] Hosaka R, Nakajima T, Aihara K, Yamaguchi Y, Mushiake H. “The suppression of beta oscillations in the primate supplementary motor complex reflects a volatile state during the updating of action sequences”. Cerebral Cortex. 2016; 26(8): 3442-52. doi: 10.1093/cercor/bhv163.

[34] Green PE, Ridding MC, Hill KD, Semmler JG, Drummond PD, Vallence AM. “Supplementary motor area—primary motor cortex facilitation in younger but not older adults”. Neurobiology of Aging. 2018; 64: 85-91. doi: 10.1016/j.neurobiolaging.2017.12.016.

[35] Chung JW, Burciu RG, Ofori E, Coombes SA, Christou EA, Okun MS, Hess CW, Vaillancourt DE. “Beta-band oscillations in the supplementary motor cortex are modulated by levodopa and associated with functional activity in the basal ganglia”. NeuroImage: Clinical. 2018; 19: 559-71. doi: 10.1016/j.nicl.2018.05.021.

[36] Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR. “Dynamic intra-and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM”. Neuroimage. 2008; 41(4): 1382-94.

[37] Ohara S, Mima T, Baba K, Ikeda A, Kunieda T, Matsumoto R, Yamamoto J, Matsuhashi M, Nagamine T, Hirasawa K, Hori T. “Increased synchronization of cortical oscillatory activities between human supplementary motor and primary sensorimotor areas during voluntary movements”. Journal of Neuroscience. 2001; 21(23): 9377-86.

[38] Rjosk V, Kaminski E, Hoff M, Gundlach C, Villringer A, Sehm B, Ragert P. “Transcranial alternating current stimulation at beta frequency: lack of immediate effects on excitation and interhemispheric inhibition of the human motor cortex”. Frontiers in Human Neuroscience. 2016; 10:560. doi: 10.3389/fnhum.2016.00560.

[39] Azarpaikan A, Taherii Torbati H, Sohrabi M, Boostani R, Ghoshuni M. “Power spectral parameter variations after transcranial direct current stimulation in a bimanual coordination task”. Adaptive Behavior. 2021; 29(1): 25-38. doi: 10.1177/1059712319879971.

[40] Goodwill AM, Teo WP, Morgan P, Daly RM, Kidgell DJ. “Bihemispheric-tDCS and upper limb rehabilitation improves retention of motor function in chronic stroke: a pilot study”. Frontiers in Human Neuroscience. 2016; 10: 258. doi: 10.3389/fnhum.2016.00258.

[41] Ciechanski P, Kirton A. “Transcranial direct-current stimulation can enhance motor learning in children”. Cerebral Cortex. 2017; 27(5): 2758-67. doi: 10.1093/cercor/bhw114.

[42] Pixa NH, Steinberg F, Doppelmayr M. “High-definition transcranial direct current stimulation to both primary motor cortices improves unimanual and bimanual dexterity”. Neuroscience Letters. 2017; 643: 84-8. doi: 10.1016/j.neulet.2017.02.033.

[43] Heise KF, Monteiro TS, Gijbels V, Leunissen IH, Mantni D, Swinnen SP. “Modulation of interhemispheric connectivity by alternating current stimulation and its impact on transitions between bimanual movements of varying stability”. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation. 2017; 10(2): 452. doi: 10.1016/j.brs.2017.01.328.

[44] Krause V, Meier A, Dinkelbach L, Pollok B. “Beta band transcranial alternating (tACS) and direct current stimulation (tDCS) applied after initial learning facilitate retrieval of a motor sequence”. Frontiers in Behavioral Neuroscience. 2016; 10: 4. doi: 10.3389/fnbeh.2016.00004.

[45] Berger A, Pixa NH, Steinberg F, Doppelmayr M. “Brain oscillatory and hemodynamic activity in a bimanual coordination task following transcranial alternating current stimulation (tACS): A combined EEG-fNIRS study”. Frontiers in Behavioral Neuroscience. 2018; 12: 67. doi: 10.3389/fnbeh.2018.00067.

Sport Sciences and Health Research
Volume 15, Issue 1
January 2023
Pages 113-125

Files

Share

How to cite

Statistics