Cerebellar transcranial direct current stimulation for learning a novel split-belt treadmill task: a randomised controlled trial.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
16 07 2020
16 07 2020
Historique:
received:
06
10
2019
accepted:
30
06
2020
entrez:
18
7
2020
pubmed:
18
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
This study aimed to examine the effect of repeated anodal cerebellar transcranial direct current stimulation (ctDCS) on learning a split-belt treadmill task. Thirty healthy individuals randomly received three consecutive sessions of active or sham anodal ctDCS during split-belt treadmill training. Motor performance and strides to steady-state performance were evaluated before (baseline), during (adaptation), and after (de-adaptation) the intervention. The outcomes were measured one week later to assess absolute learning and during the intervention to evaluate cumulative, consecutive, and session-specific effects. Data were analysed using linear mixed-effects regression models. During adaptation, there was no significant difference in absolute learning between the groups (p > 0.05). During de-adaptation, a significant difference in absolute learning between the groups (p = 0.03) indicated slower de-adaptation with anodal ctDCS. Pre-planned secondary analysis revealed that anodal ctDCS significantly reduced the cumulative (p = 0.01) and consecutive-session effect (p = 0.01) on immediate adaptation. There were significant cumulative (p = 0.02) and session-specific effects (p = 0.003) on immediate de-adaptation. Repeated anodal ctDCS does not enhance motor learning measured during adaptation to a split-belt treadmill task. However, it influences the maintenance of learnt walking patterns, suggesting that it may be beneficial in maintaining therapeutic effects.
Identifiants
pubmed: 32678285
doi: 10.1038/s41598-020-68825-2
pii: 10.1038/s41598-020-68825-2
pmc: PMC7366632
doi:
Types de publication
Journal Article
Randomized Controlled Trial
Langues
eng
Sous-ensembles de citation
IM
Pagination
11853Références
Block, H. J. & Celnik, P. Can cerebellar transcranial direct current stimulation become a valuable neurorehabilitation intervention?. Expert Rev. Neurother. 12, 1275–1277. https://doi.org/10.1586/ern.12.121 (2012).
doi: 10.1586/ern.12.121
pubmed: 23234389
pmcid: 4948999
Grimaldi, G. et al. Non-invasive cerebellar stimulation-A consensus paper. Cerebellum 13, 121–138. https://doi.org/10.1007/s12311-013-0514-7 (2014).
doi: 10.1007/s12311-013-0514-7
pubmed: 23943521
Ugawa, Y. et al. Modulation of motor cortical excitability by electrical stimulation over the cerebellum in man. J Physiol 441, 57–72 (1991).
doi: 10.1113/jphysiol.1991.sp018738
Galea, J. M., Jayaram, G., Ajagbe, L. & Celnik, P. Modulation of cerebellar excitability by polarity-specific noninvasive direct current stimulation. J. Neurosci. 29, 9115–9122. https://doi.org/10.1523/JNEUROSCI.2184-09.2009 (2009).
doi: 10.1523/JNEUROSCI.2184-09.2009
pubmed: 19605648
pmcid: 2760225
Jayaram, G., Galea, J. M., Bastian, A. J. & Celnik, P. Human locomotor adaptive learning is proportional to depression of cerebellar excitability. Cereb. Cortex 21, 1901–1909. https://doi.org/10.1093/cercor/bhq263 (2011).
doi: 10.1093/cercor/bhq263
pubmed: 21239392
pmcid: 3202738
De Zeeuw, C. I. & Ten Brinke, M. M. Motor learning and the cerebellum. Cold Spring Harb Perspect Biol 7, a021683. https://doi.org/10.1101/cshperspect.a021683 (2015).
doi: 10.1101/cshperspect.a021683
pubmed: 26330521
pmcid: 4563713
Ito, M. Mechanisms of motor learning in the cerebellum. Brain Res 886, 237–245 (2000).
doi: 10.1016/S0006-8993(00)03142-5
Yanagihara, D. & Kondo, I. Nitric oxide plays a key role in adaptive control of locomotion in cat. Proc Natl Acad Sci USA 93, 13292–13297 (1996).
doi: 10.1073/pnas.93.23.13292
Ehsani, F., Bakhtiary, A., Jaberzadeh, S., Talimkhani, A. & Hajihasani, A. Differential effects of primary motor cortex and cerebellar transcranial direct current stimulation on motor learning in healthy individuals: a randomized double-blind sham-controlled study. Neurosci. Res. 112, 10–19. https://doi.org/10.1016/j.neures.2016.06.003 (2016).
doi: 10.1016/j.neures.2016.06.003
pubmed: 27349154
Samaei, A., Ehsani, F., Zoghi, M., Yosephi, M. H. & Jaberzadeh, S. Online and offline effects of cerebellar transcranial direct current stimulation on motor learning in healthy older adults: a randomized double-blind sham-controlled study. Eur. J. Neurosci. 45, 1177–1185. https://doi.org/10.1111/ejn.13559 (2017).
doi: 10.1111/ejn.13559
pubmed: 28278354
Ferrucci, R., Cortese, F. & Priori, A. Cerebellar tDCS: How to do it. Cerebellum 14, 27–30. https://doi.org/10.1007/s12311-014-0599-7 (2015).
doi: 10.1007/s12311-014-0599-7
pubmed: 25231432
van Dun, K., Bodranghien, F., Marien, P. & Manto, M. U. tDCS of the cerebellum: Where do we stand in 2016? Technical issues and critical review of the literature. Front. Hum. Neurosci. 10, 1. https://doi.org/10.3389/fnhum.2016.00199 (2016).
doi: 10.3389/fnhum.2016.00199
Schmidt, R.A. & Lee, T.D. Motor control and learning: a behavioral emphasis. 5th edn. 327–45 (Human Kinetics, 2011).
Bastian, A. J. Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol 21, 628–633. https://doi.org/10.1097/WCO.0b013e328315a293 (2008).
doi: 10.1097/WCO.0b013e328315a293
pubmed: 18989103
pmcid: 2954436
Reisman, D. S., Block, H. J. & Bastian, A. J. Interlimb coordination during locomotion: what can be adapted and stored?. J Neurophysiol 94, 2403–2415. https://doi.org/10.1152/jn.00089.2005 (2005).
doi: 10.1152/jn.00089.2005
pubmed: 15958603
Martin, T.A., Keating, J. G., P Goodkin, H., Bastian, A.J. & Thach, W. Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Vol. 119 (Pt 4) (1996).
Kojima, Y., Iwamoto, Y. & Yoshida, K. Memory of learning facilitates saccadic adaptation in the monkey. J. Neurosci. 24, 7531. https://doi.org/10.1523/JNEUROSCI.1741-04.2004 (2004).
doi: 10.1523/JNEUROSCI.1741-04.2004
pubmed: 15329400
pmcid: 6729647
Kumari, N., Taylor, D. & Signal, N. The effect of cerebellar transcranial direct current stimulation on motor learning: a systematic review of randomized controlled trials. Front. Hum. Neurosci. 13, 328. https://doi.org/10.3389/fnhum.2019.00328 (2019).
doi: 10.3389/fnhum.2019.00328
pubmed: 31636552
pmcid: 6788395
Galea, J. M., Vazquez, A., Pasricha, N., de Xivry, J. J. O. & Celnik, P. Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. Cereb. Cortex 21, 1761–1770. https://doi.org/10.1093/cercor/bhq246 (2011).
doi: 10.1093/cercor/bhq246
pubmed: 21139077
Jayaram, G. et al. Modulating locomotor adaptation with cerebellar stimulation. J. Neurophysiol. 107, 2950–2957. https://doi.org/10.1152/jn.00645.2011 (2012).
doi: 10.1152/jn.00645.2011
pubmed: 22378177
pmcid: 3378372
Avila, E. et al. Cerebellar transcranial direct current stimulation effects on saccade adaptation. Neural Plast. 1, 1. https://doi.org/10.1155/2015/968970 (2015).
doi: 10.1155/2015/968970
Herzfeld, D. J. et al. Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. NeuroImage 98, 147–158. https://doi.org/10.1016/j.neuroimage.2014.04.076 (2014).
doi: 10.1016/j.neuroimage.2014.04.076
pubmed: 24816533
pmcid: 4099269
Cantarero, G. et al. Cerebellar direct current stimulation enhances on-line motor skill acquisition through an effect on accuracy. J. Neurosci. 35, 3285–3290. https://doi.org/10.1523/JNEUROSCI.2885-14.2015 (2015).
doi: 10.1523/JNEUROSCI.2885-14.2015
pubmed: 25698763
pmcid: 4331640
Poortvliet, P., Hsieh, B., Cresswell, A., Au, J. & Meinzer, M. Cerebellar transcranial direct current stimulation improves adaptive postural control. Clin. Neurophysiol. 129, 33–41. https://doi.org/10.1016/j.clinph.2017.09.118 (2018).
doi: 10.1016/j.clinph.2017.09.118
pubmed: 29136550
Yavari, F. et al. Cerebellum as a forward but not inverse model in visuomotor adaptation task: a tDCS-based and modeling study. Exp. Brain Res. 234, 997–1012. https://doi.org/10.1007/s00221-015-4523-2 (2016).
doi: 10.1007/s00221-015-4523-2
pubmed: 26706039
Thair, H., Holloway, A. L., Newport, R. & Smith, A. D. Transcranial direct current stimulation (tDCS): a beginner’s guide for design and implementation. Front Neurosci 11, 641. https://doi.org/10.3389/fnins.2017.00641 (2017).
doi: 10.3389/fnins.2017.00641
pubmed: 29213226
pmcid: 5702643
Brunoni, A. R., Schestatsky, P., Lotufo, P. A., Bensenor, I. M. & Fregni, F. Comparison of blinding effectiveness between sham tDCS and placebo sertraline in a 6-week major depression randomized clinical trial. Clin. Neurophysiol. 125, 298–305. https://doi.org/10.1016/j.clinph.2013.07.020 (2014).
doi: 10.1016/j.clinph.2013.07.020
pubmed: 23994192
O’Connell, N. E. et al. Rethinking clinical trials of transcranial direct current stimulation: participant and assessor blinding is inadequate at intensities of 2mA. PLoS ONE 7, e47514. https://doi.org/10.1371/journal.pone.0047514 (2012).
doi: 10.1371/journal.pone.0047514
pubmed: 23082174
pmcid: 3474749
Huynh, K. V., Sarmento, C. H., Roemmich, R. T., Stegemöller, E. L. & Hass, C. J. Comparing aftereffects after split-belt treadmill walking and unilateral stepping. Med. Sci. Sports Exerc. 46, 1392–1399. https://doi.org/10.1249/mss.0000000000000240 (2014).
doi: 10.1249/mss.0000000000000240
pubmed: 24389526
pmcid: 4104418
Sutherland, D. H. The evolution of clinical gait analysis: Part II Kinematics. Gait Posture 16, 159–179 (2002).
doi: 10.1016/S0966-6362(02)00004-8
Finley, J. M., Statton, M. A. & Bastian, A. J. A novel optic flow pattern speeds split-belt locomotor adaptation. J Neurophysiol 111, 969–976. https://doi.org/10.1152/jn.00513.2013 (2014).
doi: 10.1152/jn.00513.2013
pubmed: 24335220
Rashid, U., Kumari, N., Taylor, D., David, T. & Signal, N. Gait event anomaly detection and correction during a split-belt treadmill task. IEEE Access 1, 1 (2019).
Bates, D., Mächler, M., Bolker, B. & Walker, S (2015). Fitting linear mixed-effects models using lme4. 67, 48. https://doi.org/10.18637/jss.v067.i01 (2015).
Kutner, M. H., Nachtsheim, C. J., Neter, J. & Li, W. Applied linear statistical models (McGraw-Hill Irwin, New York, 2005).
Rao, C.R., Miller, J.P. & Rao, D.C. Handbook of statistics: epidemiology and medical statistics. (2007).
Norusis, M. J. & Inc, S. PASW statistics 18: Statistical procedures companion. (Prentice-Hall, 2010).
Field, A. Discovering statistics using SPSS. Vol. 497 (Sage London, 2011).
Boisgontier, M. P. & Cheval, B. The anova to mixed model transition. Neurosci Biobehav Rev 68, 1004–1005. https://doi.org/10.1016/j.neubiorev.2016.05.034 (2016).
doi: 10.1016/j.neubiorev.2016.05.034
pubmed: 27241200
Brunner, E., Konietschke, F., Pauly, M. & Puri, M. L. Rank-based procedures in factorial designs: hypotheses about non-parametric treatment effects. J. R. Stat. Soc. Ser. B (Stat. Methodol.) 79, 1463–1485 (2017).
doi: 10.1111/rssb.12222
de Boer, M. R., Waterlander, W. E., Kuijper, L. D., Steenhuis, I. H. & Twisk, J. W. Testing for baseline differences in randomized controlled trials: an unhealthy research behavior that is hard to eradicate. Int. J. Behav. Nutr. Phys. Act. 12, 4. https://doi.org/10.1186/s12966-015-0162-z (2015).
doi: 10.1186/s12966-015-0162-z
pubmed: 25616598
pmcid: 4310023
Hurvich, C. M. & Tsai, C.-L. Bias of the corrected AIC criterion for underfitted regression and time series models. Biometrika 78, 499–509. https://doi.org/10.1093/biomet/78.3.499 (1991).
doi: 10.1093/biomet/78.3.499
Rao, C.R., Miller, P. & Rao, D.C. in Handbook of Statistics: Epidemiology and Medical Statistics 1–351 (Elsevier Inc., 2011).
Field, A. Discovering statistics using SPSS. London ECIY 1SP. (SAGE Publications, Inc, 2011).
Krakauer, J. W. Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr. Opin. Neurol. 19, 84–90. https://doi.org/10.1097/01.wco.0000200544.29915.cc (2006).
doi: 10.1097/01.wco.0000200544.29915.cc
pubmed: 16415682
Blanchette, A., Moffet, H., Roy, J. S. & Bouyer, L. J. Effects of repeated walking in a perturbing environment: a 4-day locomotor learning study. J Neurophysiol 108, 275–284. https://doi.org/10.1152/jn.01098.2011 (2012).
doi: 10.1152/jn.01098.2011
pubmed: 22496521
Panouilleres, M. T., Joundi, R. A., Brittain, J.-S. & Jenkinson, N. Reversing motor adaptation deficits in the ageing brain using non-invasive stimulation. J. Physiol. 593, 3645–3655. https://doi.org/10.1113/JP270484 (2015).
doi: 10.1113/JP270484
pubmed: 25929230
pmcid: 4560588
Taubert, M. et al. Remote effects of non-invasive cerebellar stimulation on error processing in motor re-learning. Brain Stimul. 9, 692–699. https://doi.org/10.1016/j.brs.2016.04.007 (2016).
doi: 10.1016/j.brs.2016.04.007
pubmed: 27157059
Criscimagna-Hemminger, S. E., Bastian, A. J. & Shadmehr, R. Size of error affects cerebellar contributions to motor learning. J. Neurophysiol. 103, 2275–2284. https://doi.org/10.1152/jn.00822.2009 (2010).
doi: 10.1152/jn.00822.2009
pubmed: 20164398
pmcid: 2853280
Malone, L. A., Vasudevan, E. V. & Bastian, A. J. Motor adaptation training for faster relearning. J Neurosci 31, 15136–15143. https://doi.org/10.1523/JNEUROSCI.1367-11.2011 (2011).
doi: 10.1523/JNEUROSCI.1367-11.2011
pubmed: 22016547
pmcid: 3209529
Ruitenberg, M. F. L. et al. Neural correlates of multi-day learning and savings in sensorimotor adaptation. Sci Rep 8, 14286. https://doi.org/10.1038/s41598-018-32689-4 (2018).
doi: 10.1038/s41598-018-32689-4
pubmed: 30250049
pmcid: 6155344
Bienenstock, E. L., Cooper, L. N. & Munro, P. W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32–48 (1982).
doi: 10.1523/JNEUROSCI.02-01-00032.1982
Fricke, K. et al. Time course of the induction of homeostatic plasticity generated by repeated transcranial direct current stimulation of the human motor cortex. J. Neurophysiol. 105, 1141–1149. https://doi.org/10.1152/jn.00608.2009 (2011).
doi: 10.1152/jn.00608.2009
pubmed: 21177994
Monte-Silva, K., Kuo, M.-F., Liebetanz, D., Paulus, W. & Nitsche, M. A. 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 (2010).
doi: 10.1152/jn.00924.2009
pubmed: 20107115
Hulst, T. et al. Cerebellar patients do not benefit from cerebellar or M1 transcranial direct current stimulation during force-field reaching adaptation. J. Neurophysiol. 118, 732–748. https://doi.org/10.1152/jn.00808.2016 (2017).
doi: 10.1152/jn.00808.2016
pubmed: 28469001
pmcid: 5539455
Jalali, R., Miall, R. & Galea, J. M. No consistent effect of cerebellar transcranial direct current stimulation on visuomotor adaptation. J. Neurophysiol. 118, 655–665 (2017).
doi: 10.1152/jn.00896.2016
Mamlins, A., Hulst, T., Donchin, O., Timmann, D. & Claassen, J. No effects of cerebellar transcranial direct current stimulation on force field and visuomotor reach adaptation in young and healthy subjects. J. Neurophysiol. 121, 2112–2125. https://doi.org/10.1152/jn.00352.2018 (2019).
doi: 10.1152/jn.00352.2018
pubmed: 30943093
Rahman, A., Toshev, P. K. & Bikson, M. Polarizing cerebellar neurons with transcranial. Direct Curr. Stimul. https://doi.org/10.1016/j.clinph.2013.10.003 (2014).
doi: 10.1016/j.clinph.2013.10.003
Parazzini, M., Fiocchi, S., Rossi, E., Paglialonga, A. & Ravazzani, P. Transcranial direct current stimulation: estimation of the electric field and of the current density in an anatomical human head model. IEEE Trans. Biomed. Eng. 58, 1773–1780 (2011).
doi: 10.1109/TBME.2011.2116019
Reisman, D. S., Bastian, A. J. & Morton, S. M. Neurophysiologic and rehabilitation insights from the split-belt and other locomotor adaptation paradigms. Phys. Ther. 90, 187–195. https://doi.org/10.2522/ptj.20090073 (2010).
doi: 10.2522/ptj.20090073
pubmed: 20023001
pmcid: 2816031
Maas, C. J. & Hox, J. J. Sufficient sample sizes for multilevel modeling. Methodology 1, 86–92 (2005).
doi: 10.1027/1614-2241.1.3.86