Abstract
Recovery is dynamic during acute stroke, but whether new motor skills can be acquired with the paretic upper limb (UL) during this recovery period is unknown. Clarifying this unknown is important, because neurorehabilitation largely relies on motor learning. The aim was to investigate whether, during acute stroke, patients achieved motor skill learning and retention with the paretic UL. Over 3 consecutive days (D1–D3), 14 patients practiced with their paretic UL the CIRCUIT, a motor skill learning task with a speed/accuracy trade-off (SAT). A Learning Index (LI) was used to quantify normalised SAT changes in comparison with baseline. Spontaneous motor recovery was quantified by another task without SAT constraint (EASY), by grip force (GF), and the Box and Blocks test (BBT). In patients, CIRCUIT LI improved 98% ± 66.2 (mean ± SD). This improvement was similar to that of young healthy individuals (n = 30) who trained with a slightly different protocol for 3 consecutive days (83.8% ± 58.8%). Generalisation of SAT gains to an untrained circuit was observed in both groups. From D1 to D3, stroke patients improved their performance on EASY, while changes in GF and BBT were heterogeneous. During acute stroke, patients retained SAT gains for a motor skill learned with the paretic UL in a manner similar to that of healthy individuals. These results demonstrate acute stroke patients achieved motor skill learning and retention that exceeded paretic UL improvements explained by spontaneous recovery.
Similar content being viewed by others
References
Mozaffarian D, Benjamin EJ, Go AS et al (2016) Heart disease and stroke statistics—2016 update: a report from the American Heart Association. Circulation 133:e38–360. https://doi.org/10.1161/cir.0000000000000350
Dewilde S, Annemans L, Peeters A et al (2017) Modified Rankin scale as a determinant of direct medical costs after stroke. Int J Stroke. https://doi.org/10.1177/1747493017691984
Hackett ML, Duncan JR, Anderson CS et al (2000) Health-related quality of life among long-term survivors of stroke: results from the Auckland Stroke Study, 1991–1992. Stroke 31:440–447
Hardwick RM, Rajan VA, Bastian AJ et al (2017) Motor learning in stroke: trained patients are not equal to untrained patients with less impairment. Neurorehabil Neural Repair 31:178–189. https://doi.org/10.1177/1545968316675432
Hankey GJ, Jamrozik K, Broadhurst RJ et al (2002) Long-term disability after first-ever stroke and related prognostic factors in the Perth Community Stroke Study, 1989–1990. Stroke 33:1034–1040. https://doi.org/10.1161/01.STR.0000012515.66889.24
Stinear C (2010) Prediction of recovery of motor function after stroke. Lancet Neurol 9:1228–1232. https://doi.org/10.1016/S1474-4422(10)70247-7
Bernhardt J, Hayward KS, Kwakkel G et al (2017) Agreed definitions and a shared vision for new standards in stroke recovery research: the Stroke Recovery and Rehabilitation Roundtable taskforce. Int J Stroke 12:444–450. https://doi.org/10.1177/1747493017711816
Winters C, van Wegen EEH, Daffertshofer A, Kwakkel G (2015) Generalizability of the proportional recovery model for the upper extremity after an ischemic stroke. Neurorehabil Neural Repair 29:614–622. https://doi.org/10.1177/1545968314562115
Byblow WD, Stinear CM, Barber PA et al (2015) Proportional recovery after stroke depends on corticomotor integrity. Ann Neurol 78:848–859. https://doi.org/10.1002/ana.24472
Hawe RL, Scott SH, Dukelow SP (2019) Taking proportional out of stroke recovery. Stroke 50:204–211. https://doi.org/10.1161/strokeaha.118.023006
Kundert R, Goldsmith J, Veerbeek JM et al (2019) What the proportional recovery rule is (and is not): methodological and statistical considerations. Neurorehabil Neural Repair. https://doi.org/10.1177/1545968319872996
Kreisel SH, Hennerici MG, Bazner H (2007) Pathophysiology of stroke rehabilitation: the natural course of clinical recovery, use-dependent plasticity and rehabilitative outcome. Cerebrovasc Dis 23:243–255. https://doi.org/10.1159/000098323
Krakauer JW (2015) The applicability of motor learning to neurorehabilitation. Oxford Textb Neurorehabilitation. https://doi.org/10.1093/med/9780199673711.001.0001
Kal E, Winters M, van der Kamp J et al (2016) Is implicit motor learning preserved after stroke? A systematic review with meta-analysis. PLoS ONE 11:e0166376–e0166376. https://doi.org/10.1371/journal.pone.0166376
Krakauer JW, Carmichael ST, Corbett D, Wittenberg GF (2012) Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair 26:923–931. https://doi.org/10.1177/1545968312440745
Dobkin BH, Carmichael ST (2015) The specific requirements of neural repair trials for stroke. Neurorehabil Neural Repair 30:470–478. https://doi.org/10.1177/1545968315604400
Jones TA (2017) Motor compensation and its effects on neural reorganization after stroke. Nat Rev Neurosci 18:267–280. https://doi.org/10.1038/nrn.2017.26
Krakauer JW, Mazzoni P (2011) Human sensorimotor learning: adaptation, skill, and beyond. Curr Opin Neurobiol 21:636–644. https://doi.org/10.1016/j.conb.2011.06.012
Jang SH (2013) Motor function-related maladaptive plasticity in stroke: a review. NeuroRehabilitation 32:311–316. https://doi.org/10.3233/nre-130849
Takeuchi N, Izumi SI (2012) Maladaptive plasticity for motor recovery after stroke: mechanisms and approaches. Neural Plast. https://doi.org/10.1155/2012/359728
Jablonska A, Lukomska B (2011) Stroke induced brain changes: Implications for stem cell transplantation. Acta Neurobiol Exp 71:74–85
Lefebvre S, Dricot L, Gradkowski W et al (2012) Brain activations underlying different patterns of performance improvement during early motor skill learning. Neuroimage 62:290–299. https://doi.org/10.1016/j.neuroimage.2012.04.052
Lefebvre S, Laloux P, Peeters A et al (2012) Dual-tDCS enhances online motor skill learning and long-term retention in chronic stroke patients. Front Hum Neurosci 6:343. https://doi.org/10.3389/fnhum.2012.00343
Lefebvre S, Dricot L, Laloux P et al (2015) Neural substrates underlying motor skill learning in chronic hemiparetic stroke patients. Front Hum Neurosci 9:320. https://doi.org/10.3389/fnhum.2015.00320
Mathiowetz V, Volland G, Kashman N, Weber K (1985) Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 39:386–391
Mathiowetz V, Weber K, Volland G, Kashman N (1984) Reliability and validity of grip and pinch strength evaluations. J Hand Surg Am 9:222–226. https://doi.org/10.1016/S0363-5023(84)80146-X
Brott T, Adams HP, Olinger CP et al (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20:864–870. https://doi.org/10.1161/01.STR.20.7.864
Xu J, Ejaz N, Hertler B et al (2017) Separable systems for recovery of finger strength and control after stroke. J Neurophysiol 118:1151–1163. https://doi.org/10.1152/jn.00123.2017
Cortes JC, Goldsmith J, Harran MD et al (2017) A short and distinct time window for recovery of arm motor control early after stroke revealed with a global measure of trajectory kinematics. Neurorehabil Neural Repair 31:552–560. https://doi.org/10.1177/1545968317697034
Kreisel SH, Bäzner H, Hennerici MG (2006) Pathophysiology of stroke rehabilitation: temporal aspects of neurofunctional recovery. Cerebrovasc Dis 21:6–17. https://doi.org/10.1159/000089588
Jones TA, Adkins DL (2015) Motor system reorganization after stroke: stimulating and training toward perfection. Physiology 30:358–370. https://doi.org/10.1152/physiol.00014.2015
Levin MF, Michaelsen SM, Cirstea CM, Roby-Brami A (2002) Use of the trunk for reaching targets placed within and beyond the reach in adult hemiparesis. Exp Brain Res 143:171–180. https://doi.org/10.1007/s00221-001-0976-6
Levin MF, Liebermann DG, Parmet Y, Berman S (2016) Compensatory versus noncompensatory shoulder movements used for reaching in stroke. Neurorehabil Neural Repair 30:635–646. https://doi.org/10.1177/1545968315613863
Lefebvre S, Dricot L, Laloux P et al (2015) Neural substrates underlying stimulation-enhanced motor skill learning after stroke. Brain 138:149–163. https://doi.org/10.1093/brain/awu336
Dayan E, Cohen LG (2011) Neuroplasticity subserving motor skill learning. Neuron 72:443–454. https://doi.org/10.1016/j.neuron.2011.10.008
Shmuelof L, Krakauer JW, Mazzoni P (2012) How is a motor skill learned? Change and invariance at the levels of task success and trajectory control. J Neurophysiol 108:578–594. https://doi.org/10.1152/jn.00856.2011
Werner S, Bock O, Gizewski ER et al (2010) Visuomotor adaptive improvement and aftereffects are impaired differentially following cerebellar lesions in SCA and PICA territory. Exp Brain Res 201:429–439. https://doi.org/10.1007/s00221-009-2052-6
Mutha PK, Sainburg RL, Haaland KY (2011) Left Parietal Regions Are Critical for Adaptive Visuomotor Control. J Neurosci 31:6972–6981. https://doi.org/10.1523/JNEUROSCI.6432-10.2011
Acknowledgements
We are grateful to the patients who participated in the project, and to the nursing team of the Stroke Unit for flexibility and assistance. We thank W. Gradkowski for the initial development of the “circuit game” software. We thank the healthy individuals, as well as Dr. Brieuc Vanollande and Dr. Barbara Delgrange who collected this data set. We thank Stéphanie Lefebvre (Ph.D.) and Wojciech Gradkowski for the motor task implementation.
Funding
The work of YV was supported by the following grants: Fonds de la Recherche Scientifique (F.R.S.-FNRS, Nos. F 3/5/5-MCF/ROI/BC-19727 and F 3/5/5-MCF/XH/FC-17514) Post-Doctorate Clinical Master Specialist [SPD] 1.R.506.16 and 1.R.506.18, Fonds Spécial de Recherche (FSR) grant from the Université Catholique de Louvain (UCL) 2016, and Fondation Mont-Godinne 2015–2016. The work of MYD was supported by UCL FSR grant in 2013 and by FRNS-FRIA grants F 3/5/5 2014 and 2016. The work of AR was supported by a grant from the Fondation Mont-Godinne 2015 and by a UCL FSR grant 2016. The work of MB was self-funded.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
All procedures performed in this study were approved by the local Ethics Committee (CHU UCL Namur Mont-Godinne) and were in accordance with the 1964 Helsinki declaration and its later amendments.
Informed consent
All patients (or the next of kin, on the behalf of the patient) provided a written informed consent prior to participating in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Baguma, M., Yeganeh Doost, M., Riga, A. et al. Preserved motor skill learning in acute stroke patients. Acta Neurol Belg 120, 365–374 (2020). https://doi.org/10.1007/s13760-020-01304-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13760-020-01304-7