The importance of different learning stages for motor sequence learning after stroke

Christiane Dahms, Stefan Brodoehl, Otto W Witte, Carsten M Klingner, Christiane Dahms, Stefan Brodoehl, Otto W Witte, Carsten M Klingner

Abstract

The task of learning predefined sequences of interrelated motor actions is of everyday importance and has also strong clinical importance for regaining motor function after brain lesions. A solid understanding of sequence learning in stroke patients can help clinicians to optimize and individualize rehabilitation strategies. Moreover, to investigate the impact of a focal lesion on the ability to successfully perform motor sequence learning can enhance our comprehension of the underlying physiological principles of motor sequence learning. In this article, we will first provide an overview of current concepts related to motor sequence learning in healthy subjects with focus on the involved brain areas and their assumed functions according to the temporal stage model. Subsequently, we will consider the question of what we can learn from studies investigating motor sequence learning in stroke patients. We will first focus on the implications of lesion location. Then, we will analyze whether distinct lesion locations affect specific learning stages. Finally, we will discuss the implications for clinical rehabilitation and suggest directions for further research.

Keywords: motor cortex; motor rehabilitation; plasticity; sequence learning; stroke.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

© The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Schematic representation of the locations of areas involved in different stages of motor sequence learning. Abbreviations: CB, cerebellum; DLPFC, dorsolateral prefrontal cortex; M1, primary motor cortex; PMA, premotor area; PPC, posterior parietal cortex; pre‐SMA, pre‐supplementary motor area; SMA, supplementary motor area
Figure 2
Figure 2
Schematic representation of the involvement and the interaction of brain areas in the three stages of motor sequence learning. Abbreviations: M1, primary motor cortex; PMA, premotor area; PPC, posterior parietal cortex; pre‐SMA, pre‐supplementary motor area; SMA, supplementary motor area)

References

    1. Albouy, G. , Sterpenich, V. , Balteau, E. , Vandewalle, G. , Desseilles, M. , Dang‐Vu, T. , … Maquet, P. (2008). Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron, 58, 261–272. 10.1016/j.neuron.2008.02.008
    1. Alexander, G. E. , DeLong, M. R. , & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381. 10.1146/annurev.ne.09.030186.002041
    1. Baars, B. J. (2010). Cognition, brain, and consciousness. Elsevier, Amsterdam. 10.1016/C2009-0-01556-6
    1. Bastian, A. J. (2006). Learning to predict the future: The cerebellum adapts feedforward movement control. Current Opinion in Neurobiology, 16, 645–649. 10.1016/j.conb.2006.08.016
    1. Boyd, L. A. , Edwards, J. D. , Siengsukon, C. S. , Vidoni, E. D. , Wessel, B. D. , & Linsdell, M. A. (2009). Motor sequence chunking is impaired by basal ganglia stroke. Neurobiology of Learning and Memory, 92, 35–44. 10.1016/j.nlm.2009.02.009
    1. Boyd, L. A. , Quaney, B. M. , Pohl, P. S. , & Winstein, C. J. (2007). Learning implicitly: Effects of task and severity after stroke. Neurorehabilitation and Neural Repair, 21, 444–454. 10.1177/1545968307300438
    1. Boyd, L. A. , & Winstein, C. J. (2001). Implicit motor‐sequence learning in humans following unilateral stroke: The impact of practice and explicit knowledge. Neuroscience Letters, 298, 65–69. 10.1016/S0304-3940(00)01734-1
    1. Boyd, L. A. , & Winstein, C. J. (2003). Impact of explicit information on implicit motor‐sequence learning following middle cerebral artery stroke. Physical Therapy, 83, 976–989. 10.1093/ptj/83.11.976
    1. Boyd, L. A. , & Winstein, C. J. (2004). Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learning & Memory, 11, 388–396. 10.1101/lm.80104
    1. Censor, N. (2013). Generalization of perceptual and motor learning: A causal link with memory encoding and consolidation? Neuroscience, 250, 201–207. 10.1016/j.neuroscience.2013.06.062
    1. Censor, N. , Sagi, D. , & Cohen, L. G. (2012). Common mechanisms of human perceptual and motor learning. Nature Reviews Neuroscience, 13, 658–664. 10.1038/nrn3315
    1. Clower, D. M. , Dum, R. P. , & Strick, P. L. (2005). Basal ganglia and cerebellar inputs to ‘AIP.’. Cerebral Cortex, 15, 913–920. 10.1093/cercor/bhh190
    1. Collins, P. , Roberts, A. C. , Dias, R. , Everitt, B. J. , & Robbins, T. W. (1998). Perseveration and strategy in a novel spatial self‐ordered sequencing task for nonhuman primates: Effects of excitotoxic lesions and dopamine depletions of the prefrontal cortex. Journal of Cognitive Neuroscience, 10, 332–354.
    1. Debas, K. , Carrier, J. , Barakat, M. , Marrelec, G. , Bellec, P. , Tahar, A. H. , … Doyon, J. (2014). Off‐line consolidation of motor sequence learning results in greater integration within a cortico‐striatal functional network. NeuroImage, 99, 50–58. 10.1016/j.neuroimage.2014.05.022
    1. Debas, K. , Carrier, J. , Orban, P. , Barakat, M. , Lungu, O. , Vandewalle, G. , … Doyon, J. (2010). Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proceedings of the National Academy of Sciences, 107, 17839–17844. 10.1073/pnas.1013176107
    1. Diedrichsen, J. , Balsters, J. H. , Flavell, J. , Cussans, E. , & Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. NeuroImage, 46, 39–46. 10.1016/j.neuroimage.2009.01.045
    1. Diedrichsen, J. , & Kornysheva, K. (2015). Motor skill learning between selection and execution. Trends in Cognitive Sciences, 19, 227–233. 10.1016/j.tics.2015.02.003
    1. Dirnberger, G. , Novak, J. , & Nasel, C. (2013). Perceptual sequence learning is more severely impaired than motor sequence learning in patients with chronic cerebellar stroke. Journal of Cognitive Neuroscience, 25, 2207–2215. 10.1162/jocn_a_00444
    1. Dovern, A. , Fink, G. R. , Timpert, D. C. , Saliger, J. , Karbe, H. , Weiss, P. H. , & Koch, I. (2015). Timing matters? Learning of complex spatiotemporal sequences in left‐hemisphere stroke patients. Journal of Cognitive Neuroscience, 28, 223–236. 10.1162/jocn_a_00890
    1. Dovern, A. , Niessen, E. , Ant, J. M. , Saliger, J. , Karbe, H. , Fink, G. R. , … Weiss, P. H. (2017). Timing independent spatial motor sequence learning is preserved in left hemisphere stroke. Neuropsychologia, 106, 322–327. 10.1016/j.neuropsychologia.2017.09.030
    1. Doya, K. (2000). Complementary roles of basal ganglia and cerebellum in learning and motor control. Current Opinion in Neurobiology, 10, 732–739.
    1. Doyon, J. (2008). Motor sequence learning and movement disorders. Current Opinion in Neurology, 21, 478–483. 10.1097/WCO.0b013e328304b6a3
    1. Doyon, J. , & Benali, H. (2005). Reorganization and plasticity in the adult brain during learning of motor skills. Current Opinion in Neurobiology, 15, 161–167.
    1. Doyon, J. , Korman, M. , Morin, A. , Dostie, V. , Hadj Tahar, A. , Benali, H. , … Carrier, J. (2009). Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Experimental Brain Research, 195, 15–26. 10.1007/s00221-009-1748-y
    1. Doyon, J. , Penhune, V. , & Ungerleider, L. G. (2003). Distinct contribution of the cortico‐striatal and cortico‐cerebellar systems to motor skill learning. Neuropsychologia, 41, 252–262. 10.1016/S0028-3932(02)00158-6
    1. Doyon, J. , Song, A. W. , Karni, A. , Lalonde, F. , Adams, M. M. , & Ungerleider, L. G. (2002). Experience‐dependent changes in cerebellar contributions to motor sequence learning. Proceedings of the National Academy of Sciences, 99, 1017–1022. 10.1073/pnas.022615199
    1. Durham, K. , Van Vliet, P. M. , Badger, F. , & Sackley, C. (2009). Use of information feedback and attentional focus of feedback in treating the person with a hemiplegic arm. Physiotherapy Research International, 14, 77–90. 10.1002/pri.431
    1. Eliassen, J. , Souza, T. , & Sanes, J. (2001). Human brain activation accompanying explicitly directed movement sequence learning. Experimental Brain Research, 141, 269–280. 10.1007/s002210100822
    1. Exner, C. , Weniger, G. , & Irle, E. (2001). Implicit and explicit memory after focal thalamic lesions. Neurology, 57, 2054–2063. 10.1212/WNL.57.11.2054
    1. Fleming, M. K. , Newham, D. J. , & Rothwell, J. C. (2018). Explicit motor sequence learning with the paretic arm after stroke. Disability and Rehabilitation, 40, 323–328. 10.1080/09638288.2016.1258091
    1. Fonollosa, J. , Neftci, E. , & Rabinovich, M. (2015). Learning of chunking sequences in cognition and behavior. PLoS Computational Biology, 11, e1004592 10.1371/journal.pcbi.1004592
    1. Ghilardi, M. F. , Moisello, C. , Silvestri, G. , Ghez, C. , & Krakauer, J. W. (2009). Learning of a sequential motor skill comprises explicit and implicit components that consolidate differently. Journal of Neurophysiology, 101, 2218–2229. 10.1152/jn.01138.2007
    1. Gomez Beldarrain, M. (1999). Procedural learning is impaired in patients with prefrontal lesions | Ovid [WWW Document]. Retrieved from .
    1. Gomez Beldarrain, M. , Astorgano, A. G. , Gonzalez, A. B. , & Garcia‐Monco, J. C. (2008). Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions. Clinical Neurology and Neurosurgery, 110, 245–252. 10.1016/j.clineuro.2007.11.004
    1. Gomez Beldarrain, M. , Gafman, J. , Ruiz de Velasco, I. , Pascual‐Leone, A. , & Garcia‐Monco, J. (2002). Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks. Experimental Brain Research, 142, 529–538. 10.1007/s00221-001-0935-2
    1. Gordon, A. M. , Lee, J. H. , Flament, D. , Ugurbil, K. , & Ebner, T. J. (1998). Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements. Experimental Brain Research, 121, 153–166.
    1. Hardwick, R. M. , Rottschy, C. , Miall, R. C. , & Eickhoff, S. B. (2013). A quantitative meta‐analysis and review of motor learning in the human brain. NeuroImage, 67, 283–297. 10.1016/j.neuroimage.2012.11.020
    1. Hikosaka, O. , Nakahara, H. , Rand, M. K. , Sakai, K. , Lu, X. , Nakamura, K. , … Doya, K. (1999). Parallel neural networks for learning sequential procedures. Trends in Neurosciences, 22, 464–471. 10.1016/S0166-2236(99)01439-3
    1. Hikosaka, O. , Nakamura, K. , Sakai, K. , & Nakahara, H. (2002). Central mechanisms of motor skill learning. Current Opinion in Neurobiology, 12, 217–222. 10.1016/S0959-4388(02)00307-0
    1. Hund‐Georgiadis, M. , & von Cramon, D. Y. (1999). Motor‐learning‐related changes in piano players and non‐musicians revealed by functional magnetic‐resonance signals. Experimental Brain Research, 125, 417–425.
    1. Janacsek, K. , & Nemeth, D. (2013). Implicit sequence learning and working memory: Correlated or complicated? Cortex, 49, 2001–2006. 10.1016/j.cortex.2013.02.012
    1. Japikse, K. , Negash, S. , Howard, J. , & Howard, D. (2003). Intermanual transfer of procedural learning after extended practice of probabilistic sequences. Experimental Brain Research, 148, 38–49. 10.1007/s00221-002-1264-9
    1. Jenkins, I. H. , Brooks, D. J. , Nixon, P. D. , Frackowiak, R. S. , & Passingham, R. E. (1994). Motor sequence learning: A study with positron emission tomography. The Journal of Neuroscience, 14, 3775–3790. 10.1523/JNEUROSCI.14-06-03775.1994
    1. Johnson, L. , Burridge, J. H. , & Demain, S. H. (2013). Internal and external focus of attention during gait re‐education: An observational study of physical therapist practice in stroke rehabilitation. Physical Therapy, 93, 957–966. 10.2522/ptj.20120300
    1. Kal, E. , Houdijk, H. , Van Der Wurff, P. , Groet, E. , Van Bennekom, C. , Scherder, E. , & Van der Kamp, J. (2016). The inclination for conscious motor control after stroke: Validating the movement‐specific reinvestment scale for use in inpatient stroke patients. Disability and Rehabilitation, 38, 1097–1106. 10.3109/09638288.2015.1091858
    1. Kal, E. , Winters, M. , van der Kamp, J. , Houdijk, H. , Groet, E. , van Bennekom, C. , & Scherder, E. (2016). Is implicit motor learning preserved after stroke? A systematic review with meta‐analysis. PLoS One, 11, e0166376 10.1371/journal.pone.0166376
    1. Karni, A. , Meyer, G. , Jezzard, P. , Adams, M. M. , Turner, R. , & Ungerleider, L. G. (1995). Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature, 377, 155–158. 10.1038/377155a0
    1. Karni, A. , Meyer, G. , Rey‐Hipolito, C. , Jezzard, P. , Adams, M. M. , Turner, R. , & Ungerleider, L. G. (1998). The acquisition of skilled motor performance: Fast and slow experience‐driven changes in primary motor cortex. Proceedings of the National Academy of Sciences of the United States of America, 95, 861–868.
    1. Kleynen, M. , Braun, S. M. , Beurskens, A. J. H. M. , Verbunt, J. A. , de Bie, R. A. , & Masters, R. S. W. (2013). Investigating the Dutch movement‐specific reinvestment scale in people with stroke. Clinical Rehabilitation, 27, 160–165. 10.1177/0269215512448381
    1. Kleynen, M. , Braun, S. M. , Bleijlevens, M. H. , Lexis, M. A. , Rasquin, S. M. , Halfens, J. , … Masters, R. S. W. (2014). Using a Delphi technique to seek consensus regarding definitions, descriptions and classification of terms related to implicit and explicit forms of motor learning. PLoS One, 9, e100227 10.1371/journal.pone.0100227
    1. Kleynen, M. , Wilson, M. R. , Jie, L.‐J. , te Lintel Hekkert, F. , Goodwin, V. A. , & Braun, S. M. (2014). Exploring the utility of analogies in motor learning after stroke: A feasibility study. International Journal of Rehabilitation Research, 37, 277–280. 10.1097/MRR.0000000000000058
    1. Koechlin, E. , Basso, G. , Pietrini, P. , Panzer, S. , & Grafman, J. (1999). The role of the anterior prefrontal cortex in human cognition. Nature, 399, 148–151. 10.1038/20178
    1. Lehéricy, S. , Benali, H. , Van de Moortele, P.‐F. , Pélégrini‐Issac, M. , Waechter, T. , Ugurbil, K. , & Doyon, J. (2005). Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proceedings of the National Academy of Sciences of the United States of America, 102, 12566–12571. 10.1073/pnas.0502762102
    1. Lewis, P. A. , & Miall, R. C. (2003). Distinct systems for automatic and cognitively controlled time measurement: Evidence from neuroimaging. Current Opinion in Neurobiology, 13, 250–255. 10.1016/S0959-4388(03)00036-9
    1. Luppino, G. , Matelli, M. , Camarda, R. , & Rizzolatti, G. (1993). Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey. Journal of Comparative Neurology, 338, 114–140. 10.1002/cne.903380109
    1. Manoach, D. S. , Press, D. Z. , Thangaraj, V. , Searl, M. M. , Goff, D. C. , Halpern, E. , … Warach, S. (1999). Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI. Biological Psychiatry, 45, 1128–1137. 10.1016/S0006-3223(98)00318-7
    1. Meehan, S. K. , Randhawa, B. , Wessel, B. , & Boyd, L. A. (2011). Implicit sequence‐specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI study. Human Brain Mapping, 32, 290–303. 10.1002/hbm.21019
    1. Miall, C. (2010). Motor control: Correcting errors and learning from mistakes. Current Biology, 20, R596–R598. 10.1016/j.cub.2010.05.030
    1. Middleton, F. A. , & Strick, P. L. (2000). Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. Brain and Cognition, 42, 183–200. 10.1006/brcg.1999.1099
    1. Miller, G. A. (1994). The magical number seven, plus or minus two: Some limits on our capacity for processing information. Psychological Review, 101, 343–352.
    1. Miyachi, S. , Hikosaka, O. , Miyashita, K. , Kárádi, Z. , & Rand, M. K. (1997). Differential roles of monkey striatum in learning of sequential hand movement. Experimental Brain Research, 115, 1–5.
    1. Nakahara, H. , Doya, K. , & Hikosaka, O. (2001). Parallel cortico‐basal ganglia mechanisms for acquisition and execution of visuomotor sequences—A computational approach. Journal of Cognitive Neuroscience, 13, 626–647. 10.1162/089892901750363208
    1. Orrell, A. J. , Eves, F. F. , & Masters, R. S. (2006). Motor learning of a dynamic balancing task after stroke: Implicit implications for stroke rehabilitation. Physical Therapy, 86, 369–380. 10.1093/ptj/86.3.369
    1. Orrell, A. J. , Eves, F. F. , Masters, R. S. W. , & MacMahon, K. M. M. (2007). Implicit sequence learning processes after unilateral stroke. Neuropsychological Rehabilitation, 17, 335–354. 10.1080/09602010600832788
    1. Orrell, A. J. , Masters, R. S. W. , & Eves, F. F. (2009). Reinvestment and movement disruption following stroke. Neurorehabilitation and Neural Repair, 23, 177–183. 10.1177/1545968308317752
    1. Penhune, V. B. , & Steele, C. J. (2012). Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behavioural Brain Research, 226, 579–591. 10.1016/j.bbr.2011.09.044
    1. Pohl, P. S. , McDowd, J. M. , Filion, D. , Richards, L. G. , & Stiers, W. (2006). Implicit learning of a motor skill after mild and moderate stroke. Clinical Rehabilitation, 20, 246–253. 10.1191/0269215506cr916oa
    1. Pohl, P. S. , McDowd, J. M. , Filion, D. L. , Richards, L. G. , & Stiers, W. (2001). Implicit learning of a perceptual‐motor skill after stroke. Physical Therapy, 81, 1780–1789. 10.1093/ptj/81.11.1780
    1. Povel, D. J. , & Collard, R. (1982). Structural factors in patterned finger tapping. Acta Psychologica, 52, 107–123.
    1. Reber, A. (1993). Implicit learning and tacit knowledge: An essay on the cognitive unconscious (Oxford psychology series, no 19). Oxford: Oxford University Press.
    1. Reber, P. J. , & Squire, L. R. (1998). Encapsulation of implicit and explicit memory in sequence learning. Journal of Cognitive Neuroscience, 10, 248–263.
    1. Rosenbaum, D. A. , Kenny, S. B. , & Derr, M. A. (1983). Hierarchical control of rapid movement sequences. Journal of Experimental Psychology. Human Perception and Performance, 9, 86–102.
    1. Rösser, N. , Heuschmann, P. , Wersching, H. , Breitenstein, C. , Knecht, S. , & Flöel, A. (2008). Levodopa improves procedural motor learning in chronic stroke patients. Archives of Physical Medicine and Rehabilitation, 89, 1633–1641. 10.1016/j.apmr.2008.02.030
    1. Savion‐Lemieux, T. , & Penhune, V. B. (2005). The effects of practice and delay on motor skill learning and retention. Experimental Brain Research, 161, 423–431. 10.1007/s00221-004-2085-9
    1. Shadmehr, R. , Brandt, J. , & Corkin, S. (1998). Time‐dependent motor memory processes in amnesic subjects. Journal of Neurophysiology, 80, 1590–1597. 10.1152/jn.1998.80.3.1590
    1. Shin, J. C. , Aparicio, P. , & Ivry, R. B. (2005). Multidimensional sequence learning in patients with focal basal ganglia lesions. Brain and Cognition, Neuropsychology of Timing and Time Perception, 58, 75–83. 10.1016/j.bandc.2004.09.015
    1. Siengsukon, C. F. , & Boyd, L. A. (2009). Sleep to learn after stroke: Implicit and explicit off‐line motor learning. Neuroscience Letters, 451, 1–5. 10.1016/j.neulet.2008.12.040
    1. Stapleton, T. , Ashburn, A. , & Stack, E. (2001). A pilot study of attention deficits, balance control and falls in the subacute stage following stroke. Clinical Rehabilitation, 15, 437–444. 10.1191/026921501678310243
    1. Tanji, J. (1994). The supplementary motor area in the cerebral cortex. Neuroscience Research, 19, 251–268. 10.1016/0168-0102(94)90038-8
    1. Vakil, E. , Kahan, S. , Huberman, M. , & Osimani, A. (2000). Motor and non‐motor sequence learning in patients with basal ganglia lesions: The case of serial reaction time (SRT). Neuropsychologia, 38, 1–10. 10.1016/S0028-3932(99)00058-5
    1. Wadden, K. P. , De Asis, K. , Mang, C. S. , Neva, J. L. , Peters, S. , Lakhani, B. , & Boyd, L. A. (2017). Predicting motor sequence learning in individuals with chronic stroke. Neurorehabilitation and Neural Repair, 31, 95–104. 10.1177/1545968316662526
    1. Wadden, K. P. , Woodward, T. S. , Metzak, P. D. , Lavigne, K. M. , Lakhani, B. , Auriat, A. M. , & Boyd, L. A. (2015). Compensatory motor network connectivity is associated with motor sequence learning after subcortical stroke. Behavioural Brain Research, 286, 136–145. 10.1016/j.bbr.2015.02.054
    1. Willingham, D. B. (1998). A neuropsychological theory of motor skill learning. Psychological Review, 105, 558–584.
    1. Willingham, D. B. , Greenberg, A. R. , & Thomas, R. C. (1997). Response‐to‐stimulus interval does not affect implicit motor sequence learning, but does affect performance. Memory and Cognition, 25, 534–542. 10.3758/BF03201128
    1. Wu, T. , Kansaku, K. , & Hallett, M. (2004). How self‐initiated memorized movements become automatic: A functional MRI study. Journal of Neurophysiology, 91, 1690–1698. 10.1152/jn.01052.2003
    1. Zimerman, M. , Heise, K. F. , Hoppe, J. , Cohen, L. G. , Gerloff, C. , & Hummel, F. C. (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, 2185–2191. 10.1161/STROKEAHA.111.645382

Source: PubMed

3
Suscribir