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

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.

[1]  Á. Pascual-Leone,et al.  Prefrontal lesions impair the implicit and explicit learning of sequences on visuomotor tasks , 2002, Experimental Brain Research.

[2]  L. Squire,et al.  Encapsulation of Implicit and Explicit Memory in Sequence Learning , 1998, Journal of Cognitive Neuroscience.

[3]  Daniel B. Willingham,et al.  A Neuropsychological Theory of Motor Skill Learning , 2004 .

[4]  Bimal Lakhani,et al.  Predicting Motor Sequence Learning in Individuals With Chronic Stroke , 2017, Neurorehabilitation and neural repair.

[5]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Rothwell,et al.  Explicit motor sequence learning with the paretic arm after stroke , 2018, Disability and rehabilitation.

[7]  Daniel B. Willingham,et al.  Response-to-stimulus interval does not affect implicit motor sequence learning, but does affect performance , 1997, Memory & cognition.

[8]  D. V. von Cramon,et al.  Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals , 1999, Experimental Brain Research.

[9]  Leslie G. Ungerleider,et al.  Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning , 2009, Experimental Brain Research.

[10]  N. Censor,et al.  Generalization of perceptual and motor learning: A causal link with memory encoding and consolidation? , 2013, Neuroscience.

[11]  Investigating the Dutch Movement-Specific Reinvestment Scale in people with stroke , 2013, Clinical rehabilitation.

[12]  P. Strick,et al.  Basal Ganglia Output and Cognition: Evidence from Anatomical, Behavioral, and Clinical Studies , 2000, Brain and Cognition.

[13]  John W Krakauer,et al.  Learning of a sequential motor skill comprises explicit and implicit components that consolidate differently. , 2009, Journal of neurophysiology.

[14]  Mikhail Rabinovich,et al.  Learning of Chunking Sequences in Cognition and Behavior , 2015, PLoS Comput. Biol..

[15]  D. Filion,et al.  Implicit learning of a motor skill after mild and moderate stroke , 2006, Clinical rehabilitation.

[16]  Richard B. Ivry,et al.  Multidimensional sequence learning in patients with focal basal ganglia lesions , 2005, Brain and Cognition.

[17]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[18]  D A Rosenbaum,et al.  Hierarchical control of rapid movement sequences. , 1983, Journal of experimental psychology. Human perception and performance.

[19]  E. Scherder,et al.  Is Implicit Motor Learning Preserved after Stroke? A Systematic Review with Meta-Analysis , 2016, PloS one.

[20]  Exploring the utility of analogies in motor learning after stroke: a feasibility study , 2014, International journal of rehabilitation research. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation.

[21]  M. Desseilles,et al.  Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory , 2008, Neuron.

[22]  Jordan Grafman,et al.  Procedural learning is impaired in patients with prefrontal lesions , 1999, Neurology.

[23]  Dov Sagi,et al.  Common mechanisms of human perceptual and motor learning , 2012, Nature Reviews Neuroscience.

[24]  M. Hallett,et al.  How self-initiated memorized movements become automatic: a functional MRI study. , 2004, Journal of neurophysiology.

[25]  Carolee J Winstein,et al.  Providing explicit information disrupts implicit motor learning after basal ganglia stroke. , 2004, Learning & memory.

[26]  Carolee J Winstein,et al.  Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. , 2003, Physical therapy.

[27]  J. Edwards,et al.  Motor sequence chunking is impaired by basal ganglia stroke , 2009, Neurobiology of Learning and Memory.

[28]  Christian Nasel,et al.  Perceptual Sequence Learning Is More Severely Impaired than Motor Sequence Learning in Patients with Chronic Cerebellar Stroke , 2013, Journal of Cognitive Neuroscience.

[29]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[30]  J. Diedrichsen,et al.  Motor skill learning between selection and execution , 2015, Trends in Cognitive Sciences.

[31]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[32]  Katie M. Lavigne,et al.  Compensatory motor network connectivity is associated with motor sequence learning after subcortical stroke , 2015, Behavioural Brain Research.

[33]  D J Povel,et al.  Structural factors in patterned finger tapping. , 1982, Acta psychologica.

[34]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[35]  J. Burridge,et al.  Internal and External Focus of Attention During Gait Re-Education: An Observational Study of Physical Therapist Practice in Stroke Rehabilitation , 2013, Physical Therapy.

[36]  A Ashburn,et al.  A pilot study of attention deficits, balance control and falls in the subacute stage following stroke , 2001, Clinical rehabilitation.

[37]  Gereon R. Fink,et al.  Timing Matters? Learning of Complex Spatiotemporal Sequences in Left-hemisphere Stroke Patients , 2016, Journal of Cognitive Neuroscience.

[38]  A. C. Roberts,et al.  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 , 1998, Journal of Cognitive Neuroscience.

[39]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[40]  Catherine Sackley,et al.  Use of information feedback and attentional focus of feedback in treating the person with a hemiplegic arm. , 2009, Physiotherapy research international : the journal for researchers and clinicians in physical therapy.

[41]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[42]  Steven Warach,et al.  Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI , 1999, Biological Psychiatry.

[43]  A. Bastian.  Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[44]  R Shadmehr,et al.  Time-dependent motor memory processes in amnesic subjects. , 1998, Journal of neurophysiology.

[45]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[46]  Habib Benali,et al.  Off-line consolidation of motor sequence learning results in greater integration within a cortico-striatal functional network , 2014, NeuroImage.

[47]  R. Masters,et al.  Motor learning of a dynamic balancing task after stroke: implicit implications for stroke rehabilitation. , 2006, Physical therapy.

[48]  Christian Gerloff,et al.  Modulation of Training by Single-Session Transcranial Direct Current Stimulation to the Intact Motor Cortex Enhances Motor Skill Acquisition of the Paretic Hand , 2012, Stroke.

[49]  Mark R. Wilson,et al.  Using a Delphi Technique to Seek Consensus Regarding Definitions, Descriptions and Classification of Terms Related to Implicit and Explicit Forms of Motor Learning , 2014, PloS one.

[50]  Leslie G. Ungerleider,et al.  Brain plasticity related to the consolidation of motor sequence learning and motor adaptation , 2010, Proceedings of the National Academy of Sciences.

[51]  L. Boyd,et al.  Implicit sequence‐specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI Study , 2011, Human brain mapping.

[52]  R. Masters,et al.  Reinvestment and Movement Disruption Following Stroke , 2009, Neurorehabilitation and neural repair.

[53]  Bernard J. Baars,et al.  Cognition, brain, and consciousness , 2007 .

[54]  Dottie M. Clower,et al.  Basal ganglia and cerebellar inputs to 'AIP'. , 2005, Cerebral cortex.

[55]  R. Masters,et al.  Implicit sequence learning processes after unilateral stroke , 2007, Neuropsychological rehabilitation.

[56]  J. Doyon.  Motor sequence learning and movement disorders , 2008, Current opinion in neurology.

[57]  G. A. Miller.  THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[58]  Tal Savion-Lemieux,et al.  The effects of practice and delay on motor skill learning and retention , 2005, Experimental Brain Research.

[59]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[60]  A. Gordon,et al.  Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements , 1998, Experimental Brain Research.

[61]  P. Heuschmann,et al.  Levodopa improves procedural motor learning in chronic stroke patients. , 2008, Archives of physical medicine and rehabilitation.

[62]  P. Weiss,et al.  Timing independent spatial motor sequence learning is preserved in left hemisphere stroke , 2017, Neuropsychologia.

[63]  Lara A. Boyd,et al.  Learning Implicitly: Effects of Task and Severity After Stroke , 2007, Neurorehabilitation and neural repair.

[64]  Lara A. Boyd,et al.  Implicit motor-sequence learning in humans following unilateral stroke: the impact of practice and explicit knowledge , 2001, Neuroscience Letters.

[65]  James H. Howard,et al.  Intermanual transfer of procedural learning after extended practice of probabilistic sequences , 2002, Experimental Brain Research.

[66]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[67]  K. Doya.  Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[68]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  C. Miall.  Motor Control: Correcting Errors and Learning from Mistakes , 2010, Current Biology.

[70]  The inclination for conscious motor control after stroke: validating the Movement-Specific Reinvestment Scale for use in inpatient stroke patients , 2016, Disability and rehabilitation.

[71]  G. Weniger,et al.  Implicit and explicit memory after focal thalamic lesions , 2001, Neurology.

[72]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[73]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[74]  E. Vakil,et al.  Motor and non-motor sequence learning in patients with basal ganglia lesions: the case of serial reaction time (SRT) , 2000, Neuropsychologia.

[75]  J. García-Moncó,et al.  Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions , 2008, Clinical Neurology and Neurosurgery.

[76]  J. Sanes,et al.  Human brain activation accompanying explicitly directed movement sequence learning , 2001, Experimental Brain Research.

[77]  J. Tanji.  The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[78]  Karolina Janacsek,et al.  Implicit sequence learning and working memory: Correlated or complicated? , 2013, Cortex.

[79]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[80]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[81]  D. Filion,et al.  Implicit learning of a perceptual-motor skill after stroke. , 2001, Physical therapy.

[82]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[83]  Hormone Secretion.  COMMON MECHANISMS OF , 1977 .

[84]  K. Doya,et al.  Parallel Cortico-Basal Ganglia Mechanisms for Acquisition and Execution of Visuomotor SequencesA Computational Approach , 2001, Journal of Cognitive Neuroscience.

[85]  L. Boyd,et al.  Sleep to learn after stroke: Implicit and explicit off-line motor learning , 2009, Neuroscience Letters.

[86]  V. Penhune,et al.  Author's Personal Copy Behavioural Brain Research Parallel Contributions of Cerebellar, Striatal and M1 Mechanisms to Motor Sequence Learning , 2022 .