Imaging Brain Plasticity during Motor Skill Learning

doi:10.1006/nlme.2002.4091

Neurobiology of Learning and Memory

Volume 78, Issue 3, November 2002, Pages 553-564

https://doi.org/10.1006/nlme.2002.4091 Get rights and content

Abstract

The search for the neural substrates mediating the incremental acquisition of skilled motor behaviors has been the focus of a large body of animal and human studies in the past decade. Much less is known, however, with regard to the dynamic neural changes that occur in the motor system during the different phases of learning. In this paper, we review recent findings, mainly from our own work using fMRI, which suggest that: (i) the learning of sequential finger movements produces a slowly evolving reorganization within primary motor cortex (M1) over the course of weeks and (ii) this change in M1 follows more dynamic, rapid changes in the cerebellum, striatum, and other motor-related cortical areas over the course of days. We also briefly review neurophysiological and psychophysical evidence for the consolidation of motor skills, and we propose a working hypothesis of its underlying neural substrate in motor sequence learning.

References (37)

J.P. Donoghue
Plasticity of adult sensorimotor representations
Current Opinion in Neurobiology
(1995)
J. Doyon
Skill learning
J. Doyon et al.
Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence
Brain and Cognition
(1997)
W.T. Greenough et al.
Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex
Behavioral and Neural Biology
(1985)
A. Karni
The acquisition of perceptual and motor skills: A memory system in the adult human cortex
Cognitive Brain Research
(1996)
J.A. Kleim et al.
Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex
Neurobiological Learning and Memory
(2002)
M.M. Merzenich et al.
Cortical plasticity and memory
Current Opinion in Neurobiology
(1993)
F.A. Middleton et al.
Cerebellar output channels
International Review of Neurobiology
(1997)
R.J. Nudo et al.
Adaptive plasticity in primate motor cortex as a consequence of behavioral experience and neuronal injury
Seminars in Neuroscience
(1997)
G.S. Withers et al.
Reach training selectively alters dendritic branching in subpopulations of layer II–III pyramids in rat motor-somatosensory forelimb cortex
Neuropsychologia
(1989)

T. Brashers-Krug et al.

Consolidation in human motor memory

Nature

(1996)

J. Classen et al.

Rapid plasticity of human cortical movement representation induced by practice

Journal of Neurophysiology

(1998)

J.P. Donoghue et al.

Motor cortical substrates and mechanisms for learning

J. Doyon et al.

Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography

European Journal of Neuroscience

(1996)

J. Doyon et al.

Functional anatomy of motor skill learning

A.M. Gordon et al.

Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements

Experimental Brain Research

(1998)

S.T. Grafton et al.

Functional imaging of procedural motor learning: Relating cerebral blood flow with individual subject performance

Human Brain Mapping

(1994)

G. Hess et al.

Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex

Journal of Neurophysiology

(1996)

Cited by (467)

Gamification and neurological motor rehabilitation in children and adolescents: A systematic review
2024, Neurologia
La ludificación consiste en emplear el juego en contextos no lúdicos. Su uso en la rehabilitación motora de patologías neurológicas está muy extendido, pero sobre todo en pacientes adultos. El objetivo de esta revisión fue describir el uso de la ludificación en los tratamientos de rehabilitación en niños y adolescentes con afectación neuromotora.
Se realizó una revisión sistemática de ensayos clínicos en diferentes bases de datos: Medline (a través de Pubmed), Scielo, SCOPUS, Dialnet, Cinahl y PEDro de la literatura científica publicada hasta la fecha siguiendo el protocolo PRISMA. La calidad metodológica de los estudios identificados se evaluó a través de la escala PEDro.
De un total de 469 estudios localizados se seleccionaron 10 ensayos clínicos que cumplieron los criterios de inclusión. Se analizaron los sistemas de ludificación utilizados como parte del tratamiento rehabilitador en distintas afecciones neuromotoras en niños y adolescentes. La parálisis cerebral fue la afección con mayor número de estudios (n = 6), seguida del trastorno del desarrollo de la coordinación (n = 3). También se estudió la alteración del equilibrio y coordinación por causa neurológica (n = 1).
El uso de la ludificación en rehabilitación aporta beneficios al tratamiento convencional de las alteraciones neuromotoras en niños y adolescentes, siendo el incremento de la motivación y de la adherencia terapéutica los que mayor consenso han alcanzado entre autores. Fuerza, equilibrio, funcionalidad y coordinación son otras variables analizadas que, si bien sugieren mejoras, necesitarían futuras investigaciones para determinar una óptima dosificación.
Gamification consists of the use of games in non-playful contexts. It is widely employed in the motor rehabilitation of neurological diseases, but mainly in adult patients. The objective of this review was to describe the use of gamification in the rehabilitation of children and adolescents with neuromotor impairment.
We performed a systematic review of clinical trials published to date on the MEDLINE (PubMed), Scielo, SCOPUS, Dialnet, CINAHL, and PEDro databases, following the PRISMA protocol. The methodological quality of the studies identified was assessed using the PEDro scale.
From a total of 469 studies, 10 clinical trials met the inclusion criteria. We analysed the gamification systems used as part of the rehabilitation treatment of different neuromotor conditions in children and adolescents. Cerebral palsy was the most frequently studied condition (6 studies), followed by developmental coordination disorder (3), and neurological impairment of balance and coordination (1).
The use of gamification in rehabilitation is helpful in the conventional treatment of neuromotor disorders in children and adolescents, with increased motivation and therapeutic adherence being the benefits with the greatest consensus among authors. While strength, balance, functional status, and coordination also appear to improve, future research should aim to determine an optimal dosage.
Microstructural dynamics of motor learning and sleep-dependent consolidation: A diffusion imaging study
2023, iScience
Memory consolidation can benefit from post-learning sleep, eventually leading to long-term microstructural brain modifications to accommodate new memory representations. Non-invasive diffusion-weighted magnetic resonance imaging (DWI) allows the observation of (micro)structural brain remodeling after time-limited motor learning. Here, we combine conventional diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) that allows modeling dendritic and axonal complexity in gray matter to investigate with improved specificity the microstructural brain mechanisms underlying time- and sleep-dependent motor memory consolidation dynamics. Sixty-one young healthy adults underwent four DWI sessions, two sequential motor trainings, and a night of total sleep deprivation or regular sleep distributed over five days. We observed rapid-motor-learning-related remodeling in occipitoparietal, temporal, and motor-related subcortical regions, reflecting temporary dynamics in learning-related neuronal brain plasticity processes. Sleep-related consolidation seems not to exert a detectable impact on diffusion parameters, at least on the timescale of a few days.
Long-term kinesthetic motor imagery practice with a BCI: Impacts on user experience, motor cortex oscillations and BCI performances
2023, Computers in Human Behavior
Kinesthetic motor imagery (KMI) generates specific brain patterns in sensorimotor rhythm over the motor cortex (called event-related (de)-synchronization, ERD/ERS), allowing KMI to be detected by a Brain-Computer Interface (BCI) through electroencephalographic (EEG) signal. Because performing a KMI task stimulates synaptic plasticity, KMI-based BCIs hold promise for many applications requiring long-term KMI practice (e.g., sports training or post-stroke rehabilitation). However, there is a lack of studies on the long-term KMI-based BCI interactions, especially regarding the relationship between intrapersonal factors and motor pattern variations. This pilot study aims to understand better (i) how brain motor patterns change over time for a given individual, (ii) whether intrapersonal factors might influence BCI practice, and (iii) how the brain motor patterns underlying the KMI task (i.e., ERDs and ERSs) are modulated over time by the BCI user’s experience. To this end, we recruited an expert in this mental task who performed over 2080 KMIs in 26 different sessions over a period of five months. The originality of this study lies in the detailed examination of cross-referenced data from EEG signals, BCI data performance, and 13 different surveys. The results show that this repetitive and prolonged practice did not diminish his well-being and, in particular, generated a sense of automatization of the task. We observed a progressive attenuation of the ERD amplitude and a concentration in the motor areas as the sessions accumulated. All these elements point to a phenomenon of neural efficiency. If confirmed by other studies, this phenomenon could call into question the quality of the BCI in providing continuous stimulation to the user. In addition, the results of this pilot study provide insights into what might influence the response of the motor cortex (e.g. emotions, task control, diet, etc.) and promising opportunities for improving the instructional design of BCIs intended for long-term use.
Effects of Prefrontal Transcranial Direct Current Stimulation on Retention of Performance Gains on an Obstacle Negotiation Task in Older Adults
2023, Neuromodulation
Complex walking in older adults can be improved with task practice and might be further enhanced by pairing transcranial direct current stimulation (tDCS) to the dorsolateral prefrontal cortex. We tested the hypothesis that a single session of practice of a complex obstacle negotiation task paired with active tDCS in older adults would produce greater within-session improvements in walking performance and retention of gains, compared to sham tDCS and no tDCS conditions.
A total of 50 older adults (mean age = 74.46 years ± 6.49) with self-reported walking difficulty were randomized to receive either active tDCS (active-tDCS group) or sham tDCS (sham-tDCS group) bilaterally to the dorsolateral prefrontal cortex or no tDCS (no-tDCS group). Each group performed ten practice trials of an obstacle negotiation task at their fastest safe speed. Retention of gains in walking performance was assessed with three trials conducted one week later. Within-session effects of practice and between-session retention effects on obstacle negotiation speed were examined.
At the practice session, all three groups exhibited significant within-session gains in walking speed (p ≤ 0.005). However, the gains were significantly greater in the sham-tDCS group than in the active-tDCS and no-tDCS groups (p ≤ 0.03) and were comparable between the active-tDCS and no-tDCS groups (p = 0.89). At one-week follow-up, the active-tDCS group exhibited significant between-session retention of gains and continued “offline” improvement in walking speed (p = 0.005). The active-tDCS group showed significantly greater retention of gains than the no-tDCS (p = 0.02) but not the sham-tDCS group (p = 0.24).
Pairing prefrontal active tDCS with a single session of obstacle negotiation practice may enhance one-week retention of gains in walking performance compared to no tDCS. However, the evidence is insufficient to suggest a benefit of active tDCS over sham tDCS for enhancing the gains in walking performance. Additional studies with a multisession intervention design and larger sample size are needed to further investigate these findings.
The Clinicaltrials.gov registration number for the study is NCT03122236.
Explicit benefits: Motor sequence acquisition and short-term retention in adults who do and do not stutter
2023, Journal of Fluency Disorders
Motor sequencing skills have been found to distinguish individuals who experience developmental stuttering from those who do not stutter, with these differences extending to non-verbal sequencing behaviour. Previous research has focused on measures of reaction time and practice under externally cued conditions to decipher the motor learning abilities of persons who stutter. Without the confounds of extraneous demands and sensorimotor processing, we investigated motor sequence learning under conditions of explicit awareness and focused practice among adults with persistent development stuttering. Across two consecutive practice sessions, 18 adults who stutter (AWS) and 18 adults who do not stutter (ANS) performed the finger-to-thumb opposition sequencing (FOS) task. Both groups demonstrated significant within-session performance improvements, as evidenced by fast on-line learning of finger sequences on day one. Additionally, neither participant group showed deterioration of their learning gains the following day, indicating a relative stabilization of finger sequencing performance during the off-line period. These findings suggest that under explicit and focused conditions, early motor learning gains and their short-term retention do not differ between AWS and ANS. Additional factors influencing motor sequencing performance, such as task complexity and saturation of learning, are also considered. Further research into explicit motor learning and its generalization following extended practice and follow-up in persons who stutter is warranted. The potential benefits of motor practice generalizability among individuals who stutter and its relevance to supporting treatment outcomes are suggested as future areas of investigation.
Exploring the mechanisms of target acquisition performance in esports: The role of component kinematic phases on a first person shooter motor skill.
2023, Computers in Human Behavior
When quantifying elements of performance in bimanual tasks, such as surgery or sports, it is important to understand the errors that participants make to facilitate skill improvement. Esports lags behind when quantifying the motor skills that differentiate elites and amateurs. The purpose of this study was to leverage a large existing kinematic dataset to identify whether previously observed differences in end point performance among gamers of varying expertise, across training days within expertise groups and between stimulation conditions resulted from differences in performance during specific phases of target acquisition movements. Specifically, we evaluated the position and velocity of cursor movements to show for the first time the differences in the component phases of target acquisition movements among first person shooter gamers of various expertise and non-gamers. We also established the dose-response of these components to deliberate practice and the effect of neurostimulation on the improvement of these components in each expertise group. Overall, gamers of higher expertise show evidence of superior motor planning and sensory-motor integration and that these qualities can be improved with training. Future work should more closely examine the sub-movements and classify biomechanical movement strategies of target acquisition skills among gamers.

View all citing articles on Scopus

^☆: We thank our collaborators, M. M Adams, P. Jezzard, F. Lalonde, G. Meyer, C. Rey-Hipolito, A. W. Song, and R. Turner. We also thank E. Gutierrez for technical assistance in preparing the manuscript. Some of the material included in this paper appears in A. Karni et al., 1998, Proceedings of the National Academy of Sciences of the United States of America, 95, 861–868, and in J. Doyon and L. G. Ungerleider, 2002, Neuropsychology of memory, 3rd ed., L. R. Squire and D. L Schacter (Eds.), Guilford Press, New York. This work was supported, in part, by grants from the Natural Sciences and Engineering Research Council of Canada and the Canadian Institutes of Health Research to J. D. and through funding from the NIMH-IRP to L.G.U.

^f2: Address correspondence and reprint requests to Leslie G. Ungerleider, Laboratory of Brain and Cognition, National Institute of Mental Health, 10 Center Drive, Building 10, Room 4C104, Bethesda, MD 20892-1366. Fax: (301) 402-0921. E-mail: [email protected].

View full text

Special Issue ArticleImaging Brain Plasticity during Motor Skill Learning☆

Abstract

Current Opinion in Neurobiology

Brain and Cognition

Behavioral and Neural Biology

Cognitive Brain Research

Neurobiological Learning and Memory

Current Opinion in Neurobiology

International Review of Neurobiology

Seminars in Neuroscience

Neuropsychologia

Consolidation in human motor memory

Nature

Rapid plasticity of human cortical movement representation induced by practice

Journal of Neurophysiology

Motor cortical substrates and mechanisms for learning

Functional anatomy of visuomotor skill learning in human subjects examined with positron emission tomography

European Journal of Neuroscience

Functional anatomy of motor skill learning

Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements

Experimental Brain Research

Functional imaging of procedural motor learning: Relating cerebral blood flow with individual subject performance

Human Brain Mapping

Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex

Journal of Neurophysiology

Special Issue Article
Imaging Brain Plasticity during Motor Skill Learning☆