Components Of Motor Learning Research Articles

Repeated Concussions Impair Behavioral and Neurophysiological Changes in the Motor Learning System

Background. Concussions affect nearly 3 million people a year and are the leading cause of traumatic brain injury–related emergency department visits among youth. Evidence shows neuromotor regions are sensitive to concussive events and that motor symptoms may be the earliest clinical manifestations of neurodegenerative traumatic brain injuries. However, little is known about the effects repeated concussions play on motor learning. Namely, how does concussion acuity (time since injury) affect different behavioral and neurophysiological components of motor learning? Methods. Using a 3-pronged approach, we assessed (1) behavioral measures of motor learning, (2) neurophysiological measures underlying retention of motor learning known as occlusion, and (3) quantitative survey data capturing affective symptoms of each participant. Collegiate student athletes were stratified across 3 groups depending on their concussion history: (1) NonCon, no history of concussion; (2) Chronic, chronic-state of concussion (>1 year postinjury), or (3) Acute, acute state of concussion (<2 weeks postinjury). Results. We found that athletes in both the acute and chronic state of injury following a concussion had impaired retention and aberrant occlusion in motor skill learning as compared with athletes with no history of concussion. Moreover, higher numbers of previous concussions (regardless of the time since injury) correlated with more severe behavioral and neurophysiological motor impairments by specifically hindering neurophysiological mechanisms of learning to affect behavior. Conclusions. These results indicate the presence of motor learning impairment that is evident within 2 weeks postinjury. Our findings have significant implications for the prognosis of concussion and emphasize the need for prevention, but can also direct more relevant rehabilitation treatment targets.

Consolidation and retention of motor skill after motor imagery training

Complex motor tasks are learned through training which results in lasting improvement in sensorimotor performance and accuracy. Learning a motor skill is commonly attained via physical execution. However, research has shown that cognitive training, such as motor imagery (MI), effectively facilitates skill learning. Neurophysiological findings suggest that learning-induced plasticity in the human motor cortex, subserving consolidation and retention of motor skills, is stronger after movement execution (ME) than after MI training. Here, we designed an experimental task able to test for the fast and slow learning phases and for retention of motor skills for both MI and ME. We hypothesize that differences between MI and ME training would emerge in terms of reduced consolidation and retention of motor skills. Twenty-four young healthy subjects were divided into two groups, performing MI or ME training. Participants wore sensor-engineered gloves and their sensorimotor performance was assessed over a period of 15 days with 4-days training. We analysed the touch duration (TD), the inter-tapping interval (ITI), movement rate and accuracy. Results showed that (i) during the first phase of acquisition of motor skills, sensorimotor performance improved similarly in MI and ME groups; (ii) during the second learning phase movement rate increased more in ME than MI group and this difference was mainly driven by differences in the duration of TD; (iii) consolidation deficits with MI training reflected in impaired retention of the acquired skills, as TD and ITI were larger and movement rate was lower in the MI group with respect to the ME, till to 10 days after the last training session. Explicit component of motor learning, accuracy, was maintained in retention phase in both groups. Following our hypothesis, our findings show that MI training is as effective as ME within the first learning phase, but consolidation and retention of motor skills are less effective following MI training. This study highlights MI limitations and suggests option to enhance MI, as by providing an external sensory feedback.

Nearest neighbours reveal fast and slow components of motor learning.

Changes in behavior, due to environmental influences, development, and learning1–5, are commonly quantified based on a few hand-picked, domain-specific, features2–4,6,7 (e.g. the average pitch of acoustic vocalizations3) and assuming discrete classes of behaviors (e.g. distinct vocal syllables)2,3,8–10. Such methods generalize poorly across different behaviors and model systems and may miss important components of change. Here we present a more general account of behavioral change based on nearest-neighbor statistics11–13 and apply it to song development in a songbird, the zebra finch3. First, we introduce “repertoire dating”, whereby each rendition of a behavior (e.g. each vocalization) is assigned a repertoire time, reflecting when similar renditions were typical in the behavioral repertoire. Repertoire time (rT) isolates the components of vocal variability congruent with the long-term changes due to vocal learning and development and stratifies the behavioral repertoire into regressions (rT < true production time, t), anticipations (rT > t), and typical renditions (rT ≈ t). Second, we obtain a holistic, yet low-dimensional14, description of vocal change in terms of a stratified “behavioral trajectory”, revealing multiple, previously unrecognized, components of behavioral change on fast and slow timescales, as well as distinct patterns of overnight consolidation1,2,4,15,16. Diurnal changes in regressions undergo only weak consolidation, whereas anticipations and typical renditions consolidate fully. Because of its generality, our non-parametric description of how behavior evolves relative to itself, rather than relative to a potentially arbitrary, experimenter-defined, goal2,3,15,17 appears well-suited to compare learning and change across behaviors and species18,19, as well as biological and artificial systems5.

A rapid visuomotor response on the human upper limb is selectively influenced by implicit motor learning.

How do humans learn to adapt their motor actions to achieve task success? Recent behavioral and patient studies have challenged the classic notion that motor learning arises solely from the errors produced during a task, suggesting instead that explicit cognitive strategies can act in concert with the implicit, error-based, motor learning component. In this study, we show that the earliest wave of directionally tuned neuromuscular activity that begins within ~100 ms of peripheral visual stimulus onset is selectively influenced by the implicit component of motor learning. In contrast, the voluntary neuromuscular activity associated with reach initiation, which evolves ~100-200 ms later, is influenced by both the implicit and explicit components of motor learning. The selective influence of the implicit, but not explicit, component of motor learning on the directional tuning of the earliest cascade of neuromuscular activity supports the notion that these components of motor learning can differentially influence descending motor pathways. NEW & NOTEWORTHY Motor learning can be driven both by an implicit error-based component and an explicit strategic component, but the influence of these components on the descending pathways that contribute to motor control is unknown. In this study, we show that the implicit component selectively influences a reflexive circuit that rapidly generates a visuomotor response on the human upper limb. Our results show that the substrates mediating implicit and explicit motor learning exert distinct influences on descending motor pathways.

Multiple components in direction learning in smooth pursuit eye movements of monkeys.

We analyzed behavioral features of smooth pursuit eye movements to characterize the course of acquisition and expression of multiple neural components of motor learning. Monkeys tracked a target that began to move in an initial "pursuit" direction and suddenly, but predictably, changed direction after a fixed interval of 250 ms. As the trial is repeated, monkeys learn to make eye movements that predict the change in target direction. Quantitative analysis of the learned response revealed evidence for multiple, dynamic, parallel processes at work during learning. 1) The overall learning followed at least two trial courses: a fast component grew and saturated rapidly over tens of trials, and a slow component grew steadily over up to 1,000 trials. 2) The temporal specificity of the learned response within each trial was crude during the first 100 trials but then improved gradually over the remaining trials. 3) External influences on the gain of pursuit initiation modulate the expression but probably not the acquisition of learning. The gain of pursuit initiation and the expression of the learned response decreased in parallel, both gradually through a 1,000-trial learning block and immediately between learning trials with different gains in the initiation of pursuit. We conclude that at least two distinct neural mechanisms drive the acquisition of pursuit learning over 100 to 1,000 trials (3 to 30 min). Both mechanisms generate underlying memory traces that are modulated in relation to the gain of pursuit initiation before expression in the final motor output. NEW & NOTEWORTHY We show that cerebellum-dependent direction learning in smooth pursuit eye movements grows in at least two components over 1,100 behavioral learning repetitions. One component grows over tens of trials and the other over hundreds. Within trials, learned temporal specificity gradually improves over hundreds of trials. The expression of each learning component on a given trial can be modified by external factors that do not affect the underlying memory trace.

Aproximación teórica de la intervención de Fisioterapia en neurorehbilitación desde el aprendizaje motor en pacientes con evento cerebrovascular

Introducción: Los eventos cerebrovasculares (ECV) han ido adquiriendo una relevancia creciente tanto en países desarrollados como subdesarrollados, puesto que, comparado con otras patologías, éste se encuentra en el cuarto lugar a nivel mundial como una de las enfermedades que afecta el sistema nervioso central, llegando a afectar la calidad de vida del ser humano. El objetivo de este artículo es examinar la producción científica con respecto a la intervención de la Fisioterapia en esta área de la salud desde el aprendizaje motor en pacientes con ECV. Método: Se realizó una revisión de la literatura existente en diferentes bases de datos, el análisis del contenido de los documentos recuperados se realizó mediante un matriz con aquellos que cumplían con el criterio de intervención de la fisioterapia en la Neurorehabilitación (propósito, planeación y ejecución) tanto en miembros superiores como inferiores centrándose en lesiones de arteria cerebral media. Resultados: Se encuentran evidencias de las diferentes intervenciones como son los componentes de aprendizaje motor implícito, explícito, retroalimentación, sistema sensorial, perceptivo y realidad virtual con enfoques neurocognitivos, esto a nivel mundial; y en Colombia se encuentran artículos de revisiones sistemática publicadas entre los años 2013-2016 con temáticas generales pero que muestran exploraciones sobre el propósito, la planeación como componentes del aprendizaje motor en personas con eventos cerebrovasculares. Conclusiones: A pesar de la evidencia encontrada es pertinente, el desarrollo de investigación en cuanto al propósito y planeación de intervenciones para este tipo de población.

Flexible explicit but rigid implicit learning in a visuomotor adaptation task.

There is mounting evidence for the idea that performance in a visuomotor rotation task can be supported by both implicit and explicit forms of learning. The implicit component of learning has been well characterized in previous experiments and is thought to arise from the adaptation of an internal model driven by sensorimotor prediction errors. However, the role of explicit learning is less clear, and previous investigations aimed at characterizing the explicit component have relied on indirect measures such as dual-task manipulations, posttests, and descriptive computational models. To address this problem, we developed a new method for directly assaying explicit learning by having participants verbally report their intended aiming direction on each trial. While our previous research employing this method has demonstrated the possibility of measuring explicit learning over the course of training, it was only tested over a limited scope of manipulations common to visuomotor rotation tasks. In the present study, we sought to better characterize explicit and implicit learning over a wider range of task conditions. We tested how explicit and implicit learning change as a function of the specific visual landmarks used to probe explicit learning, the number of training targets, and the size of the rotation. We found that explicit learning was remarkably flexible, responding appropriately to task demands. In contrast, implicit learning was strikingly rigid, with each task condition producing a similar degree of implicit learning. These results suggest that explicit learning is a fundamental component of motor learning and has been overlooked or conflated in previous visuomotor tasks.

Early response markers from video games for rehabilitation strategies

Stroke commonly leads to partial or complete paralysis of one side of the body and there is limited availability of therapists to provide rehabilitation. It is a priority therefore to identify the most effective rehabilitation strategies and/or pharmacotherapies. Motor learning, the essential process underpinning rehabilitation, can be assessed more quickly and robustly than outcomes from rehabilitation. In this paper we describe a proof of concept system utilising a commodity input device to play a bespoke video game to measure the critical components of motor learning. We demonstrate that we can detect how simple changes in therapist instruction significantly change motor performance and learning. Although video games have been shown to aid in rehabilitation, this is the first time video games have been used to derive early response markers, based on the measurement of performance and motor learning, for use in the evaluation of the efficacy of a rehabilitation strategy.

Motor variability is not noise, but grist for the learning mill

A study demonstrates that variability in how people perform a movement can predict the rate of motor learning on an individual basis. This suggests that motor 'noise' is a central component of motor learning.

Putting some excitement into constraint-induced movement therapy

This commentary is on the original article by Gillick et al. on pages 44–52 of this issue. Following publication of the Cochrane review in 2007,1 constraint-induced movement therapy (CIMT) has moved beyond the realm of experiment to a treatment, supported by some of the strongest evidence for children with cerebral palsy (CP). Paradoxically, studies evaluating CIMT have also led to the establishment of similarly strong evidence for bimanual upper limb therapy.2 With 33 published clinical or randomized controlled trials, results from studies of CIMT provide strong support for upper limb treatment models that provide time-limited, top-down or goal-directed, intensive blocks of training. Gone are the days for using bottom-up approaches where a child has therapy ‘done to them’. CIMT studies support two key components of motor learning: the initiation and active ‘doing’ of activities and the repetition of these at a sufficient intensity and level of challenge. Importantly, many models of CIMT embed the practice and learning of skills in a child's natural environment including home, pre-school, and school. These modifications, along with the knowledge that parents and carers, etc. who have received education can implement CIMT, challenge previous concerns that CIMT may not be feasible in a clinical setting. Models of CIMT, and for that matter, bimanual upper limb therapy, can be simple to implement, family-friendly, low-cost, yet very effective in improving outcomes in children with unilateral CP. In the ongoing pursuit to maximize the effect of treatment, a growing list of adjunct interventions, including functional electrical stimulation botulinum toxin-type A, and virtual reality, have been combined with CIMT. The addition of primed, low-frequency repetitive transcranial magnetic stimulation (rTMS) by Gillick et al.3 is an exciting addition to this list. To varying degrees in children with early unilateral brain lesion, the persistence of contralesional corticomotor projections from the non-lesioned cortex is an environmental response to provide movement to a more affected upper limb. Recent data suggest, however, that these projections may negatively influence the quality of unimanual and bimanual upper limb performance and also influence response to CIMT.4, 5 The science of upper limb treatment has, therefore, focused on encouraging repetitive, self-initiated movement of the more affected limb to stimulate activation of ipsilesional corticomotor projections and promote improved crossed corticospinal tract integrity. In a group of children, aged 8 to 17 years, with congenital hemiparesis and intact crossed corticospinal tract integrity, Gillick et al. primed the contralesional primary motor area (M1) using low frequency rTMS. In a fascinating twist, priming the cortex membrane of the contralesional hemisphere using rTMS results in subsequent inhibition of this hemisphere. Releasing, or disinhibiting the ipsilesional hemisphere from the shackles of contralesional hemisphere dominance, provides an advantage for the recruitment of ipsilesional corticomotor projections. The repetitive use of the more affected upper limb (CIMT) during this period facilitates an increase in the excitability of dormant neurons in the ipsilesional M1 and improves the potential to establish crossed projections from the lesioned hemisphere. Put simply, the addition of rTMS to CIMT is a novel method to ramp up the potential for activity-dependent plasticity in older children. This is an exciting preliminary study and despite the potentially invasive nature, no serious adverse events were reported. Larger studies, ensuring baseline group equivalence for ability level and age, are warranted. The nature of rTMS does limit its use to older children. However, this certainly does not mean younger children will be missing out. In fact, quite the opposite. While rTMS may potentially boost outcomes in older children, preliminary data from animal studies strongly support the notion of ‘the earlier the better’ for CIMT.6 Very early therapy during the critical period of brain development (<12 mo of age) moves away from a restorative paradigm to one of prevention. It is an exciting time for upper limb rehabilitation.

Correlations between brain activity and components of motor learning in middle-aged adults: an fMRI study

Implicit learning may be shown by improvements in motor performance, which occur unconsciously with practice and are typically restricted to the task that was practiced. The purpose of this study was to examine behaviorally relevant brain activation associated with change in motor behavior during sequence-specific motor learning of a perceptuomotor continuous tracking (CT) task in middle-aged adults. To gain further insight into the neural structures associated with change in motor behavior, overall improvement in tracking (root mean square error; RMSE) was decomposed into two components—temporal precision and spatial accuracy. We hypothesized that individual differences in CT task performance would be evident in unique networks of brain activation that supported overall tracking behavior as well-temporal and spatial tracking accuracy. A group of middle-aged healthy individuals performed the CT task, which contains repeated and random segments for seven days. Functional magnetic resonance imaging (fMRI) data was collected on the first and seventh day while the participants performed the task. Subjects did not gain explicit awareness of the sequence. To assess behaviorally-relevant changes in the blood oxygenation level-dependent (BOLD) response associated with individual sequence-specific tracking performance, separate statistical images were created for each participant and weighted by the difference score between repeated and random performance for days 1 and 7. Given the similarity of performance for random and repeated sequences during early practice, there were no unique networks evident at day 1. On Day 7 the resultant group statistical fMRI image demonstrated a positive correlation between RMSE difference score and bilateral cerebellar activation (lobule VI). In addition, individuals who showed greater sequence-specific temporal precision demonstrated increased activation in the precentral gyrus, middle occipital gyrus, and putamen of the right hemisphere and the thalamus, cuneus, and cerebellum of the left hemisphere. Activation of this neural network further confirms its involvement in timing of movements as it has been previously associated with task performance when individuals are instructed to emphasize speed over accuracy. In the present study, behavioral performance was associated with neural correlates of individual variation in motor learning that characterized the ability to implicitly learn a sequence-specific CT task.

Single session motor learning demonstrated using a visuomotor task: Evidence from fMRI and behavioural analysis

There is a continuing need to improve understanding of the central nervous system control of learning. Specifically, there is a need to examine the characteristics of cortical and sub-cortical activity linked to the stages of motor learning, including those occurring within a single-session. In this study we sought to design and investigate a visuomotor task to determine its ability to assess the component of motor learning occurring during a single session of fMRI (i.e., the ‘online’ improvement in motor performance). Fourteen healthy control subjects performed a visuomotor task requiring a combination of bilateral grip force to accurately move a cursor towards a target. We assessed online motor learning by comparing behavioural measures (accuracy and error magnitude) and the extent of spatial activation in specific brain regions of interest (ROIs) using fMRI pre- and post-training. Results showed a training-related improvement in performance based on increased accuracy (p<0.0125) and decreased error magnitude (p<0.0125) from pre- to post-training. Decreases in the extent of spatial activation from pre- to post-training in the majority of ROIs supported a training-related attenuation in brain activity associated with online motor learning. Importantly, decreases in error magnitude across conditions (p<0.05) confirmed that improvements in performance continued over the entire course of the experiment. Establishing this task may permit more extensive study of the neural correlates of single-session, online learning in healthy individuals and those with motor control challenges. Information obtained from such studies may provide an opportunity to improve interventions in neurological rehabilitation.

Motor learning

Although learning a motor skill, such as a tennis stroke, feels like a unitary experience, researchers who study motor control and learning break the processes involved into a number of interacting components. These components can be organized into four main groups. First, skilled performance requires the effective and efficient gathering of sensory information, such as deciding where and when to direct one's gaze around the court, and thus an important component of skill acquisition involves learning how best to extract task-relevant information. Second, the performer must learn key features of the task such as the geometry and mechanics of the tennis racket and ball, the properties of the court surface, and how the wind affects the ball's flight. Third, the player needs to set up different classes of control that include predictive and reactive control mechanisms that generate appropriate motor commands to achieve the task goals, as well as compliance control that specifies, for example, the stiffness with which the arm holds the racket. Finally, the successful performer can learn higher-level skills such as anticipating and countering the opponent's strategy and making effective decisions about shot selection. In this Primer we shall consider these components of motor learning using as an example how we learn to play tennis.

Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat

Successful motor skill learning requires repetitive training interrupted by rest periods. In humans, improvement occurs within and between training sessions reflecting fast and slow components of motor learning [Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, et al. The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 1998;95:861–8]. Here, these components are characterized in male and female rats using a model of skilled forelimb reaching and are compared to time scales of instrumental learning. Twenty female and 14 male adult Long–Evans rats were pre-trained to operate a motorized door (via a sensor in the opposite cage wall) to access a food pellet by tongue. Latencies between pellet removal and door opening were recorded as measures of instrumental learning. After criterion performance was achieved, skilled forelimb reaching was requested by increasing the pellet–window distance to 1.5 cm. Reaching success was recorded per trial. Mean latencies decreased exponentially over sessions and no improvement within-session was found. Skill learning over eight training sessions followed an exponential course in females and a sigmoid course in males. Females acquired the skill significantly faster than males starting at higher baseline levels ( P < 0.001) but reaching similar plateaus. Within-session improvement was found during the sessions 1–3 in females and 1–4 in males. Performance at the end of session 1 was not carried over to session 2. Learning curves of individual animals were highly variable. These findings confirm in rat that motor skill learning has fast and slow components. No within-session improvement is seen in instrumental learning.

Behavioral Analysis of Signals that Guide Learned Changes in the Amplitude and Dynamics of the Vestibulo-Ocular Reflex

We characterized the dependence of motor learning in the monkey vestibulo-ocular reflex (VOR) on the duration, frequency, and relative timing of the visual and vestibular stimuli used to induce learning. The amplitude of the VOR was decreased or increased through training with paired head and visual stimulus motion in the same or opposite directions, respectively. For training stimuli that consisted of simultaneous pulses of head and target velocity 80-1000 msec in duration, brief stimuli caused small changes in the amplitude of the VOR, whereas long stimuli caused larger changes in amplitude as well as changes in the dynamics of the reflex. When the relative timing of the visual and vestibular stimuli was varied, brief image motion paired with the beginning of a longer vestibular stimulus caused changes in the amplitude of the reflex alone, but the same image motion paired with a later time in the vestibular stimulus caused changes in the dynamics as well as the amplitude of the VOR. For training stimuli that consisted of sinusoidal head and visual stimulus motion, low-frequency training stimuli induced frequency-selective changes in the VOR, as reported previously, whereas high-frequency training stimuli induced changes in the amplitude of the VOR that were more similar across test frequency. The results suggest that there are at least two distinguishable components of motor learning in the VOR. One component is induced by short-duration or high-frequency stimuli and involves changes in only the amplitude of the reflex. A second component is induced by long-duration or low-frequency stimuli and involves changes in the amplitude and dynamics of the VOR.

L9 What to do and how to do it — Two distinct components of motor learning

L9 What to do and how to do it — Two distinct components of motor learning

Nonequivalent roles for motor and visual feedback in the Müller-Lyer and horizontal-vertical illusions

The relative contributions of motor and visual feedback to illusion decrement for the Muller-Lyer (ML) and horizontal-vertical (HV) illusions were estimated after subjects judged the perceived equality of standard and comparison lines with or without visual feedback and after the subject or the experimenter adjusted the comparison line (motor feedback). Visual feedback in the absence of motor feedback reduced magnitude of illusion by 38% for the ML illusion and by 45% for the HV illusion. Motor feedback in the absence of visual feedback reduced magnitude of illusion by 17% for the ML illusion and by 27% for the HV illusion. Estimates of “strategic” factors, commonly interpreted as the correction of inaccurate routine problem-solving and judgmental factors, also contain components of motor learning.