Do you really think your doctor has the ability to translate this from healthy adults to neurologically compromised adults?
Multiple processes independently predict motor learning
Journal of NeuroEngineering and Rehabilitation volume 17, Article number: 151 (2020)
Abstract
Background
Our ability to acquire, refine and adapt skilled limb movements is a hallmark of human motor learning that allows us to successfully perform many daily activities. The capacity to acquire, refine and adapt other features of motor performance, such as visual search, eye-hand coordination and visuomotor decisions, may also contribute to motor learning. However, the extent to which refinements of multiple behavioral features and their underlying neural processes independently contribute to motor learning remains unknown. In the current study, we used an ethological approach to test the hypothesis that practice-related refinements of multiple behavioral features would be independently predictive of motor learning.
Methods
Eighteen healthy, young adults used an upper-limb robot with eye-tracking to practice six trials of a continuous, visuomotor task once a week for six consecutive weeks. Participants used virtual paddles to hit away 200 “Targets” and avoid hitting 100 “Distractors” that continuously moved towards them from the back of the workspace. Motor learning was inferred from trial-by-trial acquisition and week-by-week retention of improvements on two measures of task performance related to motor execution and motor inhibition. Adaptations involving underlying neural processes were inferred from trial-by-trial acquisition and week-by-week retention of refinements on measures of skilled limb movement, visual search, eye-hand coordination and visuomotor decisions. We tested our hypothesis by quantifying the extent to which refinements on measures of multiple behavioral features (predictors) were independently predictive of improvements on our two measures of task performance (outcomes) after removing all shared variance between predictors.
Results
We found that refinements on measures of skilled limb movement, visual search and eye-hand coordination were independently predictive of improvements on our measure of task performance related to motor execution. In contrast, only refinements of eye-hand coordination were independently predictive of improvements on our measure of task performance related to motor inhibition.
Conclusion
Our results provide indirect evidence that refinements involving multiple, neural processes may independently contribute to motor learning, and distinct neural processes may underlie improvements in task performance related to motor execution and motor inhibition. This also suggests that refinements involving multiple, neural processes may contribute to motor recovery after stroke, and rehabilitation interventions should be designed to produce refinements of all behavioral features that may contribute to motor recovery.
Introduction
Humans learn to perform a broad repertoire of motor tasks that often require diverse and adaptable limb movements (i.e., skilled limb movements) to interact with our outside world. Many motor tasks, such as cooking, walking and driving, also employ diverse and adaptable patterns of eye movements (i.e., visual search) to actively gather visual information for planning and execution of skilled limb movements. Information gathered by visual search is also used to decide what skilled limb movements should be performed to achieve task goals (i.e., visuomotor decisions). Conversely, patterns of visual search are influenced by the available repertoire of skilled limb movements that can be used to achieve task goals. These interactions between skilled limb movements and visual search lead to coordinated patterns of eye and limb movements (e.g., eye-hand coordination). Overall, skilled limb movements, visual search, eye-hand coordination and visuomotor decisions may all contribute to learning and performance of motor tasks. However, we do not know the extent to which these behavioral features and their underlying neural processes are independently refined to produce improvements in task performance.
Given that many concepts in motor learning have unclear or ambiguous definitions, we will define several concepts based on how they are used in this study. “Motor tasks” refer to all tasks that require skilled limb movements to achieve their task goal. Accordingly, most activities of daily living (e.g., cooking, walking, driving) are considered motor tasks even if they engage perceptual, cognitive and motor functions. “Neural processes” refer to brain networks that manipulate perceptual, cognitive and motor information to perform motor tasks. “Motor learning” refers to acquisition and retention of practice-related improvements in task performance, where “task performance” refers to outcomes that are specific to achieving task goals and “improvements” necessitate increased achievement of task goals. We assume that motor learning results from neural adaptations that produce refinements of behavioral features of motor tasks (e.g., skilled limb movements, visual search, eye-hand coordination, visuomotor decisions), where “refinements” are practice-related changes that do not occur in a particular direction.
Traditional studies of motor learning have examined how skilled limb movements are refined during practice of motor tasks [1,2,3]. Studies of movement dynamics have found that muscle activations, joint torques and endpoint forces exhibit trial-by-trial refinements of coordination and efficiency [4,5,6]. Similarly, studies of movement kinematics have observed trial-by-trial refinements of speed, accuracy, smoothness and variability of skilled limb movements [7,8,9], and these refinements exhibit good day-by-day retention [10,11,12,13]. However, these studies were not designed to investigate if refinements of other behavioral features, such as visual search, eye-hand coordination and visuomotor decisions, contribute to motor learning.
Research on eye movements indicates that refinements of visual search may contribute to motor learning [14, 15]. Observational studies have found that experts at different visuomotor skills have better control of eye movements than novices [16,17,18,19,20]. Experimental studies have also demonstrated that interventions designed to improve control of eye movements and attention lead to improvements in visuomotor performance [21,22,23,24,25]. While none of these studies examined trial-by-trial or week-by-week refinements of eye movements, there is ample evidence that visual search is refined during practice of perceptual tasks [26,27,28,29,30]. However, these studies did not examine any relationships between refinements of visual search and improvements in task performance, nor did they investigate refinements of other behavioral features. Thus, we do not know if refinements of visual search independently contribute to motor learning.
Studies of spatiotemporal coupling between eye and hand movements have provided evidence that refinements of eye-hand coordination may contribute to motor learning. Patterns of eye-hand coordination vary with task demands [31, 32] and are refined during motor learning in a task-dependent manner [33,34,35,36]. However, it remains unclear if refinements of eye-hand coordination independently contribute to improvements in task performance, or if they result from refinements of skilled limb movements and visual search but do not actually contribute to motor learning.
It is widely accepted that sensory processes contribute to planning and execution of skilled limb movements [37]. In addition, information from sensory feedback provides reinforcement that is known to play an important role in motor learning [2]. Recent studies have also found that motor learning can induce changes in visual processing that are associated with refinements of skilled limb movement [38, 39]. This suggests that adaptations of visual and visuomotor processing contribute to motor learning. However, these studies were not designed to investigate the extent to which refinements of other behavioral features, such as visual search, eye-hand coordination and visuomotor decisions, may independently contribute to motor learning.
Despite evidence that refinements of multiple features might underlie motor learning, we do not know the extent to which they independently contribute to motor learning. Traditional experiments cannot easily address this problem because they are designed to isolate individual processes. In contrast, ethological approaches that study real-time, natural behavior can overcome this limitation by leveraging individual patterns of variability exhibited by several behavioral features [40]. However, this approach requires carefully controlling for any covariation between different features. For example, two or more processes may be associated with motor learning, but their individual patterns of variability might exhibit substantial covariance. This shared variance can cause regression analyses to produce incorrect estimates of the contributions made by each process. Accurate estimates of the individual contributions can only be obtained from the independent variance that remains after removing all shared variance.
The objective of the current study was to investigate the extent to which multiple neural processes might independently contribute to motor learning. Healthy young adults used an upper-limb robot with eye tracking to complete six weeks of practice of a novel, visuomotor task designed to mimic the richness of real-world visuomotor tasks. Motor learning was inferred from trial-by-trial acquisition and week-by-week retention of improvements on measures of task performance. Adaptations of multiple neural processes were inferred from trial-by-trial acquisition and week-by-week retention of refinements on measures of skilled limb movement, visual search, eye-hand coordination and visuomotor decisions. Our first hypothesis was that practicing our novel, visuomotor task would elicit trial-by-trial acquisition and week-by-week retention of improvements in task performance that are mirrored by concurrent refinements of skilled limb movements, visual search, eye-hand coordination and visuomotor decisions. Our second hypothesis was that refinements related to multiple neural processes would be independently predictive of improvements in task performance.
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