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.