Catherine F. Siengsukon

Sleep to learn after stroke: Implicit and explicit off-line motor learning

After stroke, many individuals experience persistent motor impairments as well as altered patterns of sleep. Therefore, examining the role of sleep in motor skill learning following stroke is a critical issue. Other learning variables, such as type of instruction, may interact with sleep to influence sleep-dependent motor learning. Forty individuals with stroke and 40 control participants practiced a continuous motor tracking task and then either slept (sleep condition) or stayed awake (no-sleep condition) between practice and retention testing. Half were provided explicit information regarding the presence of a repeating sequence (explicit condition), while the other half were not (implicit condition). After stroke, individuals demonstrated sleep-dependent off-line motor learning of both the implicit and explicit version of the continuous tracking task; however, individuals with stroke who stayed awake between practice and retention testing did not demonstrate an improvement in motor performance at retention. Neither sleep nor instruction differentiated the performance of the healthy control participants. These data suggest that aspects of motor recovery after stroke may be modulated by sleep.

Sleep enhances off-line spatial and temporal motor learning after stroke.

Background. Individuals with chronic stroke demonstrate sleep-dependent off-line motor learning of a continuous tracking task. However, it remains unclear which aspects of learned movements are preferentially enhanced by sleep (ie, spatial accuracy and/or the time lag of tracking). Objective. The purpose of this study was to investigate whether spatial tracking accuracy, temporal tracking accuracy, or both are enhanced by sleep during off-line motor learning after stroke. Methods. Individuals with chronic stroke and control participants either practiced a continuous tracking task in the evening and underwent retention testing the following morning (sleep groups) or practiced the task in the morning and underwent retention testing in the evening (no-sleep groups). Results. Individuals with stroke who slept between practice and retention testing demonstrated off-line improvements in both spatial and temporal elements of tracking at retention. Participants with a stroke who stayed awake between practice and retention testing did not demonstrate off-line improvements in either spatial tracking accuracy or the time lag of tracking. Control participants did not demonstrate sleep- or time-dependent enhancement of either component of the movement task. Time of day of testing was not a factor in practice related changes in motor performance. Conclusion. This study provides the first evidence that sleep enhances motor learning through both improved spatial tracking accuracy and anticipation of upcoming movements, as demonstrated by a reduction in the time lag of tracking in individuals following stroke. We propose that the cerebellum and hippocampus are likely important neural correlates associated with sleep-dependent off-line motor skill learning.

Does Sleep Promote Motor Learning? Implications for Physical Rehabilitation

Sleep following motor skill practice has repeatedly been demonstrated to enhance motor skill learning off-line (continued overnight improvements in motor skill that are not associated with additional physical practice) for young people who are healthy. Mounting evidence suggests that older people who are healthy fail to demonstrate sleep-dependent off-line motor learning. However, little is known regarding the influence of sleep on motor skill enhancement following damage to the brain. Emerging evidence suggests that individuals with brain damage, particularly following stroke, do benefit from sleep to promote off-line motor skill learning. Because rehabilitation following stroke requires learning new, and re-learning old, motor skills, awareness that individuals with stroke benefit from a period of sleep following motor skill practice to enhance skill learning could affect physical therapist practice. The objective of this article is to present the evidence demonstrating sleep-dependent off-line motor learning in young people who are healthy and the variables that may influence this beneficial sleep-dependent skill enhancement. In young people who are healthy, these variables include the stages of memory formation, the type of memory, the type of instruction provided (implicit versus explicit learning), and the task utilized. The neural mechanisms thought to be associated with sleep-dependent off-line motor learning also are considered. Research examining whether older adults who are healthy show the same benefits of sleep as do younger adults is discussed. The data suggest that older adults who are healthy do not benefit from sleep to promote off-line skill enhancement. A possible explanation for the apparent lack of sleep-dependent off-line motor learning by older adults who are healthy is presented. Last, emerging evidence showing that individuals with chronic stroke demonstrate sleep-dependent off-line motor skill learning and some of the possible mechanisms for this effect are considered.

Multidimensional Motor Sequence Learning Is Impaired in Older But Not Younger or Middle-Aged Adults

Background and Purpose: The purpose of this study was to identify which characteristics of a multidimensional sequence containing motor, spatial, and temporal elements would be most salient for motor sequence learning and whether age might differentially affect this learning. Subjects: Younger (n=11, mean age=26.0 years), middle-aged (n=13, mean age=50.7 years), and older (n=11, mean age=77.5 years) adults who were neurologically intact participated in the study. Methods: Participants practiced a sequencing task with repeated motor, spatial, and temporal dimensions for 2 days; on a separate third day, participants completed retention and interference tests designed to assess sequence learning and which elements of the sequence were learned. The mean median response time for each block of responses was used to assess motor sequence learning. Results: Younger and middle-aged adults demonstrated sequence-specific motor learning at retention testing via faster response times for repeated sequences than random sequences; both of these groups showed interference for the motor dimension. In contrast, older adults demonstrated nonspecific learning (ie, similar improvements in response time for both random and repeated sequences). These findings were shown by a lack of difference between random and repeated sequence performance in the older adult group both at retention testing and during interference tests. Conclusion and Discussion: Our data suggest that, when younger and middle-aged adults practice sequences containing multiple dimensions of movement, the motor element is most important for motor learning. The absence of sequence-specific change demonstrated by an older adult group that was healthy suggests an age-related impairment in motor learning that may have profound implications for rehabilitation.

Sleep Enhances Learning of a Functional Motor Task in Young Adults

Background Sleep has been demonstrated to enhance simple motor skill learning “offline” in young adults. “Offline learning” refers to either the stabilization or the enhancement of a memory through the passage of time without additional practice. It remains unclear whether a functional motor task will benefit from sleep to produce offline motor skill enhancement. Physical therapists often teach clients functional motor skills; therefore, it is important to understand how sleep affects learning of these skills. Objective The purpose of this study was to determine whether sleep enhances the learning of a functional motor task. Design A prospective, cross-sectional, repeated-measures design was used. Methods Young participants who were healthy (N=24) were randomly assigned to either a sleep group or a no-sleep group. The sleep group practiced a novel walking task in the evening and underwent retention testing the following morning, and the no-sleep group practiced the task in the morning and underwent retention testing in the evening. Outcome measures included time around the walking path and spatiotemporal gait parameters. Results Only participants who slept after practicing the novel walking task demonstrated a significant offline improvement in performance. Compared with the no-sleep group, participants in the sleep group demonstrated a significant decrease in the time around the walking path, an increase in tandem velocity, an increase in tandem step length, and a decline in tandem step time. Limitations Time-of-day effect and inability to ensure a certain amount of sleep quantity and quality of participants were limitations of the study. Conclusions This study is the first to provide evidence that sleep facilitates learning clinically relevant functional motor tasks. Sleep is an important factor that physical therapists should consider when teaching clients motor skills.

Manipulating time-to-plan alters patterns of brain activation during the Fitts’ task

Fitts’ law predicts that there is an essential trade-off between speed and accuracy during movement. Past investigations of Fitts’ law have not characterized whether advance planning of upcoming fast and accurate movements impacts either behavior or patterns of brain activation. With an event-related functional magnetic resonance imaging (fMRI) paradigm, we investigated the neural correlates of advance planning and movement difficulty of rapid, goal-directed aimed movements using a discrete version of the classic Fitts’ task. Our behavioral data revealed strong differences in response time, initial movement velocity, and end-point accuracy based on manipulation of both time to plan movements and response difficulty. We discovered a modulation of the neural network associated with executing the Fitts’ task that was dependent on the availability of time to plan the upcoming movement and motor difficulty. Specifically, when time to plan for the upcoming movement was available, medial frontal gyrus (BA 10), pre-SMA (BA 6), putamen and cerebellar lobule VI were uniquely active to plan movements. Further, their activation correlated with behavioral measures of movement. In contrast, manipulating movement difficulty invoked a different pattern of brain activations in regions that are known to participate in motor control, including supplementary motor area (BA 6), sensory motor cortex (BA 4, 3, 2) and putamen. Our finding that medial frontal gyrus (BA 10) was important for discrete, fast and accurate movements expands the known role of this brain region, which in the past has been identified as a cognitive processing system supporting stimulus-oriented attending. We now extend this conceptualization to include motor functions such as those employed for processing for rapid, goal-directed aimed movements.

Performance on a functional motor task is enhanced by sleep in middle-aged and older adults.

Background and Purpose: Although sleep has been shown to enhance motor skill learning, it remains unclear whether sleep enhances learning of a functional motor task in middle-aged and older individuals. The purpose of this study was to examine whether sleep enhances motor learning of a functional motor task in middle-aged and older adults. Methods: Twenty middle-aged and 20 older individuals were randomly assigned to either the sleep condition or the no-sleep condition. Participants in the sleep condition practiced a novel walking task in the evening, and returned the following morning for retesting. Participants in the no-sleep condition practiced the walking task in the morning and returned the same day in the evening for a retest. Outcome measures included time around the walking path and spatiotemporal gait parameters. Results: Only the middle-aged and older adults in the sleep condition demonstrated significant off-line improvement in performance, measured as a decline in time to walk around the novel path and improvement in spatiotemporal gait parameters. The middle-aged and older adults in the no-sleep condition failed to demonstrate off-line improvements in performance of this functional task. Conclusions: This is the first study to provide evidence that sleep facilitates learning a clinically relevant functional motor task in middle-aged and older adults. Because many neurologic conditions occur in the middle-aged and older adults and sleep issues are very prevalent in many neurologic conditions, it is imperative that physical therapists consider sleep as a factor that may impact motor learning and recovery in these individuals. Video Abstract available. (See Video, Supplemental Digital Content 1, http://links.lww.com/JNPT/A73) for more insights from the authors.

Older adults with and without stroke reduce cadence to meet the demands of talking.

Purpose:Cognitive tasks performed while walking can be challenging for older adults, especially for those with stroke. Conversational speech requires attention and working memory. The purpose of this study was to examine how older adults with and without stroke meet the demands of walking while talking. Methods:Community-dwelling older adults, 12 without stroke and 24 with, were videotaped walking an irregular elliptical pathway. Audio recordings were made as subjects discussed topics such as describing a memorable vacation. Each participant performed in single and dual task conditions: speaking, walking, and speaking while walking. Primary measures of interest included cadence and speech rate. Components of language including measures of fluency, grammatical complexity, and semantic content were analyzed to examine additional changes in speech. Paired t-tests were used to compare single and dual task performance for each group. Group differences for dual task effects were examined with independent sample t tests. Results:Cadence decreased with the addition of talking for those without stroke, P < .007, and those with stroke, P < .001. Speech rates did not change with walking for either group; those without stroke did not alter the language components. Participants with stroke reduced the grammatical complexity and semantic content of speech when walking, Ps < .013. Those without stroke spent more time doing both tasks at once than those with stroke, P < .023. Conclusion:Clinicians can expect older adults to reduce walking speed to meet the demands of walking and talking. Older adults with stroke may use additional strategies to walk and talk simultaneously.

Sleep Parameters, Functional Status, and Time Post-Stroke are Associated with Offline Motor Skill Learning in People with Chronic Stroke.

Background Mounting evidence demonstrates that individuals with stroke benefit from sleep to enhance learning of a motor task. While stage NREM2 sleep and REM sleep have been associated with offline motor skill learning in neurologically intact individuals, it remains unknown which sleep parameters or specific sleep stages are associated with offline motor skill learning in individuals with stroke. Methods Twenty individuals with chronic stroke (>6 months following stroke) and 10 control participants slept for three consecutive nights in a sleep laboratory with polysomnography. Participants practiced a tracking task the morning before the third night and underwent a retention test the morning following the third night. Offline learning on the tracking task was assessed. Pearson’s correlations assessed for associations between the magnitude of offline learning and sleep variables, age, upper-extremity motor function, stroke severity, depression, and time since stroke occurrence. Results Individuals with stroke performed with significantly less error on the tracking task following a night of sleep (p = 0.006) while the control participants did not (p = 0.816). Increased sleep efficiency (r = −0.285), less time spent in stage NREM3 sleep (r = 0.260), and more time spent in stage REM sleep (r = −0.266) were weakly-to-moderately associated with increased magnitude of offline motor learning. Furthermore, higher upper-extremity motor function (r = −0.400), lower stroke severity (r = 0.360), and less time since stroke occurrence (r = 0.311) were moderately associated with increased magnitude of offline motor learning. Conclusion This study is the first study to provide insight into which sleep stages and individual characteristics may be associated with offline learning in people with stroke. Further research is needed to delineate which factors or combination of factors promote offline motor learning in people with neurologic injury to best promote motor recovery in these individuals.

Time rather than sleep appears to enhance off-line learning and transfer of learning of an implicit continuous task

There is increasing evidence that sleep promotes off-line enhancement of a variety of explicitly learned motor tasks in young adults. However, whether sleep promotes off-line consolidation of implicitly learned motor tasks is still under question. Furthermore, the role of sleep in promoting transfer of learning remains unknown. This study examined the role of sleep in learning and transfer of learning of an implicit continuous motor task. Twenty-three neurologically intact individuals (mean age 26.4 years) were randomly assigned to either a sleep group or a no-sleep group. The sleep group practiced a continuous tracking task in the evening and underwent retention and transfer testing the following morning, while the no-sleep group practiced the tracking task in the morning and underwent retention and transfer testing in the evening. The results show that in both the sleep and no-sleep groups, performance improved off-line without further practice for both the general skill and the sequence-specific skill. The results also indicate that sleep and time promote transfer of learning of both sequence-specific and general skill learning to a spatial and temporal variation of the motor task. These findings demonstrate that sleep does not play a critical role in promoting off-line learning and transfer of learning of an implicit continuous motor task.