Sleep to Learn after Stroke: The Role of Sleep and Instruction in Off-line Motor Learning

Stroke affects nearly 780,000 individuals each year in the United States and is a leading cause of adult disability. More than half of individuals following stroke experience persistent loss of function. Learning new motor skills and re-learning old motor skills is an important component of rehabilitation following stroke. Examining methods that hasten or increase the efficiency of motor skill learning following stroke is an important clinical endeavor. Sleep has been demonstrated to produce off-line improvements in motor learning in young, neurologically intact individuals. However, the role of sleep in motor learning following stroke is unclear. Addressing this question was the purpose of this body of work. Chapter 2 utilized the discrete serial reaction time (SRT) task to examine the difference in both motor performance and learning for forty-two participants who either remained unaware of the presence of the sequence (implicit condition), were given no instruction of the sequence prior to the start of practice but gained explicit awareness during practice (acquired explicit condition), or were provided explicit instruction prior to practice (explicit condition). Results demonstrate a benefit of explicit knowledge to improve response time both during task practice and at retention regardless of whether it was acquired during or provided in advance of practice. This study highlights the frequent ability of people to acquire awareness of the regularities of the task being practice, creating a continuum of implicit motor learning from "pure" implicit learning where the participants have no awareness of the regularities being practiced to full explicit motor learning with the participants having complete awareness of the task regularities. This study led us to utilize a continuous tracking task to examine the role of sleep and type of instruction in off-line motor learning following stroke and in healthy, older control participants in order to differentiate between off-line implicit and explicit motor learning. While mounting evidence demonstrates sleep is critical for motor skill learning in healthy, younger individuals, the importance of sleep for off-line motor learning after stroke is unknown. Therefore, Chapter 3 examined sleep-dependent off-line motor learning of an implicit continuous tracking task. Eighteen individuals following stroke in the MCA distribution practiced the tracking task and then either slept (sleep condition) or stayed awake (no-sleep condition) for a similar period of time before retention testing to assess off-line motor learning. Eighteen sex- and age-matched participants served as controls. Only the stroke participants who slept between practice and retention testing demonstrated off-line implicit motor learning at retention. The stroke participants who stayed awake between practice and retention did not demonstrate off-line motor learning nor did either of the control groups. This study provides the first evidence that individuals following stroke benefit from sleep to enhance implicit motor learning off-line. Other learning variables, such as type of instruction, have been shown to influence the beneficial role of sleep in off-line motor skill learning in young, neurologically intact individuals. Therefore, Chapter 4 extended the findings of Chapter 3 and examined sleep-dependent off-line motor learning of both an implicit and explicit version of the continuous tracking task. Forty individuals post-stroke and 40 control participants were assigned to either the sleep group or the no-sleep group, as in Chapter 3. To examine the influence of type of instruction on off-line learning, half of the individuals in both the sleep and no-sleep condition were provided explicit instruction regarding the presence of a repeating sequence (explicit condition) while the other half were not (implicit condition). The individuals post-stroke who slept between practice and retention testing demonstrated sleep-dependent off-line motor learning of both the implicit and explicit version of the continuous tracking task. Individuals with stroke who stayed awake between practice and retention testing did not demonstrate an off-line improvement in motor performance at retention. The healthy control participants did not demonstrate off-line improvements in performance regardless of sleep of type of instruction. These results demonstrate that after stroke, individuals benefit from sleep to improve performance of a tracking task off-line regardless of type of memory system involved. Learning a motor skill requires the integration of the spatial and temporal movement components of the task. Little is known if particular components of a motor skill task (spatial and/or temporal components) are preferentially enhanced following sleep in individuals following stroke. Chapter 5 sought to address this question by deconstructing the overall change in tracking accuracy displayed by the participants in Chapter 4 into spatial and temporal movement components. The results reveal that the individuals with stroke who demonstrated overall off-line improvements in motor learning attributable to sleep improved spatial accuracy as well as reduced the time lag of tracking off-line. Participants following stroke who stayed awake between practice and retention testing did not demonstrate an improvement in either spatial accuracy or a reduction in time lag of tracking at retention. Likewise, the control participants did not demonstrate sleep- or time-dependent enhancement of either movement component. This study provides the first evidence that sleep enhances both spatial and temporal movement components of a motor learning task in individuals following stroke. In summary, this body of work demonstrates that individuals following stroke benefit from sleep to enhance both implicit and explicit off-line motor learning. In addition, this sleep-dependent off-line motor learning extends to both the spatial and temporal movement components of the tracking task. This work also provides concurrent evidence that healthy, older adults fail to benefit from sleep to enhance off-line motor learning. While it remains unclear why individuals following stroke are able to benefit from sleep to promote off-line motor learning and healthy, older adults are not, we propose that alterations in sleep architecture and changes in cortical excitability following stroke likely contribute to sleep-dependent off-line motor learning. The findings of this body of work are important because evidence that sleep enhances off-line motor learning following stroke could impact the design of rehabilitation interventions; to maximize motor learning and recovery after stroke it may be critical to ensure that sleep occurs between practice sessions

Sleep promotes offline enhancement of an explicitly learned discrete but not an explicitly learned continuous task

Catherine F Siengsukon, Alham Al-SharmanDepartment of Physical Therapy and Rehabilitation Science, University of Kansas Medical Center, Kansas City, KS, USABackground: Healthy young individuals benefit from sleep to promote offline enhancement of a variety of explicitly learned discrete motor tasks. It remains unknown if sleep will promote learning of other types of explicit tasks. The purpose of this study is to verify the role of sleep in learning an explicitly instructed discrete motor task and to determine if participants who practice an explicitly instructed continuous tracking task demonstrate sleep-dependent offline learning of this task.Methods: In experiment 1, 28 healthy young adults (mean age 25.6 ± 3.8 years) practiced a serial reaction time (SRT) task at either 8 am (SRT no-sleep group) or 8 pm (SRT sleep group) and underwent retention testing 12 ± 1 hours later. In experiment 2, 20 healthy young individuals (mean age 25.6 ± 3.3 years) practiced a continuous tracking task and were similarly divided into a no-sleep (continuous tracking no-sleep group) or sleep group (continuous tracking sleep group). Individuals in both experiments were provided with explicit instruction on the presence of a sequence in their respective task prior to practice.Results: Individuals in the SRT sleep group demonstrated a significant offline reduction in reaction time whereas the SRT no-sleep group did not. Results for experiment 1 provide concurrent evidence that explicitly learned discrete tasks undergo sleep-dependent offline enhancement. Individuals in the continuous tracking sleep group failed to demonstrate a significant offline reduction in tracking error. However, the continuous tracking no-sleep group did demonstrate a significant offline improvement in performance. Results for experiment 2 indicate that sleep is not critical for offline enhancement of an explicit learned continuous task.Conclusion: The findings that individuals who practiced an explicitly instructed discrete task experienced sleep-dependent offline learning while those individuals who practiced an explicitly instructed continuous task did not may be due to the difference in motor control or level of complexity between discrete and continuous tasks.Keywords: sleep, motor learning, discrete task, continuous tas

Self-report sleep quality combined with sleep time variability distinguishes differences in fatigue, anxiety, and depression in individuals with multiple sclerosis: A secondary analysis

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author's publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.Background: Nearly 70% of individuals with multiple sclerosis report sleep disturbances or poor sleep quality. Sleep disturbances may exacerbate or complicate the management of multiple sclerosis-related symptoms. While sleep variability has been associated with several health outcomes, it is unclear how sleep variability is associated with multiple sclerosis-related symptoms. Objective: The purpose of this study was to determine how total sleep time variability combined with self-reported sleep quality is associated with fatigue, depression, and anxiety in individuals with multiple sclerosis. Methods: This study involved a secondary analysis of actigraphy data and questionnaires to assess sleep quality, fatigue, anxiety, and depression. Results: There were significant differences between the Good Sleepers (good sleep quality/low sleep time variability; n¼14) and Bad Sleepers (poor sleep quality/high sleep time variability; n¼23) in overall fatigue (p¼0.003), cognitive (p¼0.002) and psychosocial fatigue (p¼0.01) subscales, and in trait anxiety (p¼0.007). There were significant differences in state (p¼0.004) and trait (p¼0.001) anxiety and depression (p¼0.002) between the Good Sleepers and Poor Reported Sleepers (poor sleep quality/low sleep time variability; n¼24). Conclusion: These results indicate different factors are associated with poor sleep quality in individuals with low versus high total sleep time variability. Considering the factors that are associated with sleep quality and variability may allow for better tailoring of interventions aimed at improving sleep issues or comorbid conditions.National Multiple Sclerosis Society Pilot Grant (PP2068)National Institutes of Health Clinical and Translational Science Award Grant (UL1TR000001 formerly UL1RR033179)

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

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author’s publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.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

Integrating Sleep Promotion Education into Acute Care Orthopedics Occupational Therapy Practice: A Case Series Study

Background: The occupation of sleep is frequently under-addressed by occupational therapists with their clients. This may be in part because of a lack of general training on addressing this occupational domain or a lack of education about the basics of sleep. The domain of sleep has been in the Occupational Therapy Practice Framework since 2008. However, it remains unclear how to address the domain of sleep in occupational therapy practice. Therefore, the purpose of this case series is to describe the practical application of sleep promotion education. Methods: A practicing occupational therapist with sleep training provided sleep promotion education to five clients following an orthopedic surgery in an acute care setting. A client interview was performed to gather sleep concerns and inform specific content of the sleep promotion education. The clients were asked their motivation, satisfaction, and likelihood to use the education. Results: A detailed description of each client and how the education was tailored is provided in conjunction with the occupational therapist response to concerns. Overall, the clients reported that sleep promotion education was useful, satisfying, and that they were likely to use the education. Conclusions: This case series describes the practical application of sleep promotion education in occupational therapy practice in an acute care setting

Sleep quality in the chronic stage of concussion is associated with poorer recovery: A systematic review

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author's publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.Background Recovery from a concussion varies based on a multitude of factors. One such factor is sleep disturbances. In our prior review, it was observed that in the acute phase, sleep disturbances are predictive of poor outcomes following a concussion. The literature gap remains on how sleep in the chronic phase of recovery affects outcomes. Objective To examine the association between sleep quality during the chronic stage of concussion and post-concussion outcomes. Literature Survey: Literature searches were performed during 1 July to 1 August 2019 in selected databases along with searching grey literature. Out of the 733 results, 702 references were reviewed after duplicate removal. Methods Three reviewers independently reviewed and consented on abstracts meeting eligibility criteria (n = 35). The full-text articles were assessed independently by two reviewers. Consensus was achieved, leaving four articles. Relevant data from each study was extracted using a standard data-extraction table. Quality appraisal was conducted to assess potential bias and the quality of articles. Results One study included children (18–60 months) and three studies included adolescents and/or adults (ranging 12–35 years). The association between sleep and cognition (two studies), physical activity (one study), and emotion symptoms (one study) was examined. Sleep quality was associated with decreased cognition and emotional symptoms, but not with meeting physical activity guidelines six months post-concussion injury. Conclusions The heterogeneity in age of participants and outcomes across studies and limited number of included studies made interpretations difficult. Future studies may consider if addressing sleep quality following concussion will improve outcomes

Sleep characteristics of individuals with chronic stroke: A pilot study

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author's publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.Changes in sleep characteristics in individuals with chronic stroke are not well described, particularly compared with healthy individuals. Therefore, the aim of this pilot study was to explore the sleep characteristics in individuals with chronic stroke compared to age- and sex-matched controls. Sixteen individuals with chronic stroke and ten age- and sex-matched controls underwent two nights of polysomnographic recording. The sleep characteristics of interest included total sleep time, sleep efficiency, and percent time, as well as time in minutes spent in stages N1, N2, and N3 and stage R sleep. The individuals with chronic stroke spent less percent time in stage N3 compared with controls (P=0.048). No significant differences in the other sleep characteristics were found between the stroke and control groups. Individuals with chronic stroke present with altered stage N3 sleep compared with healthy controls. These alterations in stage N3 sleep might be a sign of neuronal dysfunction and may impact recovery following stroke. A larger scale study is needed to confirm these findings.American Heart Association Scientist Development Grant (09SDG2060618

Sleep parameters, functional status, and time post-stroke are associated with offline motor skill learning in people with chronic stroke

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author’s publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.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

Hybrid brain-computer interface and functional electrical stimulation for sensorimotor training in participants with tetraplegia: a proof-of-concept study

Background and Purpose: Impaired hand function decreases quality of life in persons with tetraplegia. We tested functional electrical stimulation (FES) controlled by a hybrid brain-computer interface (BCI) for improving hand function in participants with tetraplegia. Methods: Two participants with subacute tetraplegia (participant 1: C5 Brown-Sequard syndrome, participant 2: complete C5 lesion) took part in this proof-of-concept study. The goal was to determine whether the BCI system could drive the FES device by accurately classifying participants' intent (open or close the hand). Participants 1 and 2 received 10 sessions and 4 sessions of BCI-FES, respectively. A novel time-switch BCI strategy based on motor imagery was used to activate the FES. In one session, we tested a hybrid BCI-FES based on 2 spontaneously generated brain rhythms: a sensory-motor rhythm during motor imagery to activate a stimulator and occipital alpha rhythms to deactivate the stimulator. Participants received BCI-FES therapy 2 to 3 times a week in addition to conventional therapy. Imagery ability and muscle strength were measured before and after treatment. Results: Visual feedback was associated with a 4-fold increase of brain response during motor imagery in both participants. For participant 1, classification accuracy (open/closed) for motor imagery-based BCI was 83.5% (left hand) and 83.8% (right hand); participant 2 had a classification accuracy of 83.8% for the right hand. Participant 1 had moderate improvement in muscle strength, while there was no change for participant 2. Discussion and Conclusion: We demonstrated feasibility of BCI-FES, using 2 naturally generated brain rhythms. Studies on a larger number of participants are needed to separate the effects of BCI training from effects of conventional therapy

Effect of Cognitive Behavioral Therapy for Insomnia on Insomnia Symptoms for Individuals With Type 2 Diabetes: Protocol for a Pilot Randomized Controlled Trial

A grant from the One-University Open Access Fund at the University of Kansas was used to defray the author's publication fees in this Open Access journal. The Open Access Fund, administered by librarians from the KU, KU Law, and KUMC libraries, is made possible by contributions from the offices of KU Provost, KU Vice Chancellor for Research & Graduate Studies, and KUMC Vice Chancellor for Research. For more information about the Open Access Fund, please see http://library.kumc.edu/authors-fund.xml.Background: Insomnia symptoms are a common form of sleep difficulty among people with type 2 diabetes (T2D) affecting sleep quality and health outcomes. Several interventional approaches have been used to improve sleep outcomes in people with T2D. Nonpharmacological approaches, such as cognitive behavioral therapy for insomnia (CBT-I), show promising results regarding safety and sustainability of improvements, although CBT-I has not been examined in people with T2D. Promoting sleep for people with insomnia and T2D could improve insomnia severity and diabetes outcomes. Objective: The objective of this study is to establish a protocol for a pilot randomized controlled trial (RCT) to examine the effect of 6 sessions of CBT-I on insomnia severity (primary outcome), sleep variability, and other health-related outcomes in individuals with T2D and insomnia symptoms. Methods: This RCT will use random mixed block size randomization with stratification to assign 28 participants with T2D and insomnia symptoms to either a CBT-I group or a health education group. Outcomes including insomnia severity; sleep variability; diabetes self-care behavior (DSCB); glycemic control (A1c); glucose level; sleep quality; daytime sleepiness; and symptoms of depression, anxiety, and pain will be gathered before and after the 6-week intervention. Chi-square and independent t tests will be used to test for between-group differences at baseline. Independent t tests will be used to examine the effect of the CBT-I intervention on change score means for insomnia severity, sleep variability, DSCB, A1c, fatigue, sleep quality, daytime sleepiness, and severity of depression, anxiety, and pain. For all analyses, alpha level will be set at .05. Results: This study recruitment began in February 2019 and was completed in September 2019. Conclusions: The intervention, including 6 sessions of CBT-I, will provide insight about its effect in improving insomnia symptoms, sleep variability, fatigue, and diabetes-related health outcomes in people with T2D and those with insomnia symptoms when compared with control