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Aerobic Exercise to Improve Executive Function in Parkinson Disease: A Case Series

Tabak, Rachel PT, DPT; Aquije, Gwendolyne PT, DPT; Fisher, Beth E. PT, PhD

Journal of Neurologic Physical Therapy: June 2013 - Volume 37 - Issue 2 - p 58–64
doi: 10.1097/NPT.0b013e31829219bc
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Background and Purpose: Parkinson disease (PD) affects cognition, specifically executive function. In people with PD, impaired executive function has been identified as an indicator of fall risk and decreased quality of life. Therefore, it is important to consider impaired executive function in the physical therapy management of PD. It has been established that exercise improves cognition in older adults and emerging evidence suggests a similar effect in people with neurological conditions. We assessed changes in executive function in an aerobic exercise intervention in 2 people with cognitive impairments due to PD.

Case Description: Two individuals with PD participated in this case series. Participant 1 was a 61-year-old woman with PD dementia, who had PD for 14 years. Participant 2 was a 72-year-old man with mild cognitive impairments, who had PD for 7 years.

Intervention: The participants completed an 8-week program of aerobic exercise training on a stationary bicycle. Primary outcome measures examined executive function, and secondary measures examined disease severity, quality of life, and walking function.

Outcomes: Both participants demonstrated improvements in all measures of executive function and quality of life. Participant 1 also made improvements in walking function.

Discussion: Our outcomes provide preliminary evidence of improved executive function following aerobic exercise in people with PD with cognitive impairments. Larger studies are needed to confirm these findings and investigate whether a causal relationship exists between exercise and improved executive function in persons with PD, and how these impact motor performance and quality of life measures.

Video Abstract available (see Video, Supplemental Digital Content 1, http://links.lww.com/JNPT/A43) for more insights from the authors.

Supplemental Digital Content is Available in the Text.

Division of Biokinesiology and Physical Therapy (R.T., G.A., B.E.F.) and Department of Neurology at the Keck School of Medicine (B.E.F.), University of Southern California, Los Angeles.

Correspondence: Rachel Tabak, PT, DPT, Division of Biokinesiology and Physical Therapy, University of Southern California, 1540 E Alcazar St, Los Angeles, California 90089 (Rtabak@dhs.lacounty.gov).

Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal's Web site (www.jnpt.org).

The authors declare no conflict of interest.

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INTRODUCTION

While motor deficits are the most common focus of physical therapy intervention for people with Parkinson disease (PD), it is important to consider the impact of impaired cognition in the management of the motor deficits associated with PD and as an important contributor to the overall wellness of the individual. It is well established that PD affects cognition.1,2 The term “cognition” describes multiple mental processes, including executive function. Executive function includes but is not limited to judgment, planning, initiation, abstraction, problem solving, sequencing, and mental flexibility. Individuals with PD most notably demonstrate impaired executive function.3 The incidence of mildly impaired executive function in people with PD has been reported to be as high as 44%, and the incidence of PD dementia has been reported to be as high as 29%.4 Multiple studies5–10 have identified impaired executive function as a major indicator of quality of life in people with PD. Impaired executive function has also been shown to adversely affect motor performance and is directly related to fall risk in individuals with PD.11,12

The impact of impaired executive function on motor performance is most apparent when individuals with PD attend to a secondary task while walking, also known as dual-task performance. People with PD walk with increased gait arrhythmicity and unsteadiness when attempting to dual task, as compared with age-matched, healthy individuals.13

Aerobic exercise has been shown to improve executive function and prevent decline in healthy older adults,14–19 specifically in the domains of attention,14–19 abstraction,15 visual construction,14–16,18,19 judgment,15 verbal fluency,15,17 and immediate or delayed verbal recall.14,16–19 Similarly, emerging evidence suggests that exercise may help improve executive function in individuals with preexisting neurological, psychiatric, and cognitive impairments. Powell20 first reported improved executive function in institutionalized psychiatric patients following 12 weeks of moderate exercise. Kubesch et al21 observed improved reaction times in individuals with major depressive disorders following endurance training on a stationary bike. Similar outcomes have been reported through pilot studies of people with stroke22 and traumatic brain injury.23 A meta-analysis,24 including 30 trials of the effects of exercise on executive function in older adults with cognitive impairments, revealed a moderate effect size for improved executive functioning following aerobic exercise programs (effect size, 0.57; 95% confidence interval, 0.43-1.17).

A potential mechanism underlying the improvements observed in executive function in association with exercise is increased cerebral perfusion,25 which occurs as a direct result of increased cardiac output from aerobic exercise.26 Release of insulin growth factor–1 and vascular endothelial growth factor27 following prolonged exercise could also account for improved executive function. These growth factors, which are able to cross the blood-brain barrier, contribute to angiogenesis within the brain. Evidence of angiogenesis following aerobic exercise has been reported in a mouse model of PD.28

Three studies29–31 have investigated exercise-induced changes in executive function in people with PD, and of these, 229,30 have used multiple intervention methods, including aerobic and resistance exercise. While these studies revealed preliminary evidence of improved executive functioning following exercise, the effect of aerobic exercise alone has not been established. Importantly, no study, to date, investigating exercise-induced changes in executive function has included individuals with PD who had documented cognitive impairments. The purpose of this case series was to describe changes in executive function associated with an 8-week aerobic exercise intervention in 2 individuals with PD with cognitive impairments. We also examined changes in disease severity, quality of life, and walking function.

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CASE SERIES

Participants

Participants were recruited from the Movement Disorder Clinic at the Keck School of Medicine, University of Southern California, and through flyers distributed to local PD organizations and support groups. People with PD were eligible for participation if they had cognitive impairments, demonstrated by a score of less than 26 of 30 on the Montreal Cognitive Assessment (MoCA).32,33 The MoCA was chosen to measure cognitive impairment as it is a more sensitive measure than the Mini-Mental State Examination for the detection of subtle cognitive deficits in individuals with PD.33 Exclusion criteria included the presence of depression (measured by the Geriatric Depression Scale,34 score ≥ 12), severe cardiac disease (including congestive heart failure or ischemic disease, presence of pacemaker, or orthostatic hypotension), uncontrolled diabetes, history of stroke, traumatic brain injury or seizure disorder, or reported reduced effectiveness of their PD medications. Those currently participating in a self-directed or formal group exercise program were not included. Eighteen people expressed interest and 6 people were screened for eligibility. The 12 potential participants not screened chose to remove themselves from recruitment efforts because of the time commitment required to complete the study. All potential participants gave written informed consent to participate in the study, which had been approved by the institutional review board of the University of Southern California. Of those screened, 4 scored higher than 26 on the MoCA, and the remaining 2 people were eligible and included in this case series. Both participants completed the Physical Activity Readiness Questionnaire and the American Heart Association/American College of Sports Medicine Health/Fitness Facility Pre-participation Screening Questionnaire to identify previous or existing health conditions that might require precaution during exercise.

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Outcome Measures

Baseline and postintervention measures were taken for both participants. Executive function was measured by using the MoCA, Parkinson's Disease Cognitive Rating Scale,35 and the Color Trails Test 1 and 236 (CTT-1 and CTT-2). The MoCA has established test-retest reliability and construct validity for detecting cognitive impairments in people with PD.37 The domains of executive function measured by the MoCA include visuospatial memory, abstraction, attention, and delayed verbal memory. The Parkinson's Disease Cognitive Rating Scale is a fairly new measure that has high sensitivity and specificity for detecting mild to severe cognitive impairments in people with PD, as well as established concurrent and discriminative validity and reliability.35 This assessment measures the following domains of executive function: immediate and delayed verbal memory, confrontation naming, sustained attention, working memory, visuospatial memory, and verbal fluency. The CTT-1 and CCT-2 have established criterion validity for use in people with PD.36 The CTT measures sustained attention, set shifting, and mental flexibility by timing how fast individuals are able to consecutively connect numbers (CTT-1) while alternating between the colors in which the numbers are embedded (CTT-2).

Dual-task cost represents the decrement in performance of a task performed in the presence of a secondary task compared with when it is performed alone. Therefore, a lower dual-task (ie, less decrement) cost represents improved performance. Dual-task cost was calculated for the cognitive task of serial subtraction and the motor task of walking. Each task was performed first in a single-task condition. For the single-condition cognitive task, the seated participants were asked to perform as many correct serial subtractions as possible in 2 minutes. Participants first attempted to perform the serial subtraction test, using intervals of 7. If they were unable to correctly complete 5 serial subtractions, the interval was decreased until the participants were able to perform the task correctly. Participants received a point for each correct subtraction, starting from 200. For the single-condition motor task, the participants were asked to walk as far as they could during the 2-Minute Walk Test. The distance traveled was measured in meters. In the dual-task condition, the 2 tasks were combined such that the participant would be asked to perform the same serial subtraction while walking as far as possible during the 2-Minute Walk Test. Before performing the dual walking and subtraction task, all participants were told that serial subtraction was the priority task of attention. The equation to calculate dual-task cost, as described by Rucker et al,38 is:

Dual-task cost = ((single-task performance − dual-task performance)/single-task performance) × 100.

Assessment of secondary measures related to motor performance, participation, and quality of life was conducted. These secondary outcomes were measured to see whether they changed concurrently with executive function. Motor performance was assessed as gait speed and balance, which were measured by the 10-Meter Walk Test and the Functional Gait Assessment (FGA),39 respectively. High reliability and moderate validity for the FGA have been reported as a balance assessment in people with PD.39 The fall risk cutoff for people with PD is 15 of 30.39 Change in gait speed was collected for comparison with the established minimal detectable change for this population of 0.18 m/s.40 In addition, mentation, mood, behavior, and ability to perform activities of daily life were assessed by using the 39-Item Parkinson's Disease Questionnaire (PDQ-39)41 and the Unified Parkinson's Disease Rate Scale Part 1 and Part 2 (UPDRS-1 and UPDRS-2).42 The PDQ-39 contains 8 subcategories, each with a reported value of minimal clinically important differences.41 For the UPDRS, the minimal clinically important difference for our study population is reported to be at least 2.2 points.42

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Intervention

The intervention consisted of twenty-four 1-hour sessions performed 3 times weekly over 8 weeks. All sessions were administered by the first or second author (R. T. and G. A.) and were conducted separately for each participant. The time of the session was selected by the participants on the basis of when they felt the optimal effects of their medication, and this same relative timing was kept consistent throughout the study. Aerobic exercise consisted of cycling on a stationary bicycle (M3, Keiser, Fresno, California). All sessions took place at the Clinical Exercise Research Center at the Division of Biokinesiology and Physical Therapy, University of Southern California in Los Angeles. Each session began and ended with 5 minutes of gentle stretching, targeting major muscle groups of the upper and lower extremities, for the purpose of injury prevention. Continuous cycling was performed for 40 minutes, with the first and last 5 minutes designated as warm-up and cool-down periods, performed at a self-selected cycling pace. The intensity of the middle 30 minutes of cycling was increased progressively from an initial target of 50% maximum heart rate (HR) during week 1 to 75% of maximum HR at week 8. The maximum HR was calculated by using the following formula: 220 − age. This formula was selected as it has been used in previous studies of persons with PD.29,30 A formula more specific to determining maximum HR in older adults was not used as our eligibility criteria was not specific to older adults. As both participants were sedentary individuals, the initial intensity was set at 50% of maximum HR, because this is the least-intensive HR that is still considered to be aerobic. Participants were encouraged to cycle as fast as they could, with a goal of maintaining 90 revolutions per minute (RPM) throughout the middle 30 minutes. This rate was selected as it has been established as the most efficient pedaling rate for long-distance cyclists.43 Pedaling resistance was kept low throughout all sessions for both participants. Motivation strategies (consisting of incremental goal setting, verbal encouragement, and cycling alongside the participant) to maximally engage each participant were employed as needed per session. Measures of HR, blood pressure, RPM, and rate of perceived exertion (per the Borg 1-10 Scale) were recorded at 5-minute intervals.

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PARTICIPANT DESCRIPTION

Participant 1

Participant 1 (L.A.) was a 61-year-old woman, with a diagnosis of PD made in 1999. She received a deep brain stimulator placed in the subthalamic nucleus in 2011 for management of severe dyskinesia. Aside from a total knee replacement in 2011, she had no other significant medical history. Throughout the course of this project, L.A.'s PD was medically managed with carbidopa and levodopa (Sinemet CR, 50-200 mg, 15 tablets per day; and Sinemet, 25-100 mg, 2 tablets, 5 times per day). Her baseline MoCA score was 17 of 30, which categorized her as having dementia.

L.A. was employed as an eligibility reviewer, whose job role was to determine the eligibility of applicants and recipients for public assistance programs. She had functioned in this role for more than 17 years; however, because of her cognitive decline, her direct work with clients had been limited over the past 2 years. At the start of this study, her main job responsibilities included clerical work, such as answering phones, filing papers, stocking supplies in her office, and interoffice mail delivery. Occasionally, she would be asked to interview clients on the phone to complete or review eligibility application forms. L.A. reported involvement with approximately 30 clients at the start of this study. L.A. lived in a home with her husband and adult daughter. She required 24-hour supervision from her family or a hired caretaker to safely carry out all activities of daily life, although she did not require physical assistance or the use of an assistive device for any mobility. She was no longer able to perform light or heavy household tasks, such as cleaning, laundry, and gardening. L.A. was no longer driving a car because of her poor attention. She had never exercised on a regular basis. See Table 1 for all baseline measures for L.A. At baseline, she accomplished the single-task serial subtraction task by subtracting in increments of 2.

Table 1

Table 1

L.A. attended all 24 intervention sessions. Initially, she required moderate assistance to mount the stationary bicycle. By the 19th session, she was able to mount the bicycle without any assistance or supervision. L.A.'s baseline cycling pace was 30 RPM. By the completion of the intervention, she had improved her pace to 48 RPM. L.A. chose to pedal without resistance by setting the stationary bicycle in the lowest 3 gears throughout all sessions. Cycling continuously for 40 minutes was challenging for L.A.. She initially required constant monitoring while cycling, as she would become distracted and stop pedaling after only 90 seconds. By the 17th session, she was able to cycle continuously for the full 40 minutes without requiring redirection to maintain her attention on the cycling task. Setting her own RPM goals at the start of each session motivated L.A.. She received constant RPM feedback displayed from the monitor on the stationary bicycle. L.A. became distracted by too much verbal feedback, so she was provided with encouragement and a reminder of her RPM goal at 5-minute intervals when her HR, blood pressure, and rate of perceived exertion measures were collected. While she was only able to reach her target HR for 15 of the 24 sessions, she did attain an HR that was greater than 55% of her estimated maximum HR across all 24 sessions. See Table 2 for the maximum HR L.A. achieved at each session as well as the average time she spent at her target HR across the 3 weekly sessions.

Table 2

Table 2

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Participant 2

Participant 2 (S.W.) was a 72-year-old man, with a diagnosis of PD made in 2007. S.W.'s medical history was significant for atrial fibrillation diagnosed in 2005. This was medically managed with Amiodarone until 2007 when the condition was resolved following a cardiac ablation. Since that time, S.W. has no longer been followed for atrial fibrillation, and no other cardiac condition was identified. Throughout the course of this project, S.W.'s PD was medically managed with rasagiline mesylate (Azilect, 1 mg, once per day), caridopa-levidopa (Sinemet 1.5 g, 3 times per day), ropinirole (Requip, 1 mg, once per day). He received a 22 of 30 on the MoCA at baseline, categorizing him as having mild cognitive impairments.

S.W. was a retired engineer, and before his diagnosis, he was a marathon runner and avid hiker and skier. S.W. reported that he stopped exercising after his PD was diagnosed and, in the months before starting this aerobic exercise program, was not engaged in any formal exercise program. S.W. lived alone, was independent for all mobility tasks without an assistive device, and was able to drive. At his baseline assessment, he reported his most distressing symptoms of PD to be excessive daytime drooling and frequent leg cramps. In addition, he felt limited in his participation as a grandfather, as he was unable to take his grandchildren camping because he could not carry a large backpack or walk uphill. See Table 1 for all of S.W.'s baseline measures. Note that S.W. was able to complete the serial subtraction by increments of 7 at baseline.

S.W. attended 22 of 24 sessions. Unlike L.A., he did not have any difficulty transferring onto the bicycle or cycling for the full 40 minutes. S.W. also did not require any redirection to maintain his focus on the cycling task. His baseline RPM was 79 and he was able to pedal consistently at a pace of at least 90 RPM following his sixth session. As he began to feel comfortable cycling at 90 RPM, S.W. applied resistance on the bicycle by increasing the gears. While he began pedaling in the lowest gear (1/24) at session 1, he was able to pedal in gear 6 for the full 40 minutes by session 22. At the request of S.W., the first author (R. T.) would cycle alongside him, as he found that this motivated him to cycle faster. He would ask for his target HR before the start of each session and requested feedback of his HR when it was collected at each 5-minute interval. S.W. was able to reach his target HR at every session. See Table 2 for the maximum HR S.W. achieved at each session as well as the average time he spent at his target HR across the 3 weekly sessions.

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OUTCOMES

To control for the potential influence of PD medications on the outcomes measured, pre- and postintervention assessments for each participant were performed at the same time of the day. This time was selected at the start of the study by the participant and was identified to be the time they felt the optimal effects of their PD medications. Pre- and postintervention assessments were performed by the same reviewer.

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Participant 1—L.A.

L.A. improved on all measures of executive function. See Table 1 for specific scores attained on all primary and secondary measures. Pre- and postintervention MoCA scores are graphed with score interpretation in Figure 1. L.A.'s dual-task cost is graphed in Figure 2a to demonstrate her concurrent improvements in both the motor and cognitive components of the dual walking and serial subtraction task. While her change in gait speed did not exceed the natural variability of this measure of gait speed for PD,40 her FGA score improved from 13 of 30 to 23 of 30, no longer categorizing her as a fall risk.39 L.A.'s change on the PDQ-39 surpassed values reported41 to be clinically important for the subcategories of cognition, emotional well-being, and bodily discomfort. Likewise, her change on the UPDRS exceeded the value reported to represent clinically important change.42

Figure 1

Figure 1

Figure 2

Figure 2

L.A. subjectively reported that her mood improved as a result of the exercise, further describing her mood as less pessimistic about her future and less angry. She arrived to her final cycling session reporting that she had been given increased client responsibilities at work, with a caseload of 120 clients to manage. L.A. was expected to have greater interactions with clients, including face-to-face interviews. She was also given the responsibility of determining appropriate programs for clients, which she had not been allowed to do for 2 years. These greater responsibilities were given to her after her supervisors noticed improved performance in her clerical tasks. Her clerical work had been decreased to allow her to maintain a higher caseload.

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Participant 2—S.W.

S.W. also improved on all measures of executive function. See Table 1 for S.W.'s scores on all primary and secondary postintervention measures. The results of his pre- and postintervention MoCA are graphed with score interpretation in Figure 1. Figure 2b demonstrates S.W.'s improved performance for both the cognitive and motor components of dual walk and serial subtraction task. S.W.'s decrease in his gait speed was smaller than the natural variability of this measure.40 S.W.'s PDQ-39 score increased from a 7 to 13. His largest changes were within the mobility subcategory. Further inquiry into this decline revealed that he was attempting to perform more challenging tasks that he would not have attempted before beginning this study and, therefore, was experiencing more difficulty in his every day task performance. S.W.'s change on the UDPRS-2 surpassed values reported to be meaningful.42 S.W. reported at his postintervention assessment that he no longer had problems with daytime drooling and his painful leg cramps had resolved. In addition, he had scheduled a camping trip with 2 of his grandchildren.

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DISCUSSION

The purpose of this case series was to describe changes in executive functioning associated with participation in an 8-week aerobic exercise program in 2 individuals with PD cognitive impairments. To our knowledge, this is the first study that describes improved executive function in persons with PD in association with aerobic exercise. While these results support previous studies29–31 of exercise-induced executive function changes in people with PD, our study differed in 2 ways. First, we used an aerobic-only intervention. Cruise et al,30 included both resistance training and 30 minutes of aerobic exercise performed between 60% to 85% of estimated maximum HR in each of their 24 intervention sessions. While the focus of the intervention conducted in the study by Tanaka et al29 was on coordination, muscular resistance, and balance training, participants maintained an HR of 60% to 80% of their estimated maximum HR throughout each 1-hour session. The aerobic components of these 2 studies29,30 may have been sufficiently similar to that in our study in intensity and duration to produce similar effects on executive function. Importantly, the participants in our case series demonstrated cognitive impairment as measured by the MoCA before the intervention, whereas all other accounts of exercise-induced changes were measured in individuals with PD who did not demonstrate cognitive impairment.

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Changes in Secondary Measures for L.A. and S.W.

Existing evidence44 supports the ability of people with PD to improve dual-task performance through training. Both participants in this case series demonstrated improved dual-task performance following the aerobic training, which is consistent with the findings of the case study by Nocera et al.31 The improved ability to dual task for L.A. may be associated with the large improvement observed in the FGA score. Two items on the FGA grade a person's ability to change speed and to turn in place at the moment he or she is given a verbal command. Two additional items require that the person count his or her steps and perform a head turn after every third step. The coordination of walking while listening for a cue or walking while counting steps in preparation to perform a secondary task may be very challenging for an individual with impaired cognition. In our case series, this task was challenging for participant 1, who at baseline was categorized as having dementia. Therefore, the improvements in L.A.'s FGA score may be more related to her ability to perform a dual task and less likely associated with any improvements to her postural stability or motor performance as no balance intervention was provided. These findings suggest that improving cognition may help to improve balance for people with PD who also have dementia.

Both participants in this case series demonstrated improvements in the combined score of UPDRS 1 and 2, with values surpassing what has been reported to be clinically meaningful.42 L.A. also demonstrated improvement in her PDQ-39. The results of this case series add to the existing literature45,46 that reports a positive effect of aerobic-based exercise on quality of life in people with PD.

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LIMITATIONS

Despite the favorable outcomes reported, our case series design prevents us from drawing conclusions about the impact of aerobic exercise on executive function in people with PD. Likewise, no inference of causality between improved executive function and improved measures of balance or disease severity can be made. The inherent design of any case series creates a selection bias that must be taken into consideration when reviewing outcomes. The authors acknowledge that some improvements recorded may have been related to the consistent interaction that both participants had with the physical therapist leading each session. This social interaction may have improved the participants' mood or desire to perform better on our outcome measures. Finally, our case series lacked clear measurement of aerobic exercise dose, which could be obtained through use of a stress test to obtain maximum HR. As demonstrated by L.A.'s difficulty achieving the target of 75% maximal HR at the end of the study, higher HR zones may not be feasible for all people with PD. Knowledge of the minimum aerobic exercise dose needed to produce similar outcomes is imperative for the clinical application of our findings.

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DIRECTIONS FOR FUTURE RESEARCH

Larger studies with a control group are warranted to confirm these outcomes. Future studies should focus on the necessary and optimal dose of aerobic exercise needed to produce meaningful improvements in executive function. In this case series, while improvements in measures of executive function, quality of life, as well as balance were demonstrated, a larger study would allow for investigation into the causal relationship between aerobic exercise and improved cognition, balance, and quality of life measures. Future research should also determine whether aerobic exercise is more effective than other forms of exercise for improving cognition in people with PD.

There is a need to better understand central mechanisms that may be responsible for the improvements observed in executive function following exercise. Significant increases in brain volume of healthy older adults following aerobic exercise have been reported.47 Likewise, multiple animal studies48–50 have revealed angiogenesis occurring in the brain following aerobic exercise. Both diminished brain volume51 and decreased blood flow52 in the brain of individuals with PD have been observed. Recognition that brain volume increases and/or angiogenesis may occur in individuals with PD in response to aerobic exercise, with parallel improvement in executive function, suggests potential disease-modifying effects of aerobic exercise.

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ACKNOWLEDGMENTS

The authors thank Dr E Todd Schroeder for providing the equipment and space needed to complete this project and Dr Giselle Petzinger for her assistance with recruitment and mentorship provided throughout this research process.

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Keywords:

cognition; cycling; dual-task performance; wellness

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