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Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Can exercise improve language and cognition in Parkinson's disease? A case report Joe R. Nocera
a b
& Chris J. Hass
c
, Lori J. P. Altmann , Christine Sapienza
b c
, Michael S. Okun
a d
b e
a
Department of Neurology, University of Florida, Gainesville, FL, USA
b
Brain Rehabilitation Research Center, Malcom Randall VAMC, Gainesville, FL, USA
c
Department of Communicative Disorders, University of Florida, Gainesville, FL, USA d
Department of Neurosurgery, University of Florida, Gainesville, FL, USA
e
Department of Applied Physiology & Kinesiology, University of Florida, Gainesville, FL, USA Version of record first published: 12 Apr 2010
To cite this article: Joe R. Nocera, Lori J. P. Altmann, Christine Sapienza, Michael S. Okun & Chris J. Hass (2010): Can exercise improve language and cognition in Parkinson's disease? A case report, Neurocase: The Neural Basis of Cognition, 16:4, 301-306 To link to this article: http://dx.doi.org/10.1080/13554790903559663
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NEUROCASE 2010, 16 (4), 301–306
Can exercise improve language and cognition in Parkinson’s disease? A case report
NNCS
Exercise and Cognition
Joe R. Nocera,1,2 Lori J. P. Altmann,3 Christine Sapienza,2,3 Michael S. Okun,1,4 and Chris J. Hass2,5 1Department
of Neurology, University of Florida, Gainesville, FL, USA Rehabilitation Research Center, Malcom Randall VAMC, Gainesville, FL, USA 3Department of Communicative Disorders, University of Florida, Gainesville, FL, USA 4Department of Neurosurgery, University of Florida, Gainesville, FL, USA 5Department of Applied Physiology & Kinesiology, University of Florida, Gainesville, FL, USA
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2Brain
Parkinson’s disease is commonly accompanied by cognitive issues that limit participation in activities of daily living. Unfortunately, most current treatment paradigms and pharmacotherapeutics fail to address the cognitive impairment demonstrated in this population. Mounting evidence in healthy older adults suggests that aerobic exercise may improve cognitive function. This article describes a patient with Parkinson’s disease prescribed 8 weeks of aerobic exercise. Despite very high performance at baseline, the participant improved on several cognitive measures post exercise. The results of this investigation mimic the research in healthy older adults. We therefore suggest that future large scale randomized trials are warranted to evaluate the efficacy of aerobic exercise for ameliorating declines in cognitive performance in persons with PD. Keywords: Cognition; Aerobic exercise; Neurological disease; Parkinson’s disease.
INTRODUCTION The neuropsychological consequences of Parkinson’s disease (PD) have become increasingly well recognized (Taylor & Saint-Cyr, 1995; Zgaljardic, Borod, Foldi, & Mattis, 2003). These cognitive disturbances most commonly affect executive functions, including situations that require planning, cognitive flexibility, and multi-tasking (Taylor & Saint-Cyr, 1995). Further, activities of daily living are often performed under conditions which require the simultaneous performance of cognitive function and motor tasks. Thus, even slight or subtle declines in cognitive function may impact performance of routine activities. Indeed, performance of concurrent tasks (cognitive and motor or two motor tasks) produces a significant
deterioration in postural stability and gait performance and increases the risk for falls in individuals with PD (Morris, Iansek, Smithson, & Huxham, 2000). Unfortunately, current interventions that ameliorate motor manifestations of PD do not adequately address, or significantly impact cognitive deficits. Dopaminergic therapy, for example, significantly improves motor function, while the effects on cognitive function are dissociated (Growdon et al., 1998). Further, deep brain stimulation, which produces substantial motor benefits in some patients, may have deleterious effects on cognitive function (Woods, Fields, & Tröster, 2002). Thus, there is a growing need for development of therapies that not only treat motor dysfunction but also the cognitive sequelae in PD.
Address correspondence to Joe R. Nocera, Department of Applied Physiology and Kinesiology, University of Florida, PO Box 118205, Rm 151 Florida Gym, Gainesville, FL 32611, USA. (E-mail:
[email protected]).
© 2010 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business http://www.psypress.com/neurocase DOI: 10.1080/13554790903559663
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Mounting evidence from research on healthy older adults suggests that aerobic exercise may not only improve physical health, but also overall brain health and cognitive function (Colcombe & Kramer, 2003; Colcombe et al., 2006; Hillman, Weiss, Hagberg, & Hatfield, 2002; Kramer, Colcombe, McAuley, Scalf, & Erickson, 2005; Kramer et al., 1999). Cross-sectional studies have demonstrated a reduction in age-related declines in cortical tissue density in older adults with high fitness capacity. The greatest neuroprotective effects appear to be localized to the frontal and prefrontal areas of the brain (Colcombe et al., 2006; Kramer et al., 1999) which support cognitive/executive function. This finding is meaningful because these areas typically demonstrate the greatest age-related decline both structurally and in terms of cognitive/executive performance (Raz, 2000). Additionally, Kramer et al. (1999) reported that aerobic training can produce substantial improvements in performance on tasks requiring executive control. Importantly, these cortical areas and their associated cognitive functions are exactly those impaired in PD (Taylor & Saint-Cyr, 1995). Although the effects of aerobic exercise on the physical and cognitive well-being of healthy older adults are pronounced, it cannot be assumed that the effect is identical in PD. To the best of our knowledge, to date no exercise interventions aimed at improving cognition in PD have been published. Cognitive deficits in PD have proven resistant to other PD interventions (Woods et al., 2002). Furthermore, it is unknown whether the altered neuroanatomy and neurochemical environment in the frontal lobes of individuals with PD might limit therapeutic benefits of aerobic exercise. Therefore, the present case study assessed the effects of 8 weeks of aerobic exercise training on the cognitive performance of a person with idiopathic PD. Our battery also assessed complex language production as an example of a functional cognitive task tapping both executive function and working memory resources (Kemper & Sumner, 2001; Murray & Lenz, 2001). Additionally, to improve the ecological validity of the study, we assessed performance utilizing both single and dual task paradigms to increase the challenge on executive resources.
METHODS Participant The patient presented was a screened participant in a randomized controlled trial (RCT) comparing
the effects of two forms of exercise training on locomotor performance in people with early to mid-staged PD. To be included in the RTC, participants had to be able to ambulate without an assistive device. Participants were excluded if they had on-state freezing or exercise was limited by musculoskeletal, neurological (other than PD), and cardiovascular factors. Further, participants were excluded if they had participated in regular progressive exercise within the last 1 year. Before participating in the study, each participant signed an informed consent form that had been approved by the University of Florida Institutional Review Board. Similar to other participants in the RCT, this patient was recruited from the Movement Disorders Center at the University of Florida. She was being treated with stable doses of dopaminomimetics and was tested and exercised while clinically in an on-state, or fully responsive to her PD medications. Measurements and exercises were done at the same time of day and the participant was asked to take her medication at the same time of day throughout testing. Additionally, like all participants in the RCT, she was rated using the Unified Parkinson’s Disease Rating Scale (UPDRS) and the modified Hoehn and Yahr (H & Y). The UPDRS is designed to follow the longitudinal course of the disease and considered the gold standard for quantifying signs and symptoms of PD. It is made up of four sections: (1) Mentation, Behavior, and Mood, (2) Activities of Daily Living, (3) Motor, and (4) complications of therapy. These sections are evaluated by interview and as the disease progresses, UPDRS scores increase (106 maximum). The H & Y, a subsection of the UPDRS, is used to determine stage (1–5) of PD. This particular participant is described because due to schedule constraints she was unable to participate in the group classes of either arm of the RCT. As a result her neurologist prescribed her monitored aerobic exercise which was tracked throughout the intervention. The patient was a 66year-old right-handed female with idiopathic PD diagnosed, by a fellowship trained Movement Disorders neurologist, at stage 2 (bilateral disease without impairment of balance) of the H & Y scale and a score of 31 on the UPDRS. Her disease duration was 11 years and her antiparkinson medications included 3 times daily 1.5 mg Mirapex and 3 times daily 25 mg Sinemet. Non-PD medications included Aspirin and Vitamin B12.
EXERCISE AND COGNITION
Tests and measures
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The participant completed 2 days of cognitive/ language assessment prior to and following the exercise intervention. Single and dual task performance was assessed on separate days to reduce contamination due to practice effects, and mental and physical fatigue. During dual task trials, the participant pedaled on a stationary ergometer. Initially, the participant pedaled at a self-selected cadence which was recorded as baseline motor performance. After pedaling at this cadence for 30 s, the cognitive/language task commenced and was conducted concurrently with the cycling. Materials The Mini-Mental Status Examination (Folstein, Folstein, & McHugh, 1975) and Stroop (Elias & Treland, 1999) were given solely in the single task condition because they would have required considerable alteration from the validated methods to be used concurrently with the motor task. Cognitive tasks performed in both single and dual task conditions included verbal fluency using animals and letter cues (letters: F,A,S), digit span forward and digit span backward, which capture proficiencies in executive function, verbatim memory, and working memory, respectively (Wechsler, 1987). We utilized a picture description task in both single and dual task settings to examine language function. The participant viewed a series of line drawings on a projection screen and was asked to produce one sentence describing each picture. Different but equivalent pictures were utilized at each test segment. Pictures showed from one to three actors involved in various interactions to encourage the production of different types of sentences (Bock, Loebell, & Morey, 1992; Troche Altmann, Rosenbek, & Sapienza, 2008). Responses were digitally recorded, transcribed verbatim, and scored by a trained psycholinguist. Responses were scored for number of words, comments, dysfluencies, grammatical sentences, propositions, gist meaning, and extraneous comments. Exercise intervention The individual performed 20 min of aerobic exercise three times a week for 8 weeks on a stationary exercise cycle. Exercise intensity began at low levels (50% of maximal heart rate reserve (HRRmax))
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and increased by 5% every week to a maximum of 75% HRRmax. Each exercise session was monitored by a clinical exercise physiologist.
RESULTS AND DISCUSSION In this open label study, 8 weeks of aerobic exercise improved several measures of cognitive function (Table 1). Specifically, performance on the Stroop color X’s and color words improved by 31 and 20%, respectively. Verbal fluency (animals) also significantly improved (11–23 words) following training in the single task setting. However, verbal fluency (letters: F,A,S), showed only minimal improvement. Although there was no improvement in verbatim memory (which was in the high normal range at pretest), there was considerable improvement in working memory. These improvements paralleled those reported in the healthy older adult literature in which tasks measuring executive function benefit most from aerobic exercise (Colcombe & Kramer, 2003; Kramer et al., 1999). Baseline responses on the picture description task were extremely long, contained many extraneous comments (e.g., they all look very happy), and were less focused (i.e., greater number of words per proposition), particularly in the dual task condition. Post-intervention, responses were more concise while still capturing gist meaning, and a greater proportion of responses were grammatical. Fluency was explored in two ways, using the proportion of responses that were fluent and using the total number of dysfluencies per response. The proportion of fluent responses improved only in the single task condition at post-test; however, the total number of dysfluencies per sentence decreased in both the single and dual task setting at post-test. This reflects the fact that many of pretest responses included several dysfluencies, while this was rare at post-test. Exercise training improved motor output during both single and dual task conditions. Collectively, during all dual task paradigms, motor output improved approximately 50% following the intervention. Equally important, the dual task effect, (the decline in performance due to the simultaneous performance of another task), decreased at post-test (Figure 1). Studies examining the effects of exercise on dual task performance have reported mixed results. Melzer, Marx, and Kurz (2008) recently reported that a history of regular exercise
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NOCERA ET AL. TABLE 1 Pre and post-test scores in the single and dual task conditions Dual task2
Dual task RPM3
Task
Pre
Post
Pre
Post
RPM mean4 MMSE (max 30)4 Stroop Color XXX4 Stroop Color Words4 Verbal Fluency (animals)4 Verbal Fluency (Letters: F,A,S)4 Digit Span Forward (max 14)4 Digit Span Backward (max 14)4
39 30 66 40 11 37 11 6
60 30 87 48 23 40 9 9
– – – – 12 38 12 5
– – – – 10 38 11 7
Picture Description4 Total Words5 Words per Sentence5 Words per Proposition5 Proportion Grammatical4 Proportion Fluent4 Dyfluencies per Sentence5 Proportion with Gist Meaning4 Extraneous Comments5
383 15.96 2.90 0.88 .58 .67 0.92 7
335 13.96 2.82 0.83 .71 .29 1.00 1
325 13.54 3.42 0.75 .58 .38 0.95 7
Pre
Post
32.7 – – – 34 33.7 34 32
58.5 – – – 56 58.7 65 57
30
56
292 12.17 2.75 0.92 .58 .29 1.00 3
1Indicates
the scores for each task while performing the given task in a single task setting. the scores for each task while performing the given task and a secondary motor task. 3Dual Task RPM indicates the revolutions per minute while performing the given cognitive task. 4 Indicates a higher score is advantageous. 5 Indicates a lower score is advantageous. 2Indicates
Avg. RPM during single and dual tasks conditions 70 60
RPM
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Single task1
50
Single
40
Dual
30 20 Pre
Post
Figure 1. Average RPM (revolutions per minute) and error bars in both the single and dual task conditions (RPM’s averaged across: Verbal Fluency, animals and letters: F,A,S; Digits Forward and Backwards; and the Picture Description task). In the single task setting the average motor output improved from 39 RPM’s pre training to 60 RPM’s post training. Similarly, in the dual task condition average motor output improved from 32.7 RMP’s pre training to 58.5 RPM’s post training. Equally important, the dual task cost (decline in motor output in the presence of a secondary task), decreased at post test with the average decline reducing from 6.3 RPM’s pre training to 1.5 RPM’s post training.
including tai chi, Feldenkrais, aerobic training and strength improve stepping performance conditions (performance on a
balance training, training did not during dual task modified Stroop)
compared to sedentary controls. However, this study relied on self-reported exercise history, rather than an actual exercise program. Conversely, Albinet, Bernard, and Palut (2006) reported that a physical activity program allowed elderly subjects to improve their ability to perform an attentiondemanding cognitive task while standing still with their eyes closed. In the Albinet study participants completed a 12-week, twice weekly, physical activity program focusing on posture, balance and mobility. Therefore, the demonstrated improvement during the dual paradigm in the Albinet study as well as this case report may be the result of a more efficient use of motor system as well as improved cognitive function brought on by the adaptation of a structured exercise program. Herein we provide novel evidence that cognitive and language function in individuals with PD may improve following an aerobic exercise intervention. The participant in this open label case study demonstrated improvements in executive function, working memory, and language production following intervention. Moreover, motor output improved considerably in single and dual task conditions. Although preliminary, these results may have two important implications. First, these findings suggest
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EXERCISE AND COGNITION
that aerobic exercise may be an effective intervention to improve executive function, working memory and communication in persons with PD. Importantly, these deficits often do not respond to pharmacological or surgical interventions. Furthermore, exercise is relatively inexpensive, non-invasive and unlikely to interact with other treatments, while also improving physical wellbeing. However, it is currently unknown whether the cognitive changes documented are specific to tasks that require executive function and working memory or whether they represent general changes in cognitive function. An additional implication is that regular aerobic exercise may make a particular motor task more resistant to interference from competing cognitive tasks in individuals with PD. However, it is unknown whether this effect will generalize to other motor tasks such as walking. Future studies will need to examine the effects of exercise and will need to employ more rigorous methodology to minimize the limitations of the current case study. For example, using different motor tasks for assessment and training would allow the researcher to disentangle the improvements due to practice on the training task and improvements due to increased efficiency of cognitive function. For this preliminary study, the cycling ergometer was utilized in this study during the dual task evaluation to minimize possibility of falls during concurrent tasks which is often demonstrated in PD. Similarly, the issue of improved performance due to practice/learning effects demonstrated during repeated administration of cognitive testing cannot be ignored. However, we believe that learning effects were minimized based on (1) improvements demonstrated in areas not typically known for demonstrating a learning effect (e.g., digits backward, verbal fluency), (2) improvements in single task but not dual task performance (e.g., verbal fluency, and fluency in the language production tasks), and (3) improvements on the complex language task utilized as a functional measure that taps both executive function and working memory. Moreover, future studies would obviously benefit from larger groups of individuals with PD and the use of a delayed treatment group to control for possible practice effects. Finally, future research in general will need to address the specific mechanisms of recovery, and examine how physical activity promotes neurochemical, structural and/or behavioral changes that impact plasticity and cognitive function in the PD model.
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Original manuscript received 17 October 2008 Revised manuscript accepted 16 September 2009 First published online 12 April 2010
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