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Aerobic Exercise Improves Mood, Cognition, and Language Function in Parkinson’s Disease: Results of a Controlled Study

Published online by Cambridge University Press:  22 September 2016

Lori J.P. Altmann*
Affiliation:
Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, Florida Department of Speech, Language, and Hearing Sciences, University of Florida, Gainesville, Florida
Elizabeth Stegemöller
Affiliation:
Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, Florida Department of Kinesiology, Iowa State University, Ames, Iowa
Audrey A. Hazamy
Affiliation:
Department of Department of Speech Communication Arts and Sciences, Brooklyn College, Brooklyn, New York
Jonathan P. Wilson
Affiliation:
Department of Speech-Language Pathology, Midwestern University, Downers Grove, Illinois
Dawn Bowers
Affiliation:
Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida
Michael S. Okun
Affiliation:
Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, Florida Department of Neurology and Neurosurgery, University of Florida, Gainesville, Florida
Chris J. Hass
Affiliation:
Center for Movement Disorders and Neurorestoration, University of Florida, Gainesville, Florida Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, Florida
*
Correspondence and reprint requests to: Lori J. P. Altmann, Box 100174, 1220 Center Drive, University of Florida, Gainesville, FL 32610-0174. E-mail: laltmann@ufl.edu

Abstract

Objectives: Parkinson’s disease (PD) results in a range of non-motor deficits that can affect mood, cognition, and language, and many of these issues are unresponsive to pharmacological intervention. Aerobic exercise can improve mood and cognition in healthy older adults, although only a few studies have examined exercise effects on these domains in PD. The current study assesses the effects of aerobic exercise on aspects of cognition, mood, and language production in people with PD. Methods: This study compares the effects of aerobic exercise to stretch-balance training and a no-contact control group in participants with idiopathic PD. The aerobic and stretch-balance groups trained three times a week for 16 weeks, while controls continued normal activities. Outcome measures included disease severity, mood, cognition (speed of processing, memory, and executive function), and language production (picture descriptions). Cognition and language were assessed in single and dual task conditions. Results: Depressive symptoms increased only in the control group (p<.02). Executive function improved in the aerobic exercise group only in the single task (p=.007) and declined in controls in the dual task. Completeness of picture descriptions improved significantly more in the aerobic group than in the stretch-balance group (p<.02). Conclusions: Aerobic exercise is a viable intervention for PD that can be protective against increased depressive symptoms, and can improve several non-motor domains, including executive dysfunction and related aspects of language production. (JINS, 2016, 22, 878–889)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

REFERENCES

Aarsland, D., Andersen, K., Larsen, J.P., Lolk, A., & Kragh-Sorensen, P. (2003). Prevalence and characteristics of dementia in Parkinson disease: An 8-year prospective study. Archives of Neurology, 60(3), 387392.CrossRefGoogle ScholarPubMed
Altmann, L.J.P., Stegemöller, E., Hazamy, A.A., Wilson, J.P., Okun, M.S., McFarland, N.R., & Hass, C.J. (2015). Unexpected dual task benefits on cycling in Parkinson disease and healthy adults: A neuro-behavioral model. PLoS One, 13, e0125470. doi:10.1371/journal.pone.0125470 CrossRefGoogle Scholar
Altmann, L.J.P., & Troche, M.S. (2011). High-level language production in Parkinson’s disease: A review. Parkinon’s Disease, 2011, 238956. doi:10.4061/2011/238956 Google ScholarPubMed
American Parkinson’s Disease Association. (2009). Be active. Retrieved from http://www.apdaparkinson.org/uploads/files/Be-Active-Book_For-Web-90o.pdf.Google Scholar
Anderson-Hanley, C., Arciero, P.J., Brickman, A.M., Nimon, J.P., Okuma, N., Westen, S.C., & Zimmerman, E.A. (2012). Exergaming and older adult cognition: A cluster randomized clinical trial. American Journal of Preventive Medicine, 42(2), 109119. doi:http://dx.doi.org/10.1016/j.amepre.2011.10.016.CrossRefGoogle ScholarPubMed
Barone, P., Antonini, A., Colosimo, C., Marconi, R., Morgante, L., Avarello, T.P., & Ceravolo, R. (2009). The PRIAMO study: A multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson’s disease. Movement Disorders, 24(11), 16411649. doi:10.1002/mds.22643 CrossRefGoogle ScholarPubMed
Bastiaanse, R., & Leenders, K.L. (2009). Language and Parkinson’s disease. Cortex, 45, 912914.CrossRefGoogle ScholarPubMed
Bayles, K.A. (1990). Language and Parkinson disease. Alzheimer Disease and Associated Disorders, 4(3), 171180.CrossRefGoogle ScholarPubMed
Beck, A.T., & Steer, R.A. (1993). Beck Anxiety Inventory Manual. San Antonio, TX: Harcourt Brace and Company.Google Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Bland, W., Busam, V., Gunlogson, B., Mekkes, G., & Saunders, A. (2006). Audacity: A free digital audio editor (Version 1.2.6). Retrieved from http://audacity.sourceforge.net/: SourceForge.net.Google Scholar
Blumenthal, J.A., Babyak, M.A., Moore, K.A., et al. (1999). Effects of exercise training on older patients with major depression. Archives of Internal Medicine, 159(19), 23492356. doi:10.1001/archinte.159.19.2349 CrossRefGoogle ScholarPubMed
Bock, K., Loebell, H., & Morey, R. (1992). From conceptual roles to structural relations: Bridging the syntactic cleft. Psychological Review, 99(1), 150171. doi:10.1037/0033-295X.99.1.150 CrossRefGoogle ScholarPubMed
Bopp, K.L., & Verhaeghen, P. (2005). Aging and verbal memory span: A meta-analysis. The Journals of Gerontology: Series B: Psychological Sciences and Social Sciences, 60B(5), P223P233.CrossRefGoogle Scholar
Buysse, D.J., Reynolds, C.F., Monk, T.H., Berman, S.R., & Kupfer, D.J. (1989). The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatry Research, 28(2), 193213.CrossRefGoogle ScholarPubMed
Coelho, F.G., Andrade, L.P., Pedroso, R.V., Santos-Galduroz, R.F., Gobbi, S., Costa, J.L., & Gobbi, L.T. (2013). Multimodal exercise intervention improves frontal cognitive functions and gait in Alzheimer’s disease: A controlled trial. Geriatrics & Gerontology International, 13(1), 198203. doi:10.1111/j.1447-0594.2012.00887.x CrossRefGoogle ScholarPubMed
Colcombe, S.J., Erickson, K.I., Scalf, P.E., Kim, J.S., Prakash, R., McAuley, E., & Kramer, A.F. (2006). Aerobic exercise training increases brain volume in aging humans. The Journal so Gerontology. Series A, Biological Sciences and Medical Sciences, 61(11), 11661170.CrossRefGoogle ScholarPubMed
Colman, K.S.F., Koerts, J., van Beilen, M., Leenders, K.L., Post, W.J., & Bastiaanse, R. (2009). The impact of executive functions on verb production in patients with Parkinson’s disease. [Research Support, Non-U.S. Gov’t]. Cortex, 45(8), 930942. doi:10.1016/j.cortex.2008.12.010 CrossRefGoogle ScholarPubMed
Conway, A.R.A., Kane, M.J., Bunting, M.F., Hambrick, D.Z., Wilhelm, O., & Engle, R.W. (2005). Working memory span tasks: A methodological review and user’s guide. [Review]. Psychonomic Bulletin & Review, 12(5), 769786.CrossRefGoogle ScholarPubMed
Cooper, J.A., Sagar, H.J., Jordan, N., Harvey, N.S., & Sullivan, E.V. (1991). Cognitive impairment in early, untreated Parkinson’s disease and its relationship to motor disability. Brain, 114(5), 20952122.CrossRefGoogle ScholarPubMed
Cotman, C.W., & Berchtold, N.C. (2002). Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neurosciences, 25(6), 295301.CrossRefGoogle Scholar
Cruise, K.E., Bucks, R.S., Loftus, A.M., Newton, R.U., Pegoraro, R., & Thomas, M.G. (2010). Exercise and Parkinson’s: Benefits for cognition and quality of life. Acta Neurologica Scandinavica, 123, 1319. doi:10.1111/j.1600-0404.2010.01338.x CrossRefGoogle Scholar
Cummings, J.L., Darkins, A., Mendez, M., & Hill, M.A. (1988). Alzheimer’s disease and Parkinson’s disease: Comparison of speech and language alterations. Neurology, 38(5), 680684.CrossRefGoogle ScholarPubMed
David, F.J., Robichaud, J.A., Leurgans, S.E., Poon, C., Kohrt, W.M., Goldman, J.G., & Corcos, D.M. (2015). Exercise improves cognition in Parkinson’s disease: The PRET‐PD randomized, clinical trial. Movement Disorders, 30, 16571663. doi:10.1002/mds.262 CrossRefGoogle ScholarPubMed
Dishman, R.K., Berthoud, H.R., Booth, F.W., Cotman, C.W., Edgerton, V.R., Fleshner, M.R., & Zigmond, M.J. (2006). Neurobiology of exercise. Obesity (Silver Spring, Md), 14(3), 345356. doi:10.1038/oby.2006.46 CrossRefGoogle ScholarPubMed
Emre, M. (2003). What causes mental dysfunction in Parkinson’s disease? Movement Disorders, 18(S6), 6371.CrossRefGoogle ScholarPubMed
Erickson, K.I., Voss, M.W., Prakash, R.S., Basak, C., Szabo, A., Chaddock, L., & Kramer, A.F. (2011). Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences of the United States of America, 108(7), 30173022. doi:10.1073/pnas.1015950108 CrossRefGoogle ScholarPubMed
Eriksen, B.A., & Eriksen, C.W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Perception & Psychophysics, 16(1), 143149.CrossRefGoogle Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189198. doi:10.1016/0022-3956(75)90026-6 CrossRefGoogle Scholar
Fougnie, D., & Marois, R. (2006). Distinct capacity limits for attention and working memory: Evidence from attentive tracking and visual working memory paradigms. Psychological Science, 17(6), 526534. doi:10.1111/j.1467-9280.2006.01739.x CrossRefGoogle ScholarPubMed
Fournet, N., Moreaud, O., Roulin, J.L., Naegele, B., & Pellat, J. (2000). Working memory functioning in medicated Parkinson’s disease patients and the effect of withdrawal of dopaminergic medication. [Comparative Study]. Neuropsychology, 14(2), 247253.CrossRefGoogle ScholarPubMed
Godin, G., & Shephard, R. (1997). Godin leisure-time exercise questionnaire. Medicine and Science in Sports and Exercise, 29(6), 3638.Google Scholar
Goetz, C.G., Fahn, S., Martinez-Martin, P., Poewe, W., Sampaio, C., Stebbins, G.T., & LaPelle, N. (2007). Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Process, format, and clinimetric testing plan. Movement Disorders, 22(1), 4147. doi:10.1002/mds.21198 CrossRefGoogle ScholarPubMed
Harrison, D.J., Busse, M., Openshaw, R., Rosser, A.E., Dunnett, S.B., & Brooks, S.P. (2013). Exercise attenuates neuropathology and has greater benefit on cognitive than motor deficits in the R6/1 Huntington’s disease mouse model. Experimental Neurology, 248, 457469.CrossRefGoogle ScholarPubMed
Hoehn, M., & Yahr, M.D. (1967). Parkinsonisam: Onset, progression and mortality. Neurology, 17, 427442.CrossRefGoogle ScholarPubMed
Jarvis, B. (2006a). DirectRT. New York: Empirisoft.Google Scholar
Jarvis, B. (2006b). MediaLab. New York: Empirisoft.Google Scholar
Jones, J.D., Butterfield, L.C., Song, W., Lafo, J., Mangal, P., Okun, M.S., & Bowers, D. (2015). Anxiety and depression are better correlates of Parkinson’s disease quality of life than apathy. The Journal of Neuropsychiatry and Clinical Neurosciences, 27(3), 213218. doi:10.1176/appi.neuropsych.13120380 CrossRefGoogle ScholarPubMed
Jones, J.D., Malaty, I., Price, C.C., Okun, M.S., & Bowers, D. (2012). Health comorbidities and cognition in 1948 patients with idiopathic Parkinson’s disease. Parkinsonism & Related Disorders, 18(10), 10731078. doi:10.1016/j.parkreldis.2012.06.004 CrossRefGoogle ScholarPubMed
Jones, J.D., Marsiske, M., Okun, M.S., Bowers, D., Jones, J.D., Butterfield, L.C., & Bowers, D. (2015). Latent growth-curve analysis reveals that worsening Parkinson’s disease quality of life is driven by depression. Neuropsychology, 29(4), 603609. doi:10.1037/neu0000158 CrossRefGoogle ScholarPubMed
Kahneman, D. (1970). Remarks on attentional control. In A.F. Sanders (Ed.), Attention and performance III (pp. 118131). Amsterdam: North Holland Publishing Co.Google Scholar
Kempler, D. (2003). Kempler Sentence Comprehension Task. Boston: Emerson College.Google Scholar
Leentjens, A.F.G. (2004). Depression in Parkinson’s disease: Conceptual issues and clinical challenges. [Review]. Journal of Geriatric Psychiatry and Neurology, 17(3), 120126. doi:10.1177/0891988704267456 CrossRefGoogle ScholarPubMed
Lezak, M.D., Howieson, D.B., Loring, D.W., Hannay, H.J., & Fischer, J.S. (2004). Neuropsychological assessment ((4th ed.), New York, NY: Oxford University Press.Google Scholar
Little, T.D., Rhemtulla, M., Gibson, K., & Schoemann, A.M. (2013). Why the items versus parcels controversy needn’t be one. Psychological Methods, 18(3), 285.CrossRefGoogle ScholarPubMed
Marin, R.S., Biedrzycki, R.C., & Firinciogullari, S. (1991). Reliability and validity of the Apathy Evaluation Scale. Psychiatry Research, 38(2), 143162.CrossRefGoogle ScholarPubMed
Martinez‐Martin, P., Rodriguez‐Blazquez, C., Kurtis, M.M., & Chaudhuri, K. (2011). The impact of non‐motor symptoms on health‐related quality of life of patients with Parkinson’s disease. [Multicenter Study]. Movement Disorders, 26(3), 399406. doi:10.1002/mds.23462 CrossRefGoogle ScholarPubMed
Mattis, S. (1988). Dementia Rating Scale: Professional manual. Odessa, FL: Psychological Assessment Resources.Google Scholar
Murray, L.L. (2000). Spoken language production in Huntington’s and Parkinson’s diseases. Journal of Speech, Language, and Hearing Research, 43(6), 13501366. doi:10.1044/jslhr.4306.1350 CrossRefGoogle ScholarPubMed
Murray, L.L. (2008). Language and Parkinson’s disease. Annual Review of Applied Linguistics, 28, 113127. doi:10.1017/S0267190508080100 CrossRefGoogle Scholar
Nocera, J.R., Altmann, L.J.P., Sapienza, C., Okun, M.S., & Hass, C.J. (2010). Can exercise improve language and cognition in Parkinson’s disease? A case report. Neurocase, 16(4), 301306.CrossRefGoogle ScholarPubMed
Nystrom, L.E., Braver, T.S., Sabb, F.W., Delgado, M.R., Noll, D.C., & Cohen, J.D. (2000). Working memory for letters, shapes, and locations: fMRI evidence against stimulus-based regional organization in human prefrontal cortex. Neuroimage, 11(5 Pt 1), 424446.CrossRefGoogle ScholarPubMed
Owen, A.M., Iddon, J.L., Hodges, J.R., & Summers, B.A. (1997). Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia, 35(4), 519532. doi:10.1016/S0028-3932(96)00101-7 CrossRefGoogle ScholarPubMed
Parkinsons Disease Foundation. (2016). Statistics on Parkinson’s. Retrieved from http://www.pdf.org/en/ Accessed May 3, 2016.Google Scholar
Pirozzolo, F.J., Hansch, E.C., Mortimer, J.A., Webster, D.D., & Kuskowski, M.A. (1982). Dementia in Parkinson’s disease: A neuropsychological analysis. Brain and Cognition, 1, 7183.CrossRefGoogle ScholarPubMed
Saint-Cyr, J.A., Trepanier, L.L., Kumar, R., Lozano, A.M., & Lang, A.E. (2000). Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain, 123(Pt 10), 20912108.CrossRefGoogle ScholarPubMed
Skeel, R.L., Crosson, B., Nadeau, S.E., Algina, J., Bauer, R.M., & Fennell, E.B. (2001). Basal ganglia dysfunction, working memory, and sentence comprehension in patients with Parkinson’s disease. Neuropsychologia, 39(9), 962971.CrossRefGoogle ScholarPubMed
Slaughter, J.R., Slaughter, K.A., Nichols, D., Holmes, S.E., & Martens, M.P. (2001). Prevalence, clinical manifestations, etiology, and treatment of depression in Parkinson’s disease. [Review]. The Journal of Neuropsychiatry and Clinical Neurosciences, 13(2), 187196. doi:10.1176/jnp.13.2.187 CrossRefGoogle ScholarPubMed
Suzuki, T., Shimada, H., Makizako, H., Doi, T., Yoshida, D., Ito, K., & Kato, T. (2013). A randomized controlled trial of multicomponent exercise in older adults with mild cognitive impairment. PLoS One, 8(4), e61483.CrossRefGoogle ScholarPubMed
Tanaka, K., de Quadros, A.C. Jr., Santos, R.F., Stella, F., Gobbi, L.T.B., & Gobbi, S. (2009). Benefits of physical exercise on executive functions in older people with Parkinson’s Disease. Brain and Cognition, 69(2), 435441. doi:10.1016/j.bandc.2008.09.008 CrossRefGoogle ScholarPubMed
Taylor, A.E., Saint-Cyr, J.A., & Lang, A.E. (1986). Frontal lobe dysfunction in Parkinson’s disease. The cortical focus of neostriatal outflow. Brain, 109(5), 845883.CrossRefGoogle ScholarPubMed
Troche, M.S., & Altmann, L.J.P. (2012). Sentence production in Parkinson’s disease: Effects of conceptual and task complexity. Applied Psycholinguistics, 33, 225251. doi:10.1017/S0142716411000336 CrossRefGoogle Scholar
Uc, E.Y., Doerschug, K.C., Magnotta, V., Dawson, J.D., Thomsen, T.R., Kline, J.N., & Grabowski, T.J. (2014). Phase I/II randomized trial of aerobic exercise in Parkinson disease in a community setting. Neurology, 83(5), 413425.CrossRefGoogle Scholar
Voss, M.W., Prakash, R.S., Erickson, K.I., Basak, C., Chaddock, L., Kim, J.S., & Kramer, A.F. (2010). Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Frontiers in Aging Neuroscience, 2, pii: 32 doi:10.3389/fnagi.2010.00032 Google Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale-Third Edition (WAIS-III). San Antonio, TX: The Psychological Corporation.Google Scholar
Weerkamp, N.J., Tissingh, G., Poels, P.J., Zuidema, S.U., Munneke, M., Koopmans, R.T., & Bloem, B.R. (2013). Nonmotor symptoms in nursing home residents with Parkinson’s disease: Prevalence and effect on quality of life. Journal of the American Geriatrics Society, 61(10), 17141721.CrossRefGoogle ScholarPubMed
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