Skip to main content
Top
Published in: Sport Sciences for Health 2/2019

01-08-2019 | Parkinson's Disease | Original Article

The effects of voluntary exercise on learning and memory deficit in Parkinson’s disease model of rats

Authors: F. Rafie, V. Sheibani, M. Shahbazi, N. Naghdi, M. Pourranjbar, M. Sheikh

Published in: Sport Sciences for Health | Issue 2/2019

Login to get access

Abstract

Parkinson’s disease (PD) is a neurodegenerative disease characterized by progressive and loss of dopaminergic neurons in the SNpc. Behavioral symptoms and cognitive impairments even dementia are common in Parkinson disease. Physical activity impacts functional recovery in humans, however, its effects in experimental animals submitted to Parkinson model have been inconsistent. The present work was focused on the neuroprotective effect of 4 weeks voluntary exercise (wheel running) against experimentally (6-OHDA) induced Parkinson’s disease in rat, by analyzing the memory and learning. Morris water maze test was used for measurement of spatial learning and memory. Results did not demonstrate any main effect differences between the exercise and control groups on weight gain (p > 0.05). 6-OHDA injection caused a significant cognitive deficit in spatial water maze tasks and this effect was reversed in rats after receiving exercise protocol. Voluntary exercise improved the cognitive performance in both reference and working spatial memory against 6-OHDA administration (p < 0.05). We suggest that voluntary exercise interventions may has the potential role in promoting neuroplasticity and repair cognitive dysfunction in Parkinson’s disease (PD).
Literature
1.
go back to reference Miyasaki JM et al (2006) Practice Parameter: Evaluation and treatment of depression, psychosis, and dementia in Parkinson disease (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 66(7):996–1002PubMedCrossRef Miyasaki JM et al (2006) Practice Parameter: Evaluation and treatment of depression, psychosis, and dementia in Parkinson disease (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 66(7):996–1002PubMedCrossRef
2.
go back to reference De Rijk Md et al (1997) Prevalence of parkinsonism and Parkinson’s disease in Europe: the EUROPARKINSON Collaborative Study. European Community Concerted Action on the Epidemiology of Parkinson’s disease. J Neurol Neurosurg Psychiatry 62(1):10–15PubMedPubMedCentralCrossRef De Rijk Md et al (1997) Prevalence of parkinsonism and Parkinson’s disease in Europe: the EUROPARKINSON Collaborative Study. European Community Concerted Action on the Epidemiology of Parkinson’s disease. J Neurol Neurosurg Psychiatry 62(1):10–15PubMedPubMedCentralCrossRef
3.
go back to reference Fahn S (2003) Description of Parkinson’s disease as a clinical syndrome. Ann N Y Acad Sci 991(1):1–14PubMedCrossRef Fahn S (2003) Description of Parkinson’s disease as a clinical syndrome. Ann N Y Acad Sci 991(1):1–14PubMedCrossRef
5.
go back to reference Carbon M, Marié RM (2003) Functional imaging of cognition in Parkinson’s disease. Curr Opin Neurol 16(4):475–480PubMed Carbon M, Marié RM (2003) Functional imaging of cognition in Parkinson’s disease. Curr Opin Neurol 16(4):475–480PubMed
6.
go back to reference Witt K, Nuhsman A, Deuschl G (2002) Dissociation of habit-learning in Parkinson’s and cerebellar disease. J Cogn Neurosci 14(3):493–499PubMedCrossRef Witt K, Nuhsman A, Deuschl G (2002) Dissociation of habit-learning in Parkinson’s and cerebellar disease. J Cogn Neurosci 14(3):493–499PubMedCrossRef
7.
go back to reference Lewis SJ, Slabosz A, Robbins TW, Barker RA, Owen AM (2005) Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson’s disease. Neuropsychologia 43(6):823–832PubMedCrossRef Lewis SJ, Slabosz A, Robbins TW, Barker RA, Owen AM (2005) Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson’s disease. Neuropsychologia 43(6):823–832PubMedCrossRef
8.
go back to reference Ang ET, Gomez-Pinilla F (2007) Potential therapeutic effects of exercise to the brain. Curr Med Chem 14:2564–2571PubMedCrossRef Ang ET, Gomez-Pinilla F (2007) Potential therapeutic effects of exercise to the brain. Curr Med Chem 14:2564–2571PubMedCrossRef
9.
go back to reference van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427–13431PubMedCrossRef van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427–13431PubMedCrossRef
10.
go back to reference Tillerson JL, Caudle WM, Reveron ME, Miller GW (2003) Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience 119:899–911PubMedCrossRef Tillerson JL, Caudle WM, Reveron ME, Miller GW (2003) Exercise induces behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson’s disease. Neuroscience 119:899–911PubMedCrossRef
11.
go back to reference Petzinger GM et al (2013) Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson’s disease. Lancet Neurol 12(7):716–726PubMedPubMedCentralCrossRef Petzinger GM et al (2013) Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson’s disease. Lancet Neurol 12(7):716–726PubMedPubMedCentralCrossRef
12.
go back to reference Goodwin VA, Richards SH, Taylor RS, Taylor AH, Campbell JL (2008) The effectiveness of exercise interventions for people with Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 23:631–640PubMedCrossRef Goodwin VA, Richards SH, Taylor RS, Taylor AH, Campbell JL (2008) The effectiveness of exercise interventions for people with Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 23:631–640PubMedCrossRef
13.
go back to reference Julien C et al (2006) Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and parkinsonian monkeys. Neurochem Int 48(5):404–414PubMedCrossRef Julien C et al (2006) Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and parkinsonian monkeys. Neurochem Int 48(5):404–414PubMedCrossRef
14.
go back to reference Samadi P et al (2006) Docosahexaenoic acid reduces levodopa-induced dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine monkeys. Ann Neurol 59(2):282–288PubMedCrossRef Samadi P et al (2006) Docosahexaenoic acid reduces levodopa-induced dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine monkeys. Ann Neurol 59(2):282–288PubMedCrossRef
15.
go back to reference Schapira AH et al (2006) Novel pharmacological targets for the treatment of Parkinson’s disease. Nat Rev Drug Discov 5(10):845–854PubMedCrossRef Schapira AH et al (2006) Novel pharmacological targets for the treatment of Parkinson’s disease. Nat Rev Drug Discov 5(10):845–854PubMedCrossRef
16.
go back to reference Kim D-H et al (2010) Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav 101(5):660–665PubMedCrossRef Kim D-H et al (2010) Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav 101(5):660–665PubMedCrossRef
17.
go back to reference Kim S-E et al (2010) Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45(5):357–365PubMedCrossRef Kim S-E et al (2010) Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45(5):357–365PubMedCrossRef
18.
19.
go back to reference Farbood Y et al (2015) Ellagic acid protects the brain against 6-hydroxydopamine induced neuroinflammation in a rat model of Parkinson’s disease. Basic Clin Neurosci 6(2):83–90PubMedPubMedCentral Farbood Y et al (2015) Ellagic acid protects the brain against 6-hydroxydopamine induced neuroinflammation in a rat model of Parkinson’s disease. Basic Clin Neurosci 6(2):83–90PubMedPubMedCentral
20.
go back to reference Rafie F, Shabazi M, Sheikh M, Naghdi N, Sheibani V (2017) Effects of voluntary exercise on motor function in Parkinson’s disease model of rats. Ann Appl Sport Sci 5(2):81–86CrossRef Rafie F, Shabazi M, Sheikh M, Naghdi N, Sheibani V (2017) Effects of voluntary exercise on motor function in Parkinson’s disease model of rats. Ann Appl Sport Sci 5(2):81–86CrossRef
21.
go back to reference Da Cunha C, Angelucci ME, Canteras NS, Wonnacott S, Takahashi RN (2002) The lesion of the rat substantia nigra pars compacta dopaminergic neurons as a model for Parkinson’s disease memory disabilities. Cell Mol Neurobiol 22(3):227–237PubMedCrossRef Da Cunha C, Angelucci ME, Canteras NS, Wonnacott S, Takahashi RN (2002) The lesion of the rat substantia nigra pars compacta dopaminergic neurons as a model for Parkinson’s disease memory disabilities. Cell Mol Neurobiol 22(3):227–237PubMedCrossRef
22.
go back to reference Salari M, Sheibani V, Saadati H, Pourrahimi A, Esmaeelpour K, Khodamoradi M (2015) The compensatory effect of regular exercise on long-term memory impairment in sleep deprived female rats. Behav Process 119:50–57CrossRef Salari M, Sheibani V, Saadati H, Pourrahimi A, Esmaeelpour K, Khodamoradi M (2015) The compensatory effect of regular exercise on long-term memory impairment in sleep deprived female rats. Behav Process 119:50–57CrossRef
23.
go back to reference Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 69(3):308–312PubMedPubMedCentralCrossRef Schrag A, Jahanshahi M, Quinn N (2000) What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry 69(3):308–312PubMedPubMedCentralCrossRef
24.
go back to reference Gorton LM et al (2010) Exercise effects on motor and affective behavior and catecholamine neurochemistry in the MPTP-lesioned mouse. Behav Brain Res 213(2):253–262PubMedPubMedCentralCrossRef Gorton LM et al (2010) Exercise effects on motor and affective behavior and catecholamine neurochemistry in the MPTP-lesioned mouse. Behav Brain Res 213(2):253–262PubMedPubMedCentralCrossRef
25.
go back to reference Howells FM et al (2005) Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson’s disease. Behav Brain Res 165(2):210–220PubMedCrossRef Howells FM et al (2005) Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson’s disease. Behav Brain Res 165(2):210–220PubMedCrossRef
26.
go back to reference Nieuwboer A et al (2009) Motor learning in Parkinson’s disease: limitations and potential for rehabilitation. Parkinsonism Relat Disord 15:S53–S58 (48) PubMedCrossRef Nieuwboer A et al (2009) Motor learning in Parkinson’s disease: limitations and potential for rehabilitation. Parkinsonism Relat Disord 15:S53–S58 (48) PubMedCrossRef
27.
go back to reference Sheibani V, Rafie F, Shahbazi M, Naghdi N, Sheikh M (2017) Comparison of voluntary and forced exercise effects on motor behavior in 6-hydroxydopamine-lesion rat model of Parkinson’s disease. Sport Sci Health 13(1):203–211CrossRef Sheibani V, Rafie F, Shahbazi M, Naghdi N, Sheikh M (2017) Comparison of voluntary and forced exercise effects on motor behavior in 6-hydroxydopamine-lesion rat model of Parkinson’s disease. Sport Sci Health 13(1):203–211CrossRef
29.
go back to reference Kinni H et al (2011) Cerebral metabolism after forced or voluntary physical exercise. Brain Res 1388:48–55PubMedCrossRef Kinni H et al (2011) Cerebral metabolism after forced or voluntary physical exercise. Brain Res 1388:48–55PubMedCrossRef
30.
go back to reference Lambert M et al (1996) Tests of running performance do not predict subsequent spontaneous running in rats. Physiol Behav 60(1):171–176PubMedCrossRef Lambert M et al (1996) Tests of running performance do not predict subsequent spontaneous running in rats. Physiol Behav 60(1):171–176PubMedCrossRef
31.
go back to reference Tarr BA et al (2004) Voluntary running distance is negatively correlated with striatal dopamine release in untrained rats. Behav Brain Res 154(2):493–499PubMedCrossRef Tarr BA et al (2004) Voluntary running distance is negatively correlated with striatal dopamine release in untrained rats. Behav Brain Res 154(2):493–499PubMedCrossRef
32.
go back to reference Ferro MM, Bellissimo MI, Anselmo-Franci JA, Angellucci ME, Canteras NS, Da Cunha C (2005) Comparison of bilaterally 6-OHDA-and MPTP-lesioned rats as models of the early phase of Parkinson’s disease: histological, neurochemical, motor and memory alterations. J Neurosci Methods 148(1):78–87PubMedCrossRef Ferro MM, Bellissimo MI, Anselmo-Franci JA, Angellucci ME, Canteras NS, Da Cunha C (2005) Comparison of bilaterally 6-OHDA-and MPTP-lesioned rats as models of the early phase of Parkinson’s disease: histological, neurochemical, motor and memory alterations. J Neurosci Methods 148(1):78–87PubMedCrossRef
33.
go back to reference Sconce MD, Churchill MJ, Greene RE, Meshul CK (2015) Intervention with exercise restores motor deficits but not nigrostriatal loss in a progressive MPTP mouse model of Parkinson’s disease. Neuroscience 299:156–174PubMedCrossRef Sconce MD, Churchill MJ, Greene RE, Meshul CK (2015) Intervention with exercise restores motor deficits but not nigrostriatal loss in a progressive MPTP mouse model of Parkinson’s disease. Neuroscience 299:156–174PubMedCrossRef
34.
go back to reference Braak H, Rüb U, Steur EJ, Del Tredici K, De Vos RA (2005) Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 64(8):1404–10PubMedCrossRef Braak H, Rüb U, Steur EJ, Del Tredici K, De Vos RA (2005) Cognitive status correlates with neuropathologic stage in Parkinson disease. Neurology 64(8):1404–10PubMedCrossRef
35.
go back to reference Murray DK, Sacheli MA, Eng JJ, Stoessl AJ (2014) The effects of exercise on cognition in Parkinson’s disease: a systematic review. Transl Neurodegen 3(1):1CrossRef Murray DK, Sacheli MA, Eng JJ, Stoessl AJ (2014) The effects of exercise on cognition in Parkinson’s disease: a systematic review. Transl Neurodegen 3(1):1CrossRef
36.
go back to reference García-Capdevila S, Portell-Cortés I, Torras-Garcia M, Coll-Andreu M, Costa-Miserachs D (2009) Effects of long-term voluntary exercise on learning and memory processes: dependency of the task and level of exercise. Behav Brain Res 202(2):162–170PubMedCrossRef García-Capdevila S, Portell-Cortés I, Torras-Garcia M, Coll-Andreu M, Costa-Miserachs D (2009) Effects of long-term voluntary exercise on learning and memory processes: dependency of the task and level of exercise. Behav Brain Res 202(2):162–170PubMedCrossRef
37.
go back to reference Cotman CW, Engesser-Cesar C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30(2):75–79PubMedCrossRef Cotman CW, Engesser-Cesar C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30(2):75–79PubMedCrossRef
38.
go back to reference Crowley EK, Nolan YM, Sullivan AM (2018) Neuroprotective effects of voluntary running on cognitive dysfunction in an α-synuclein rat model of Parkinson’s disease. Neurobiol Aging 65:60–68PubMedCrossRef Crowley EK, Nolan YM, Sullivan AM (2018) Neuroprotective effects of voluntary running on cognitive dysfunction in an α-synuclein rat model of Parkinson’s disease. Neurobiol Aging 65:60–68PubMedCrossRef
39.
go back to reference Paillard T, Rolland Y, de Souto Barreto P (2015) Protective effects of physical exercise in Alzheimer’s disease and Parkinson’s disease: a narrative review. J Clin Neurol 11(3):212–219PubMedPubMedCentralCrossRef Paillard T, Rolland Y, de Souto Barreto P (2015) Protective effects of physical exercise in Alzheimer’s disease and Parkinson’s disease: a narrative review. J Clin Neurol 11(3):212–219PubMedPubMedCentralCrossRef
40.
go back to reference Alomari MA, Khabour OF, Alzoubi KH, Alzubi MA (2016) Combining restricted diet with forced or voluntary exercises improves hippocampal BDNF and cognitive function in rats. Int J Neurosci 126(4):366–373PubMedCrossRef Alomari MA, Khabour OF, Alzoubi KH, Alzubi MA (2016) Combining restricted diet with forced or voluntary exercises improves hippocampal BDNF and cognitive function in rats. Int J Neurosci 126(4):366–373PubMedCrossRef
41.
go back to reference Vučcković MG, Li Q, Fisher B, Nacca A et al (2010) Exercise elevates dopamine D2 receptor in a mouse model of Parkinson’s disease: in vivo imaging with (18F) fallypride. Mov Disord 25(16):2777–2784CrossRef Vučcković MG, Li Q, Fisher B, Nacca A et al (2010) Exercise elevates dopamine D2 receptor in a mouse model of Parkinson’s disease: in vivo imaging with (18F) fallypride. Mov Disord 25(16):2777–2784CrossRef
42.
go back to reference Mabandla M, Kellaway L, Gibson ASC, Russell VA (2004) Voluntary running provides neuroprotection in rats after 6-hydroxydopamine injection into the medial forebrain bundle. Metab Brain Dis 19(1–2):43–50PubMedCrossRef Mabandla M, Kellaway L, Gibson ASC, Russell VA (2004) Voluntary running provides neuroprotection in rats after 6-hydroxydopamine injection into the medial forebrain bundle. Metab Brain Dis 19(1–2):43–50PubMedCrossRef
43.
go back to reference Aguiar AS, Castro AA, Moreira EL, Glaser V et al (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 132(11):560–567PubMedCrossRef Aguiar AS, Castro AA, Moreira EL, Glaser V et al (2011) Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech Ageing Dev 132(11):560–567PubMedCrossRef
44.
go back to reference Zang J, Liu Y, Li W, Xiao D, Zhang Y, Luo Y, Liang W, Liu F, Wei W (2017) Voluntary exercise increases adult hippocampal neurogenesis by increasing GSK-3β activity in mice. Neuroscience 354:122–135PubMedCrossRef Zang J, Liu Y, Li W, Xiao D, Zhang Y, Luo Y, Liang W, Liu F, Wei W (2017) Voluntary exercise increases adult hippocampal neurogenesis by increasing GSK-3β activity in mice. Neuroscience 354:122–135PubMedCrossRef
45.
go back to reference Zhou W, Barkow JC, Freed CR (2017) Running wheel exercise reduces α-synuclein aggregation and improves motor and cognitive function in a transgenic mouse model of Parkinson’s disease. PloS One 12(12):e0190160PubMedPubMedCentralCrossRef Zhou W, Barkow JC, Freed CR (2017) Running wheel exercise reduces α-synuclein aggregation and improves motor and cognitive function in a transgenic mouse model of Parkinson’s disease. PloS One 12(12):e0190160PubMedPubMedCentralCrossRef
Metadata
Title
The effects of voluntary exercise on learning and memory deficit in Parkinson’s disease model of rats
Authors
F. Rafie
V. Sheibani
M. Shahbazi
N. Naghdi
M. Pourranjbar
M. Sheikh
Publication date
01-08-2019
Publisher
Springer Milan
Published in
Sport Sciences for Health / Issue 2/2019
Print ISSN: 1824-7490
Electronic ISSN: 1825-1234
DOI
https://doi.org/10.1007/s11332-019-00531-7

Other articles of this Issue 2/2019

Sport Sciences for Health 2/2019 Go to the issue