AEROBIC EXERCISE IMPROVES WORKING MEMORY IN AN ANIMAL MODEL OF PARKINSON’S DISEASE
Abstract
Regular physical activity is known to have extensive health benefits. Physical activity increases overall survival and reduces the risk of various chronic diseases such as cardiovascular disorders, cancer, hypertension, morbid obesity, depression, diabetes, and osteoporosis. Various molecular mechanisms may be responsible for the observed positive effect associated with physical activity. The most important one refers to the capability of physical exercise to influence the brain’s chemistry and plasticity. Material and methods: we created 2 experimental groups of 6 rats each. First group received a physical exercise intervention, consisting of running on a treadmill adapted for small rodents, for a period of 2 weeks with training sessions composed of 3 sets of 5 minutes per day. The second group was used as control group. All the 12 rats received the pharmaceutical treatment with the substance was N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) for the Parkinson disease model (20 mg / kg). Results: One-Way ANOVA showed that there was a statistically significant difference (p<0.001) between the rats which were randomly assigned to the control group and the rats assigned in the second group, which received the aerobic exercise intervention in regard to the spontaneous alternations’ percent F (1, 10) = 41.096. These results show that aerobic exercise significantly increased spontaneous alternation percent by enhancing neurogenesis in our animal model of Parkinson’s disease. Physical exercise improved memory acquisition, memory retention and reversal learning in the Y-maze task. Conclusions: aerobic exercise increases neurogenesis, which influences both learning and memory. The interactions between the aerobic physical exercise, neurogenesis, learning, and memory are very complex and remarkably dynamic.
References
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35. Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory?. J Neurosci 2001; 31: 10721-10731
36. Botton P H, Costa, M S, Ardais, et al. Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res, 2010; 214: 254-259.
37. Zarow C, Lyness SA, Mortimer JA, Chui HC. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 2003; 60, 337-341
38. Braak H, Del Tredici K, Rub U, et al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 2003; 24: 197-211.
39. Meyer PM, Strecker K, Kendziorra K, et al. Reduced alpha4 beta2*- nicotinic acetylcholine receptor binding and its relationship to mild cognitive and depressive symptoms in Parkinson disease. Arch Gen Psychiatry 2009; 66: 866-877.
40. Mesulam MM, Mufson EJ, Wainer BH, Levey AI. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature. Neuroscience 1983; 10: 1185-1201.
41. Di Rosa G, Puzzo D, Sant’Angelo A, Trinchese F Arancio O. Alpha-synuclein: between synaptic function and dysfunction. Histol Histopathol 2003; 18: 1257-1266.
42. Fordyce DE, Wehner JM. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Research, 1993; 619: 111-119.
43. Fordyce DE, Farrar RP. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behavioural Brain Research 1991; 43: 115-123.
44. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein Cell. 1994; 79: 59-68.
45. Guzowski JF, McGaugh JL. Antisense oligo deoxynucleotide mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training Proceedings of the National Academy of Sciences, USA 1997; 94: 2693-2698.
46. Kida S, Josselyn SA, de Ortiz SP, et al. CREB required for the stability of new and reactivated fear memories. Nature Neuroscience 2002; 5: 348 -355.
47. Fabel K, Tam B, Kaufer D, et al. VEGF is necessary for exercise-induced adult hippocampal neuro-genesis. European Journal of Neuroscience 2003; 18: 2803-2812.
48. Gomez-Pinilla F, Dao L, So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Research 1997; 764: 1- 8.
49. Trejo JL, Carro E, Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. Journal of Neuroscience 2001; 21: 1628 -1634.
50. Endres M, Gertz K, Lindauer U, et al. Mechanisms of stroke protection by physical activity. Annals of Neurology, 2003; 54: 582-590.
51. Swain RA, Harris AB, Wiener EC, et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003; 117: 1037-1046.
52. Pietropaolo S, Feldon J, Alleva E, Cirulli F, Yee BK. The role of voluntary exercise in enriched rearing: A behavioral analysis. Behavioral Neuroscience 2006; 120: 787- 803.
53. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ. The role of the hippocampus in trace conditioning: Temporal discontinuity or task difficulty? Neurobiology of Learning and Memory, 2001; 76: 447- 461.
54. Takehara K, Kawahara S, Kirino, Y Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. Journal of Neuroscience 2003; 23: 9897-9905.
55. Trofin FP, Ciobica A, Cojocaru D, et al. Increased oxidative stress status in rat serum after five minutes treadmill exercise. Cent Eur J Med 2014; 9: 722-728.
56. Gavril R, Dobrin I, Chirita R, Stefanescu C. Current aspects regarding the relevance of inflammation in major depressive disorder. Medical-Surgical Journal 2019; 123(1): 42-50.
57. Turcanu A, Turcu D, Dobrin I, Cristofor A, Poroch V, Enache A. Erythrocyte Sedimentation Rate and Total Serum Protein as Biochemical Markers of Anxiety in Chronic Obstructive Pulmonary Disease. Rev Chim 2019; 70(5): 1689-1693.
58. Debiec J, Ledoux JE, Nader K Cellular and systems reconsolidation in the hippocampus. Neuron 2002; 36: 527-538.
2. da Silva PG, Domingues DD, de Carvalho LA, Allodi S, Correa CL. Neurotrophic factors in Parkin-son’s disease are regulated by exercise: Evidence-based practice. J Neurol Sci 2016; 363: 5-15.
3. Hou L, Chen W, Liu X, Qiao D, Zhou FM. Exercise-induced neuroprotection of the nigrostriatal dopamine system in Parkinson’s disease. Front Aging Neurosci 2017; 9: 358.
4. Petzinger GM, Fisher BE, McEwen S, Beeler JA, Walsh JP, Jakowec MW, et al. Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson’s disease. Lancet Neurol 2013; 12: 716-726.
5. Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: Exercise effects on brain and cognition. Nat Rev Neurosci 2008; 9: 58-65.
6. Hirsch MA, Farley BG. Exercise and neuroplasticity in persons living with Parkinson’s disease. Eur J Phys Rehabil Med 2009; 45: 215-229.
7. Colcombe SJ, Erickson KI, Scalf PE, et al. Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 2006; 61: 1166-1170.
8. Lauzé M, Daneault JF, Duval C. The effects of physical activity in Parkinson’s disease: A Review. J Parkinsons Dis 2016; 6: 685-698.
9. Speelman AD, van de Warrenburg BP, van Nimwegen M, et al How might physical activity benefit patients with Parkinson disease? Nat Rev Neurol 2011; 7: 528-534.
10. Aarsland D, Andersen K, Larsen JP, et al Risk of dementia in Parkinson’s disease: a community based, prospective study Neurology 2001; 56: 730-736.
11. Elgh E, Domello M, Linder J, Edstrom M, Stenlund H, Forsgren L Cognitive function in early Par-kinson’s disease: a population-based study Eur J Neurol 2009; 16: 1278-1284.
12. Mamikonyan E, Moberg PJ, Siderowf A, et al Mild cognitive impairment is common in Parkinson’s disease patients with normal Mini-Mental State Examination (MMSE) scores Parkinsonism Relat Disord 2009; 15: 226-231.
13. Keri S, Moustafa AA, Myers CE, Benedek G, Gluck MA Alpha-Synuclein gene duplication impairs reward learning Proc Natl Acad Sci USA 2010; 107: 15992-15994.
14. Janvin CC, Aarsland D, Larsen JP Cognitive predictors of dementia in Parkinson’s disease: a com-munity-based, 4-year longitudinal study J Geriatr Psychiatry Neurol 2005; 18: 149-154
15. Janvin CC, Larsen JP, Aarsland D, Hugdahl K Subtypes of mild cognitive impairment in Parkinson’s disease: progression to dementia Mov Disord 2006; 21: 1343-1349.
16. Klepac N, Trkulja V, Relja M, Babic T. Is quality of life in nondemented Parkinson’s disease patients related to cognitive performance? A clinic-based cross-sectional study Eur J Neurol 2008; 15: 128-133.
17. Cools R, StefANOVA E, Barker RA, Robbins TW, Owen AM. Dopaminergic modulation of high-level cognition in Parkinson’s disease: the role of the prefrontal cortex revealed by PET. Brain 2002; 125: 584-594.
18. Monchi, O, Petrides M, Doyon J, Postuma RB, Worsley K, Dagher A. Neural bases of set-shifting deficits in Parkinson’s disease J Neurosci, 2004; 24: 702-710.
19. Cameron IG, Watanabe M, Pari G, Munoz DP. Executive impairment in Parkinson’s disease: response automaticity and task switching Neuropsychologia, 2010; 48: 1948-1957.
20. Peterson DA, Elliott C, Song DD, Makeig S, Sejnowski TJ, Poizner H. Probabilistic reversal learning is impaired in Parkinson’s disease Neuroscience 2009; 163: 1092-1101.
21. Partiot A, Verin M, Pillon B, Teixeira-Ferreira C, Agid Y, Dubois, B. Delayed response tasks in basal ganglia lesions in man: further evidence for a striato-frontal cooperation in behavioral adaptation Neuropsychologia 1996; 34: 709-721.
22. Higginson CI, Wheelock VL, Carroll KE, Sigvardt KA. Recognition memory in Parkinson’s disease with and without dementia: evidence inconsistent with the retrieval deficit hypothesis. J Clin Exp Neuropsychol, 2005; 27: 516-528.
23. Whittington CJ, Podd J, Stewart-Williams S. Memory deficits in Parkinson’s disease J Clin Exp Neuropsychol, 2006; 28: 738-754.
24. Knowlton BJ, Mangels JA Squire LR. A neostriatal habit learning system in humans Science 1996; 273: 1399-1402.
25. Wang XP, Sun BM, Ding HL. Changes of procedural learning in Chinese patients with non-demented Parkinson disease Neurosci Lett 2009; 449: 161-163.
26. Colcombe SJ, Kramer AF, Erickson KI, et al. Cardiovascular fitness, cortical plasticity, and aging. Proceedings of the National Academy of Sciences, USA, 2004; 101: 3316 -3321
27. Fabre C, Chamari K, Mucci P, Masse-Biron J, Prefaut C. Improvement of cognitive function by mental and/or individualized aerobic training in healthy elderly subjects International Journal of Sports Medicine 2002; 23: 415- 421.
28. Van Praag H, Christie BR, Sejnowski TJ, Gage H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences, USA, 1996: 96: 13427-13431.
29. Van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice Journal of Neuroscience 2005; 25: 8680-8685.
30. Burghardt PR, Pasumarthi RK, Wilson MA, Fadel J. Alterations in fear conditioning and amygdalar activation following chronic wheel running in rats. Pharmacology Biochemistry and Behavior 2006; 84: 306-312.
31. Samorajski T, Delaney, C, Durham, L, Ordy, J M, Johnson, J A, Dunlap, W P (1985) Effect of exer-cise on longevity, body weight, locomotor performance, and passive-avoidance memory of C57BL/6J mice. Neurobiology of Aging 1985; 6: 17-24.
32. Sarter M, Bodewitz G, Stephens DN Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines Psychopharma-cology (Berl) 1988; 94: 491-495.
33. Parada-Turska J, Turski WA Excitatory amino acid antagonists and memory: effect of drugs acting at N-methyl-D-aspartate receptors in learning and memory tasks. Neuropharmacology 1990; 29: 1111-1116.
34. Wall PM, Blanchard RJ, Yang M, Blanchard DC. Infralimbic D2 receptor influences on anxiety-like behavior and active memory ⁄ attention in CD-1 mice. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27(3): 395-410.
35. Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory?. J Neurosci 2001; 31: 10721-10731
36. Botton P H, Costa, M S, Ardais, et al. Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res, 2010; 214: 254-259.
37. Zarow C, Lyness SA, Mortimer JA, Chui HC. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 2003; 60, 337-341
38. Braak H, Del Tredici K, Rub U, et al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 2003; 24: 197-211.
39. Meyer PM, Strecker K, Kendziorra K, et al. Reduced alpha4 beta2*- nicotinic acetylcholine receptor binding and its relationship to mild cognitive and depressive symptoms in Parkinson disease. Arch Gen Psychiatry 2009; 66: 866-877.
40. Mesulam MM, Mufson EJ, Wainer BH, Levey AI. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature. Neuroscience 1983; 10: 1185-1201.
41. Di Rosa G, Puzzo D, Sant’Angelo A, Trinchese F Arancio O. Alpha-synuclein: between synaptic function and dysfunction. Histol Histopathol 2003; 18: 1257-1266.
42. Fordyce DE, Wehner JM. Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase C activity in C57BL/6 and DBA/2 mice. Brain Research, 1993; 619: 111-119.
43. Fordyce DE, Farrar RP. Physical activity effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behavioural Brain Research 1991; 43: 115-123.
44. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein Cell. 1994; 79: 59-68.
45. Guzowski JF, McGaugh JL. Antisense oligo deoxynucleotide mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training Proceedings of the National Academy of Sciences, USA 1997; 94: 2693-2698.
46. Kida S, Josselyn SA, de Ortiz SP, et al. CREB required for the stability of new and reactivated fear memories. Nature Neuroscience 2002; 5: 348 -355.
47. Fabel K, Tam B, Kaufer D, et al. VEGF is necessary for exercise-induced adult hippocampal neuro-genesis. European Journal of Neuroscience 2003; 18: 2803-2812.
48. Gomez-Pinilla F, Dao L, So V. Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Research 1997; 764: 1- 8.
49. Trejo JL, Carro E, Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. Journal of Neuroscience 2001; 21: 1628 -1634.
50. Endres M, Gertz K, Lindauer U, et al. Mechanisms of stroke protection by physical activity. Annals of Neurology, 2003; 54: 582-590.
51. Swain RA, Harris AB, Wiener EC, et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003; 117: 1037-1046.
52. Pietropaolo S, Feldon J, Alleva E, Cirulli F, Yee BK. The role of voluntary exercise in enriched rearing: A behavioral analysis. Behavioral Neuroscience 2006; 120: 787- 803.
53. Beylin AV, Gandhi CC, Wood GE, Talk AC, Matzel LD, Shors TJ. The role of the hippocampus in trace conditioning: Temporal discontinuity or task difficulty? Neurobiology of Learning and Memory, 2001; 76: 447- 461.
54. Takehara K, Kawahara S, Kirino, Y Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. Journal of Neuroscience 2003; 23: 9897-9905.
55. Trofin FP, Ciobica A, Cojocaru D, et al. Increased oxidative stress status in rat serum after five minutes treadmill exercise. Cent Eur J Med 2014; 9: 722-728.
56. Gavril R, Dobrin I, Chirita R, Stefanescu C. Current aspects regarding the relevance of inflammation in major depressive disorder. Medical-Surgical Journal 2019; 123(1): 42-50.
57. Turcanu A, Turcu D, Dobrin I, Cristofor A, Poroch V, Enache A. Erythrocyte Sedimentation Rate and Total Serum Protein as Biochemical Markers of Anxiety in Chronic Obstructive Pulmonary Disease. Rev Chim 2019; 70(5): 1689-1693.
58. Debiec J, Ledoux JE, Nader K Cellular and systems reconsolidation in the hippocampus. Neuron 2002; 36: 527-538.
Published
2022-06-30
Section
BASIC SCIENCES
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