Volume 27, Issue 2 (July 2023)                   Physiol Pharmacol 2023, 27(2): 161-170 | Back to browse issues page


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Shahidi S, Rafiee H, Sohrabi S, Mohebi N, Jahani M, Sohrabi F, et al . Effects of swimming exercise during pre-adolescence on learning and memory in adult rats: behavioral and electrophysiological approaches. Physiol Pharmacol 2023; 27 (2) :161-170
URL: http://ppj.phypha.ir/article-1-1753-en.html
Abstract:   (1073 Views)

Introduction: The positive impact of physical activity on age-related memory impairment is well documented. There is no clear report on the effects of pre-adolescent exercise on cognitive abilities in adulthood.
Methods: Male Wistar rats (4-week-old) were randomized to a non-swimmer (control, n=20) and swimmer (n=20). The swimmer group trained for 30min a day, 6 days per week, 6 weeks. After the last day, behavior (through passive avoidance learning and radial maze) and electrophysiological techniques were evaluated in rats.
Results: Swimming exercise led to a decrease in the number of trials in the passive avoidance test. In addition, swimming reduced the number of working memory and reference memory errors in the radial maze task. On the radial maze task, the two groups showed equal learning ability in finding the baited food arms by day 15. The results of the recall tests showed that the number of total memory errors and working memory errors was significantly lower in the swimmer group than in the non-swimmer group. Exercise also improved both Population spike (PS) amplitude and field-excited postsynaptic potential slope.
Conclusion: These results revealed that swimming exercise could improve memory by increasing synaptic plasticity in rats.

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References
1. Abshenas R, Artimani T, Shahidi S, Ranjbar A, Komaki A, Salehi I, et al. Treadmill exercise enhances the promoting effects of preconditioned stem cells on memory and neurogenesis in Aβ-induced neurotoxicity in the rats. Life Sci 2020; 249: 117482. [DOI:10.1016/j.lfs.2020.117482]
2. Afshar S, Shahidi S, Rohani AH, Komaki A, Asl SS. The effect of NAD-299 and TCB-2 on learning and memory, hippocampal BDNF levels and amyloid plaques in Streptozotocin-induced memory deficits in male rats. Psychopharmacology 2018; 235: 2809-22. [DOI:10.1007/s00213-018-4973-x]
3. Ahmed T, Frey JU. Plasticity-specific phosphorylation of CaMKII, MAP-kinases and CREB during late-LTP in rat hippocampal slices in vitro. Neuropharmacology 2005; 49: 477-92. [DOI:10.1016/j.neuropharm.2005.04.018]
4. Amaral DG, Scharfman HE, Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 2007; 163: 3-22. [DOI:10.1016/S0079-6123(07)63001-5]
5. Arnett JJ. Emerging adulthood. A theory of development from the late teens through the twenties. Am Psychol 2000; 55: 469-80. [DOI:10.1037/0003-066X.55.5.469]
6. Avchalumov Y, Mandyam CD. Plasticity in the hippocampus, neurogenesis and drugs of abuse. Brain Sci 2021; 11: 404. [DOI:10.3390/brainsci11030404]
7. Bogin B. Adolescence in evolutionary perspective. Acta Paediatr Suppl 1994; 406: 29-35. [DOI:10.1111/j.1651-2227.1994.tb13418.x]
8. Brust V, Schindler PM, Lewejohann L. Lifetime development of behavioural phenotype in the house mouse (Mus musculus). Front Zool 2015; 12: S17. [DOI:10.1186/1742-9994-12-S1-S17]
9. Cechella JL, Leite MR, Rosario AR, Sampaio TB, Zeni G. Diphenyl diselenide-supplemented diet and swimming exercise enhance novel object recognition memory in old rats. Age 2014; 36: 9666. [DOI:10.1007/s11357-014-9666-8]
10. Da Cruz JN, De Lima DD, Dal Magro D D, Da Cruz JGP. The effects of swimming exercise on recognition memory for objects and conditioned fear in rats. Acta Scientiarum. Health Sciences 2012; 34: 163-69. [DOI:10.4025/actascihealthsci.v34i2.4378]
11. Dahl RE. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 2004; 1021: 1-22. [DOI:10.1196/annals.1308.001]
12. de Lima DD, Dal Magro DD, da Cruz JN, da Cruz JGP. The effects of swimming exercise on recognition memory for objects and conditioned fear in rats. Acta Scientiarum. Health Sciences 2012; 34: 163-9. [DOI:10.4025/actascihealthsci.v34i2.4378]
13. Dehbani Z, Komaki A, Etaee F, Shahidi S, Taheri M, Komaki S, et al. Effect of a hydro-alcoholic extract of Melissa officinalis on passive avoidance learning and memory. J Herbmed Pharmacol 2019; 8: 120-5. [DOI:10.15171/jhp.2019.19]
14. Eiland L, Romeo RD. Stress and the developing adolescent brain. Neuroscience 2013; 249: 162-71. [DOI:10.1016/j.neuroscience.2012.10.048]
15. Farmer J, Zhao X, van Praag H, Wodtke K, Gage FH, Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004; 124: 71-9. [DOI:10.1016/j.neuroscience.2003.09.029]
16. Habibi P, Alihemmati A, NourAzar A, Yousefi H, Mortazavi S, Ahmadiasl N. Expression of the Mir-133 and Bcl-2 could be affected by swimming training in the heart of ovariectomized rats. Iran J Basic Med Sci 2016; 19: 381-7.
17. Hatami M, Conrad S, Naghsh P, Alvarez-Bolado G, Skutella T. Cell-biological requirements for the generation of dentate gyrus granule neurons. Front Cell Neurosci 2018; 12: 402. [DOI:10.3389/fncel.2018.00402]
18. Hosseini M, Khodabandehloo F, Karami R, Mohammadpour T, Rajaei Z, Fereidoni M, et al. Different effects of scopolamine on memory of young male and female rats. Pharmacologyonline 2010; 3: 450-8.
19. Huang YW, Hu WW, Chen Z, Zhang LS, Shen HQ, Timmerman H, et al. Effect of the histamine H3-antagonist clobenpropit on spatial memory deficits induced by MK-801 as evaluated by radial maze in Sprague-Dawley rats. Behav Brain Res 2004; 151: 287-93. [DOI:10.1016/j.bbr.2003.09.002]
20. Karamian R, Komaki A, Salehi I, Tahmasebi L, Komaki H, Shahidi S, et al. Vitamin C reverses lead-induced deficits in hippocampal synaptic plasticity in rats. Brain Res Bull 2015; 116: 7-15. [DOI:10.1016/j.brainresbull.2015.05.004]
21. Kemp A, Manahan-Vaughan D. The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression. Cereb Cortex 2008; 18: 968-77. [DOI:10.1093/cercor/bhm136]
22. Khajehnasiri N, Dehkordi MB, Amini-Khoei H, Mohammadabadi MSM, Sadeghian R. Effect of exercise intensity and duration on the levels of stress hormones and hypothalamic-pituitary-gonadal axis in adult male rats: an experimental study. Hormones (Athens) 2021; 20: 483-90. [DOI:10.1007/s42000-021-00303-4]
23. Khani F, Pourmotabbed A, Hosseinmardi N, Nedaei SE, Fathollahi Y, Azizi H. Impairment of spatial memory and dorsal hippocampal synaptic plasticity in adulthood due to adolescent morphine exposure. Prog Neuropsychopharmacol Biol Psychiatry 2022; 116: 110532. [DOI:10.1016/j.pnpbp.2022.110532]
24. Lenroot RK, Gogtay N, Greenstein DK, Wells EM, Wallace GL, Clasen LS, et al. Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage 2007; 36: 1065-73. [DOI:10.1016/j.neuroimage.2007.03.053]
25. Li MY, Huang MM, Li SZ, Tao J, Zheng GH, Chen LD. The effects of aerobic exercise on the structure and function of DMN-related brain regions: a systematic review. Int J Neurosci 2017; 127: 634-49. [DOI:10.1080/00207454.2016.1212855]
26. Liston C, Watts R, Tottenham N, Davidson MC, Niogi S, Ulug AM, et al. Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cereb Cortex 2006; 16: 553-60. [DOI:10.1093/cercor/bhj003]
27. Liu HL, Zhao G, Cai K, Zhao Hh. Treadmill exercise prevents decline in spatial learning and memory in APP/PS1 transgenic mice through improvement of hippocampal long-term potentiation. Behav Brain Res 2011; 218: 308-14. [DOI:10.1016/j.bbr.2010.12.030]
28. Mohammadi S, Oryan S, Komaki A, Eidi A, Zarei M. Effects of intra-dentate gyrus microinjection of myokine irisin on long-term potentiation in male rats. Arq Neuropsiquiatr 2019; 77: 881-7. [DOI:10.1590/0004-282x20190184]
29. Molaei A, Hatami H, Dehghan G, Sadeghian R, Khajehnasiri N. Synergistic effects of quercetin and regular exercise on the recovery of spatial memory and reduction of parameters of oxidative stress in animal model of Alzheimer’s disease. Excli j 2020; 19: 596-612.
30. Muetzel RL, Collins PF, Mueller BA, Schissel AM, Lim KO, Luciana M. The development of corpus callosum microstructure and associations with bimanual task performance in healthy adolescents. Neuroimage 2008; 39: 1918-25. [DOI:10.1016/j.neuroimage.2007.10.018]
31. O’Callaghan RM, Ohle R, Kelly AM. The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial-and non-spatial learning. Behav Brain Res 2007; 176: 362-6. [DOI:10.1016/j.bbr.2006.10.018]
32. Olesen P J, Nagy Z, Westerberg H, Klingberg T. Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Res Cogn Brain Res 2003; 18: 48-57. [DOI:10.1016/j.cogbrainres.2003.09.003]
33. Poulter S L, Kosaki Y, Sanderson D J, McGregor A. Spontaneous object-location memory based on environmental geometry is impaired by both hippocampal and dorsolateral striatal lesions. Brain Neurosci Adv 2020; 4: 2398212820972599. [DOI:10.1177/2398212820972599]
34. Raichlen DA, Alexander GE. Adaptive capacity: an evolutionary neuroscience model linking exercise, cognition, and brain health. Trends Neurosci 2017; 40: 408-21. [DOI:10.1016/j.tins.2017.05.001]
35. Rajizadeh MA, Esmaeilpour K, Haghparast E, Ebrahimi MN, Sheibani V. Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats. Brain Res 2020; 1729: 146598. [DOI:10.1016/j.brainres.2019.146598]
36. Sadeghian R, Shahidi S, Komaki A, Habibi P, Ahmadiasl N, Yousefi H, et al. Synergism effect of swimming exercise and genistein on the inflammation, oxidative stress, and VEGF expression in the retina of diabetic-ovariectomized rats. Life Sci 2021; 284: 119931. [DOI:10.1016/j.lfs.2021.119931]
37. Salehi I, Karamian R, Komaki A, Tahmasebi L, Taheri M, Nazari M, et al. Effects of vitamin E on lead-induced impairments in hippocampal synaptic plasticity. Brain Res 2015; 1629: 270-81. [DOI:10.1016/j.brainres.2015.10.007]
38. Salmanzadeh H, Ahmadi-Soleimani SM, Pachenari N, Azadi M, Halliwell R, Rubino T, et al. Adolescent drug exposure: a review of evidence for the development of persistent changes in brain function. Brain Res Bull 2020; 156:105-17. [DOI:10.1016/j.brainresbull.2020.01.007]
39. Sexton CE, Betts JF, Demnitz N, Dawes H, Ebmeier KP, Johansen-Berg H. A systematic review of MRI studies examining the relationship between physical fitness and activity and the white matter of the ageing brain. Neuroimage 2016; 131: 81-90. [DOI:10.1016/j.neuroimage.2015.09.071]
40. Shahidi S, Arjipour M, Komaki A, Mahmoodi M. Differential Effects of Sildenafil (Viagra) on processing steps of spatial learning and memory in rat. Avicenna J Neuro Psych Physiology 2014; 1: 20-5. [DOI:10.17795/ajnpp-18671]
41. Shahidi S, Komaki A, Sadeghian R, Asl SS. Different doses of methamphetamine alter long-term potentiation, level of BDNF and neuronal apoptosis in the hippocampus of reinstated rats. J Physiol Sci 2019a; 69: 409-19. [DOI:10.1007/s12576-019-00660-1]
42. Shahidi S, Komaki A, Sadeghian R, Soleimani Asl S. Effect of a 5-HT(1D) receptor agonist on the reinstatement phase of the conditioned place preference test and hippocampal long-term potentiation in methamphetamine-treated rats. Brain Res 2018; 1698: 151-60. [DOI:10.1016/j.brainres.2018.07.030]
43. Shahidi S, Mehrpour O, Sadeghian R, Asl SS, Komaki A. Alteration level of hippocampus BDNF expression and long-term potentiation upon microinjection of BRL15572 hydrochloride in a rat model of methamphetamine relapse. Brain Res Bull 2019b; 148: 18-24. [DOI:10.1016/j.brainresbull.2019.03.008]
44. Shahidi S, Motamedi F, Naghdi N. Effect of reversible inactivation of the supramammillary nucleus on spatial learning and memory in rats. Brain Res 2004; 1026: 267-74. [DOI:10.1016/j.brainres.2004.08.030]
45. Shahidi S, Rabiee L, Komaki A, Sadeghian R. High-dose fluoxetine improved long-term potentiation of the hippocampal dentate gyrus in male rats. Physiol Pharmacol (Iran) 2021; 25: 223-30. [DOI:10.52547/ppj.25.3.223]
46. Shahidi S, Vishteh M, komaki A, Sadeghian R. The effects of sildenafil on the hippocampal long-term potentiation in male rats. Physiol-Pharmacol 2022; 26: 138-144. [DOI: 10.52547/phypha.26.2.9]
47. Steventon JJ, Foster C, Furby H, Helme D, Wise RG, Murphy K. Hippocampal blood flow is increased after 20 min of moderate-intensity exercise. Cereb Cortex 2020; 30: 525-33. [DOI:10.1093/cercor/bhz104]
48. Van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 1999; 96: 13427-31. [DOI:10.1073/pnas.96.23.13427]
49. Zhang L, Tang M, Wang F, Zhao Y, Liu Z. The impact of different exercise intensities on working memory and BDNF protein expression in prefrontal cortex of sleep deprivation rat. Int J Clin Exp Med 2017; 10: 9265-70.

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