Skip to main content
Log in

Intermittent exercise improves working memory and locomotor activity by attenuating oxidative stress in the prefrontal cortex and cerebellum of ovariectomized rats

  • Original Article
  • Published:
Sport Sciences for Health Aims and scope Submit manuscript

Abstract

Objectives

The aim of the present study was to investigate the effects of moderate- or high-intensity intermittent exercise (MIIE/HIIE) on the oxidative status of the prefrontal cortex and cerebellum, locomotor activities, as well as working memory performances of rats.

Materials and Methods

Twenty female rats were divided into four groups: (1) sham-operated (Sham), (2) ovariectomy (OVX), (3) OVX + MIIE, and (4) OVX + HIIE groups. The OVX + MIIE and OVX + HIIE groups exercised on a rat treadmill for 7 weeks. The assessment on the working memory performances and locomotor activities were conducted on the last day of the exercise period. Levels of superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX) enzyme activities, as well as levels of hydrogen peroxidase (H2O2), and malondialdehyde (MDA) in the prefrontal cortex and cerebellum were determined using a spectrophotometer.

Results

Ovariectomy depressed the working memory, locomotor activities, the levels of SOD, CAT, and GPX enzyme activities, and elevated the levels of H2O2, and MDA in the prefrontal cortex and cerebellum.

Conclusion

MIIE and HIIE exert their neuroprotective effects by reducing oxidative stress in the brain of ovariectomized rats. HIIE has more potent effects than MIIE in suppressing the levels of oxidants in the prefrontal cortex and cerebellum by increasing the levels of SOD and CAT activities more than MIIE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Genazzani A, Pluchino N, Luisi S, Luisi L (2007) Estrogen, cognition and female ageing. Hum Reprod Update 13:175–187

    Article  CAS  Google Scholar 

  2. World Health Organization (2007) Women, ageing and health: a framework for action focus on gender. WHO Press, Geneva

    Google Scholar 

  3. Parker WH, Broder MS, Liu Z, Shoupe D, Farquhar C, Berek JS (2005) Ovarian conservation at the time of hysterectomy for benign disease. Obstet Gynecol 2005 106:219–226

    Article  Google Scholar 

  4. Petrovska S, Dejanova B, Jurisic V (2012) Estrogens: mechanisms of neuroprotective effects J Physiol Biochem 68:455–460

    Article  CAS  Google Scholar 

  5. McEwen BS, Alves SE (1999) Estrogen actions in the central nervous system. Endocr Rev 20:279–307

    CAS  PubMed  Google Scholar 

  6. de Chaves G, Moretti M, Castro AA et al (2009) Effects of long-term ovariectomy on anxiety and behavioral despair in rats. Physiol Behav 97:420–425

    Article  Google Scholar 

  7. Baeza I, De Castro NM, Giménez-Llort L, De la Fuente M (2010) Ovariectomy, a model of menopause in rodents, causes a premature aging of the nervous and immune systems. J Neuroimmunol 219:90–99

    Article  CAS  Google Scholar 

  8. Signorelli SS, Neri S, Sciacchitano S et al (2006) Behaviour of some indicators of oxidative stress in postmenopausal and fertile women. Maturitas 53:77–82

    Article  CAS  Google Scholar 

  9. Tan MN, Kartal M, Guldal D (2014) The effect of physical activity and body mass index on menopausal symptoms in Turkish women: a cross-sectional study in primary care. BMC Womens Health 14:38

    Article  Google Scholar 

  10. Kaidah S, Soejono SK, Partadiredja G (2016) Exercise improves hippocampal estrogen and spatial memory of ovariectomized rats. Bratisl Med J 117:94–99

    Article  CAS  Google Scholar 

  11. Mishr N, Mishra VN, Devanshi (2011) Exercise beyond menopause: dos and don’ts. J Midlife Health 2:51–56

    Google Scholar 

  12. Justine M, Azizan A, Hassan V, Salleh Z, Manaf H (2013) Barriers to participation in physical activity and exercise among middle-aged and elderly individuals. Singap Med J 54:581–586

    Article  Google Scholar 

  13. Coquart JBJ, Lemaire C, Dubart AE, Luttembacher DP, Douillard C, Garcin M (2008) Intermittent versus continuous exercise: effects of perceptually lower exercise in obese women. Med Sci Sports Exerc 40:1546–1553

    Article  Google Scholar 

  14. Gibala MJ, McGee SL (2008) Metabolic adaptations to short-term high-intensity interval training: a little pain for a lot of gain? Exerc Sport Sci Rev 36:58–63

    Article  Google Scholar 

  15. Racil G, Ounis OB, Hammouda O et al (2013) Effects of high vs. moderate exercise intensity during interval training on lipids and adiponectin levels in obese young females. Eur J Appl Physiol 113:2531–2540

    Article  CAS  Google Scholar 

  16. Delwing-de Lima D, Ulbricht ASSF., Werlang-Coelho C et al (2017) Effects of two aerobic exercise training protocols on parameters of oxidative stress in the blood and liver of obese rats. J Physiol Sci. https://doi.org/10.1007/s12576-017-0584-2

    Article  PubMed  Google Scholar 

  17. Afzalpour ME, Chadorneshin HT, Foadoddini M, Eivari HA (2015) Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain. Physiol Behav 147:78–83

    Article  CAS  Google Scholar 

  18. Agustiningsih D, Soejono SK, Soesatyo MHNE., Prakosa D (2015) Exercise induces the synthesis of estrogen in ovariectomized Sprague–Dawley rats ventricular myocardium trough increase expression of CYP19 aromatase. Sport Sci Health 11:337–343

    Article  Google Scholar 

  19. Brooks GA, White TP (1978) Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol Respir Environ Exerc Physiol 45:1009–1015

    CAS  PubMed  Google Scholar 

  20. Hritcu L, Stefan M, Brandsch R, Mihasan M (2013) 6-Hydroxy-l-nicotine from arthrobacter nicotinovorans sustain spatial memory formation by decreasing brain oxidative stress in rats. J Physiol Biochem 69:25–34

    Article  CAS  Google Scholar 

  21. Marques-Aleixo I, Santos-Alves E, Balca MM et al (2015) Physical exercise improves brain cortex and cerebellum mitochondrial bioenergetics and alters apoptotic, dynamic and auto(mito)phagy markers. Neuroscience 301:480–495

    Article  CAS  Google Scholar 

  22. Iwai K, Nakaya N, Kawasaki Y, Matsue H (2002) Antioxidative functions of natto, a kind of fermented soybeans: effect on LDL oxidation and lipid metabolism in cholesterol-fed rats. J Agric Food Chem 50:3597–3601

    Article  CAS  Google Scholar 

  23. Gülçin I, Küfrevioǧlu ÖI, Oktay M, Büyükokuroǧlu ME (2004) Antioxidant, antimicrobial, antiulcer and analgesic activities of nettle (Urtica dioica L.). J Ethnopharmacol 90:205–215

    Article  Google Scholar 

  24. Singh RP, Murthy KNC, Jayaprakasha GK (2002) Studies on the antioxidant activity of pomegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 50:81–86

    Article  CAS  Google Scholar 

  25. Rauf S, Soejono SK, Partadiredja G (2015) Effects of treadmill exercise training on cerebellar estrogen and estrogen receptors, serum estrogen, and motor coordination performance of ovariectomized rats. Iran J Basic Med Sci 18:587–592

    PubMed  PubMed Central  Google Scholar 

  26. Behr GA, Schnorr CE, Simoes-Pires A, Motta LLD, Frey BN, Moreira JCF (2012) Increased cerebral oxidative damage and decreased antioxidant defenses in ovariectomized and sham-operated rats supplemented with vitamin A. Cell Biol Toxicol 28:317–330

    Article  CAS  Google Scholar 

  27. Ciobica A, Olteanu Z, Padurariu M, Hritcu L (2012) The effects of pergolide on memory and oxidative stress in a rat model of Parkinson’s disease. J Physiol Biochem 68:59–69

    Article  CAS  Google Scholar 

  28. Borrás C, Gambini J, Gómez-Cabrera MC et al (2005) 17β-oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFЌB cascade. Aging Cell 4:113–118

    Article  Google Scholar 

  29. Vina J, Gambini J, Lopez-GruesoR (2011) Females live longer than males: role of oxidative stress. Curr Pharm Des 17:3959–3965

    Article  CAS  Google Scholar 

  30. Evsen MS, Ozler A, Gocmez C et al (2013) Effects of estrogen, estrogen/progesteron combination and genistein treatments on oxidant/antioxidant status in the brain of ovariectomized rats. Eur Rev Med Pharmacol Sci 17:1869–1873

    CAS  PubMed  Google Scholar 

  31. Aksu I, Topcu A, Camsari UM, Acikgoz O (2009) Effect of acute and chronic exercise on oxidant–antioxidant equilibrium in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 452:281–285

    Article  CAS  Google Scholar 

  32. Oliveira PJ, Moreira PI (2012) Physical exercise as a possible strategy for brain protection: evidence from mitochondrial-mediated mechanisms. Prog Neurobiol 99:149–162

    Article  Google Scholar 

  33. Pingitore A, Lima GPP, Mastorci F, Quinones A, Iervasi G, Vassalle C (2015) Exercise and oxidative stress: potential effects of antioxidant dietary strategies in sports. Nutrition 31:916–922

    Article  CAS  Google Scholar 

  34. Rattan SI (2004) Aging, anti-aging, and hormesis. Mech Ageing Dev 125:285–289

    Article  CAS  Google Scholar 

  35. Radak Z, Marton O, Nagy E, Koltai E, Goto S (2013) The complex role of physical exercise and reactive oxygen species on brain. J Sport Helath Sci 2:87–93

    Article  Google Scholar 

  36. Daud DM, Karim AAH, Mohammad M, Hamid NAA, Ngah WZW (2006) Effect of exercise intensity on antioxidant enzymatic activities in sedentary adults. Malay J Biochem Mol Biol 13:37–47

    CAS  Google Scholar 

  37. Radak Z, Ishihara K, Tekus E et al (2017) Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biol 12:285–290

    Article  CAS  Google Scholar 

  38. Melisa A, Bradley-Whitman MA, Timmons MD (2014) Nucleic acid oxidation: an early feature of Alzheimer’s disease. J Neurochem 128:294–304

    Article  Google Scholar 

  39. Liu J, Head E, Gharib AM (2002) Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-l-carnitine and/or R-α-lipoic acid. PNAS 99:2356–2361

    Article  CAS  Google Scholar 

  40. Liu R, Liu IY, Bi X (2003) Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. PNAS 100:8526–8531

    Article  CAS  Google Scholar 

  41. Garcia PC, Real CC, Ferreira AFB, Alouche SR, Britto LRG, Pires RS (2012) Different protocols of physical exercise produce different effects on synaptic and structural proteins in motor areas of the rat brain. Brain Res 1456:36–48

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by a grant from the Indonesia Endowment Fund for Education, Ministry of Finance, the Republic of Indonesia (Grant number: PRJ-956/LPDP/2014). The authors would like to thank Suparno (Department of Physiology, Faculty of Medicine, Universitas Gadjah Mada) and Yulianto (Department of PAU, Universitas Gadjah Mada) for their technical assistance, as well as Erik C Hookom for the language editing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ginus Partadiredja.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The Ethics Committee of the Faculty of Medicine, Universitas Gadjah Mada has approved all experimental procedures in this study (approval number: KE/FK/217/EC/2016).

Informed consent

There is no informed consent for this study since the study was not conducted on humans.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rauf, S., Soesatyo, M., Agustiningsih, D. et al. Intermittent exercise improves working memory and locomotor activity by attenuating oxidative stress in the prefrontal cortex and cerebellum of ovariectomized rats. Sport Sci Health 14, 615–624 (2018). https://doi.org/10.1007/s11332-018-0470-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11332-018-0470-1

Keywords

Navigation