Metabolic Brain Disease

, Volume 34, Issue 1, pp 21–37 | Cite as

Neuroprotective effects of exercise in rodent models of memory deficit and Alzheimer's

  • Zahra Jahangiri
  • Zahra GholamnezhadEmail author
  • Mahmoud Hosseini
Review Article


Alzheimer's disease (AD) is a fastest growing neurodegenerative condition with no standard treatment. There are growing evidence about the beneficial effects of exercise in brain health promotion and slowing the cognitive decline. The aim of this study was to review the protective mechanisms of treadmill exercise in different models of rodent memory deficits. Online literature database, including PubMed-Medline, Scopus, Google scholar were searched from 2003 till 2017. Original article with English language were chosen according to following key words in the title: (exercise OR physical activity) AND (memory OR learning). Ninety studies were finally included in the qualitative synthesis. The results of these studies showed the protective effects of exercise on AD induced neurodegerative and neuroinflammatory process. Neuroperotective effects of exercise on the hippocampus seem to be increasing in immediate-early gene c-Fos expression in dentate gyrus; enhancing the Wnt3 expression and inhibiting glycogen synthase kinase-3β expression; increasing the 5-bro-mo-2'-deoxyridine-positive and doublecortin-positive cells (dentate gyrus); increasing the level of astrocytes glial fibrillary acidic protein and decrease in S100B protein, increasing in blood brain barrier integrity; prevention of oxidative stress injury, inducing morphological changes in astrocytes in the stratum radiatum of cornu ammonis 1(CA1) area; increase in cell proliferation and suppress apoptosis in dentate gyrus; increase in brain-derived neurotrophic factor and tropomyosin receptor kinase B expressions; enhancing the glycogen levels and normalizing the monocarboxylate transporter 2 expression.


Alzheimer' disease Neurodegeneration Exercise Memory Learning Animal models 


Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


  1. Abareshi A et al (2016) The effects of captopril on lipopolysaccharide induced learning and memory impairments and the brain cytokine levels and oxidative damage in rats. Life Sci 167:46–56. CrossRefPubMedGoogle Scholar
  2. Aguiar AS Jr 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 132:560–567. CrossRefPubMedGoogle Scholar
  3. Ahn JH et al (2016) Long-Term Exercise Improves Memory Deficits via Restoration of Myelin and Microvessel Damage, and Enhancement of Neurogenesis in the Aged Gerbil Hippocampus After Ischemic Stroke. Neurorehabil Neural Repair 30:894–905. CrossRefPubMedGoogle Scholar
  4. Albeck DS, Sano K, Prewitt GE, Dalton L (2006) Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res 168:345–348. CrossRefPubMedGoogle Scholar
  5. Anaeigoudari A et al (2015a) Lipopolysaccharide-induced memory impairment in rats is preventable using 7-nitroindazole. Arq Neuropsiquiatr 73:784–790. CrossRefPubMedGoogle Scholar
  6. Anaeigoudari A et al (2015b) The effects of L-arginine on spatial memory and synaptic plasticity impairments induced by lipopolysaccharide. Adv Biomed Res 4:202. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Anaeigoudari A, Soukhtanloo M, Reisi P, Beheshti F, Hosseini M (2016a) Inducible nitric oxide inhibitor aminoguanidine, ameliorates deleterious effects of lipopolysaccharide on memory and long term potentiation in rat. Life Sci 158:22–30. CrossRefPubMedGoogle Scholar
  8. Anaeigoudari A et al (2016b) Neuronal nitric oxide synthase has a role in the detrimental effects of lipopolysaccharide on spatial memory and synaptic plasticity in rats. Pharmacol Rep 68:243–249. CrossRefPubMedGoogle Scholar
  9. Archer T, Badgaiyan RD, Blum K (2017) Physical Exercise Interventions for Drug Addictive Disorders. J Reward Defic Syndr Addict Sci 3:17–20CrossRefGoogle Scholar
  10. Azizi-Malekabadi H, Hosseini M, Saffarzadeh F, Karami R, Khodabandehloo F (2011) Chronic treatment with the nitric oxide synthase inhibitor, L-NAME, attenuates estradiol-mediated improvement of learning and memory in ovariectomized rats. Clinics 66:673–679CrossRefGoogle Scholar
  11. Azizi-Malekabadi H, Hosseini M, Soukhtanloo M, Sadeghian R, Fereidoni M, Khodabandehloo F (2012) Different effects of scopolamine on learning, memory, and nitric oxide metabolite levels in hippocampal tissues of ovariectomized and Sham-operated rats. Arq Neuropsiquiatr 70:447–452CrossRefGoogle Scholar
  12. Baghcheghi Y et al (2017) The effects of vitamin E on brain derived neurotrophic factor, tissues oxidative damage and learning and memory of juvenile hypothyroid rats. Metab Brain Dis 33(3):713–724. CrossRefPubMedGoogle Scholar
  13. Baghcheghi Y, Hosseini M, Beheshti F, Salmani H, Anaeigoudari A (2018) Thymoquinone reverses learning and memory impairments and brain tissue oxidative damage in hypothyroid juvenile rats. Arq Neuropsiquiatr 76:32–40. CrossRefPubMedGoogle Scholar
  14. Bargi R, Asgharzadeh F, Beheshti F, Hosseini M, Sadeghnia HR, Khazaei M (2017) The effects of thymoquinone on hippocampal cytokine level, brain oxidative stress status and memory deficits induced by lipopolysaccharide in rats. Cytokine 96:173–184. CrossRefPubMedGoogle Scholar
  15. Beheshti F, Hosseini M, Shafei MN, Soukhtanloo M, Ghasemi S, Vafaee F, Zarepoor L (2017) The effects of Nigella sativa extract on hypothyroidism-associated learning and memory impairment during neonatal and juvenile growth in rats. Nutr Neurosci 20:49–59. CrossRefPubMedGoogle Scholar
  16. Benedict C et al (2013) Association between physical activity and brain health in older adults. Neurobiol Aging 34:83–90. CrossRefPubMedGoogle Scholar
  17. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464:529–535. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cardoso FDS et al (2017) Aerobic exercise reduces hippocampal ERK and p38 activation and improves memory of middle-aged rats. Hippocampus 27:899–905. CrossRefPubMedGoogle Scholar
  19. Cassilhas RC, Tufik S, de Mello MT (2016) Physical exercise, neuroplasticity, spatial learning and memory. Cell Mol Life Sci 73:975–983. CrossRefPubMedGoogle Scholar
  20. Chaddock L et al (2010) A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children. Brain Res 1358:172–183. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Chae CH, Kim HT (2009) Forced, moderate-intensity treadmill exercise suppresses apoptosis by increasing the level of NGF and stimulating phosphatidylinositol 3-kinase signaling in the hippocampus of induced aging rats. Neurochem Int 55:208–213. CrossRefPubMedGoogle Scholar
  22. Chen K, Zhang L, Tan M, Lai CS, Li A, Ren C, So KF (2017) Treadmill exercise suppressed stress-induced dendritic spine elimination in mouse barrel cortex and improved working memory via BDNF/TrkB pathway. Transcult Psychiatry 7:e1069. CrossRefGoogle Scholar
  23. Chen Y et al (2013) A non-transgenic mouse model (icv-STZ mouse) of Alzheimer's disease: similarities to and differences from the transgenic model (3xTg-AD mouse). Molecular neurobiology 47:711–725. CrossRefPubMedGoogle Scholar
  24. Chennaoui M et al (2015) Effects of exercise on brain and peripheral inflammatory biomarkers induced by total sleep deprivation in rats. J Inflamm (Lond) 12:56. CrossRefGoogle Scholar
  25. Christie BR, Swann SE, Fox CJ, Froc D, Lieblich SE, Redila V, Webber A (2005) Voluntary exercise rescues deficits in spatial memory and long-term potentiation in prenatal ethanol-exposed male rats. Eur J Neurosci 21:1719–1726. CrossRefPubMedGoogle Scholar
  26. Clark A, Mach N (2016) Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr 13:43. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Cui J et al (2018) Effects of exercise on learning and memory, oxidative stress and nNOS expression in marginal division of striatum of the ovariectomized rats. J Sports Med Phys Fitness 58(3):356–365. CrossRefPubMedGoogle Scholar
  28. Czerniawski J, Miyashita T, Lewandowski G, Guzowski JF (2015) Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: Evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav Immun 44:159–166. CrossRefPubMedGoogle Scholar
  29. Dao AT, Zagaar MA, Levine AT, Salim S, Eriksen JL, Alkadhi KA (2013) Treadmill exercise prevents learning and memory impairment in Alzheimer's disease-like pathology. Curr Alzheimer Res 10:507–515CrossRefGoogle Scholar
  30. de Senna PN et al (2017) Physical exercise reverses spatial memory deficit and induces hippocampal astrocyte plasticity in diabetic rats. Brain Res 1655:242–251. CrossRefPubMedGoogle Scholar
  31. de Senna PN et al (2011) Effects of physical exercise on spatial memory and astroglial alterations in the hippocampus of diabetic rats. Metab Brain Dis 26:269–279. CrossRefPubMedGoogle Scholar
  32. Dinas PC, Koutedakis Y, Flouris AD (2011) Effects of exercise and physical activity on depression. Ir J Med Sci 180:319–325. CrossRefPubMedGoogle Scholar
  33. Duzel E, van Praag H, Sendtner M (2016) Can physical exercise in old age improve memory and hippocampal function? Brain 139:662–673. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Fernandes J et al (2013) Aerobic exercise attenuates inhibitory avoidance memory deficit induced by paradoxical sleep deprivation in rats. Brain Res 1529:66–73. CrossRefPubMedGoogle Scholar
  35. Flores MF, Martins A, Schimidt HL, Santos FW, Izquierdo I, Mello-Carpes PB, Carpes FP (2014) Effects of green tea and physical exercise on memory impairments associated with aging. Neurochem Int 78:53–60. CrossRefPubMedGoogle Scholar
  36. Ghafari S, Golalipour MJ (2014) Prenatal morphine exposure reduces pyramidal neurons in CA1, CA2 and CA3 subfields of mice hippocampus. Iran J Basic Med Sci 17:155–161PubMedPubMedCentralGoogle Scholar
  37. Ghasemi M, Zendehbad B, Zabihi H, Hosseini M, Hadjzadeh MA, Hayatdavoudi P (2016) Beneficial Effect of Leptin on Spatial Learning and Memory in Streptozotocin-Induced Diabetic Rats. Balkan Med J 33:102–107. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ghodrati-Jaldbakhan S, Ahmadalipour A, Rashidy-Pour A, Vafaei AA, Miladi-Gorji H, Alizadeh M (2017) Low- and high-intensity treadmill exercise attenuates chronic morphine-induced anxiogenesis and memory impairment but not reductions in hippocampal BDNF in female rats. Brain Res 1663:20–28. CrossRefPubMedGoogle Scholar
  39. Gholamnezhad Z, Boskabady MH, Hosseini M, Sankian M, Khajavi Rad A (2014) Evaluation of immune response after moderate and overtraining exercise in wistar rat. Iran J Basic Med Sci 17:1–8PubMedPubMedCentralGoogle Scholar
  40. Global Recommendations on Physical Activity for Health. (2010). In World Health Organization, Geneva, p 8Google Scholar
  41. Gomez-Pinilla F, Hillman C (2013) The influence of exercise on cognitive abilities. Compr Physiol 3:403–428. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hashemi Nosrat Abadi T, Vaghef L, Babri S, Mahmood-Alilo M, Beirami M (2013) Effects of different exercise protocols on ethanol-induced spatial memory impairment in adult male rats. Alcohol 47:309–316. CrossRefPubMedGoogle Scholar
  43. Heo YM, Shin MS, Kim SH, Kim TW, Baek SB, Baek SS (2014a) Treadmill exercise ameliorates disturbance of spatial learning ability in scopolamine-induced amnesia rats. J Exerc Rehabil 10:155–161. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Heo YM, Shin MS, Lee JM, Kim CJ, Baek SB, Kim KH, Baek SS (2014b) Treadmill exercise ameliorates short-term memory disturbance in scopolamine-induced amnesia rats. Int Neurourol J 18:16–22. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Himi N et al (2016) Exercise in the Early Stage after Stroke Enhances Hippocampal Brain-Derived Neurotrophic Factor Expression and Memory Function Recovery. J Stroke Cerebrovasc Dis 25:2987–2994. CrossRefPubMedGoogle Scholar
  46. Hosseini M, Headari R, Oryan S, Hadjzadeh MA, Saffarzadeh F, Khazaei M (2010) The effect of chronic administration of L-arginine on the learning and memory of estradiol-treated ovariectomized rats tested in the morris water maze. Clinics 65:803–807CrossRefGoogle Scholar
  47. Hosseini M, Mohammadpour T, Karami R, Rajaei Z, Reza Sadeghnia H, Soukhtanloo M (2015) Effects of the hydro-alcoholic extract of Nigella sativa on scopolamine-induced spatial memory impairment in rats and its possible mechanism. Chin J Integr Med 21:438–444. CrossRefPubMedGoogle Scholar
  48. Hosseini M, Nemati Karimooy HA, Hadjzadeh MA, Safari V (2011) Inducible nitric oxide synthase inhibitor aminoguanidine, differently affects Morris water maze tasks of ovariectomized and naive female rats. Acta Physiol Hung 98:421–432. CrossRefPubMedGoogle Scholar
  49. Huang CX et al (2013) Exercise-induced changes of the capillaries in the cortex of middle-aged rats. Neuroscience 233:139–145. CrossRefPubMedGoogle Scholar
  50. Hwang DS et al (2016) Treadmill Exercise Improves Memory Function Depending on Circadian Rhythm Changes in Mice. Int Neurourol J 20:S141–S149. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jack CR Jr, Holtzman DM (2013) Biomarker modeling of Alzheimer's disease. Neuron 80:1347–1358. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jamialahmadi K, Sadeghnia HR, Mohammadi G, Kazemabad AM, Hosseini M (2013) Glucosamine alleviates scopolamine induced spatial learning and memory deficits in rats. Pathophysiology : the official journal of the International Society for. Pathophysiology 20:263–267. CrossRefPubMedGoogle Scholar
  53. Jee YS et al (2008) Effects of treadmill exercise on memory and c-Fos expression in the hippocampus of the rats with intracerebroventricular injection of streptozotocin. Neurosci Lett 443:188–192. CrossRefPubMedGoogle Scholar
  54. Jin JJ, Ko IG, Kim SE, Shin MS, Kim SH, Jee YS (2014) Swimming exercise ameliorates multiple sclerosis-induced impairment of short-term memory by suppressing apoptosis in the hippocampus of rats. J Exerc Rehabil 10:69–74. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Johansen-Berg H, Duzel E (2016) Neuroplasticity: Effects of Physical and Cognitive activity on brain structure and function. Neuroimage 131:1–3CrossRefGoogle Scholar
  56. Jung SY, Kim DY (2017) Treadmill exercise improves motor and memory functions in cerebral palsy rats through activation of PI3K-Akt pathway. J Exerc Rehabil 13:136–142. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Kaidah S, Soejono SK, Partadiredja G (2016) Exercise improves hippocampal estrogen and spatial memory of ovariectomized rats. Bratisl Lek Listy 117:94–99PubMedGoogle Scholar
  58. Karimi S, Hejazian SH, Alikhani V, Hosseini M (2015) The effects of tamoxifen on spatial and nonspatial learning and memory impairments induced by scopolamine and the brain tissues oxidative damage in ovariectomized rats. Adv Biol Res 4:196. CrossRefGoogle Scholar
  59. Kim DM, Leem YH (2016) Chronic stress-induced memory deficits are reversed by regular exercise via AMPK-mediated BDNF induction. Neuroscience 324:271–285. CrossRefPubMedGoogle Scholar
  60. Kim DY, Jung SY, Kim K, Kim CJ (2016) Treadmill exercise ameliorates Alzheimer disease-associated memory loss through the Wnt signaling pathway in the streptozotocin-induced diabetic rats. J Exerc Rehabil 12:276–283. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kim K, Sung YH, Seo JH, Lee SW, Lim BV, Lee CY, Chung YR (2015a) Effects of treadmill exercise-intensity on short-term memory in the rats born of the lipopolysaccharide-exposed maternal rats. J Exerc Rehabil 11:296–302. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kim SE 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 45:357–365. CrossRefPubMedGoogle Scholar
  63. Kim SE, Ko IG, Park CY, Shin MS, Kim CJ, Jee YS (2013) Treadmill and wheel exercise alleviate lipopolysaccharide-induced short-term memory impairment by enhancing neuronal maturation in rats. Mol Med Rep 7:31–36. CrossRefPubMedGoogle Scholar
  64. Kim TW, Sung YH (2017) Regular exercise promotes memory function and enhances hippocampal neuroplasticity in experimental autoimmune encephalomyelitis mice. Neuroscience 346:173–181. CrossRefPubMedGoogle Scholar
  65. Kim YH, Sung YH, Lee HH, Ko IG, Kim SE, Shin MS, Kim BK (2014) Postnatal treadmill exercise alleviates short-term memory impairment by enhancing cell proliferation and suppressing apoptosis in the hippocampus of rat pups born to diabetic rats. J Exerc Rehabil 10:209–217. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Kim YM et al (2015b) Treadmill exercise improves short-term memory by enhancing hippocampal cell proliferation in quinolinic acid-induced Huntington's disease rats. J Exerc Rehabil 11:5–11. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Kitazawa M, Medeiros R, Laferla FM (2012) Transgenic mouse models of Alzheimer disease: developing a better model as a tool for therapeutic interventions. Curr Pharm Des 18:1131–1147CrossRefGoogle Scholar
  68. Kraska A et al (2012) In vivo cross-sectional characterization of cerebral alterations induced by intracerebroventricular administration of streptozotocin. PloS one 7:e46196. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Krstic D, Knuesel I (2013) Deciphering the mechanism underlying late-onset Alzheimer disease. Nat Rev Neurol 9:25–34. CrossRefPubMedGoogle Scholar
  70. Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN, Katzmarzyk PT (2012) Effect of physical inactivity on major non-communicable diseases worldwide: an analysis of burden of disease and life expectancy. Lancet 380:219–229. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lee JW, Lee YK, Yuk DY, Choi DY, Ban SB, Oh KW, Hong JT (2008) Neuro-inflammation induced by lipopolysaccharide causes cognitive impairment through enhancement of beta-amyloid generation. J Neuroinflammation 5:37. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Li C, Liu Y, Yin S, Lu C, Liu D, Jiang H, Pan F (2015) Long-term effects of early adolescent stress: dysregulation of hypothalamic-pituitary-adrenal axis and central corticotropin releasing factor receptor 1 expression in adult male rats. Behav Brain Res 288:39–49. CrossRefPubMedGoogle Scholar
  73. Lin TW et al (2015) Running exercise delays neurodegeneration in amygdala and hippocampus of Alzheimer's disease (APP/PS1) transgenic mice. Neurobiol Learn Mem 118:189–197. CrossRefPubMedGoogle Scholar
  74. Lister JP, Barnes CA (2009) Neurobiological changes in the hippocampus during normative aging. Arch Neurol 66:829–833. CrossRefPubMedGoogle Scholar
  75. Liu HL, Zhao G, Cai K, Zhao HH, Shi LD (2011) Treadmill exercise prevents decline in spatial learning and memory in APP/PS1 transgenic mice through improvement of hippocampal long-term potentiation. Behav Brain Res 218:308–314. CrossRefPubMedGoogle Scholar
  76. Loprinzi PD, Edwards MK, Frith E (2017) Potential avenues for exercise to activate episodic memory-related pathways: a narrative review. Eur J Neurosci 46(5):2067–2077. CrossRefGoogle Scholar
  77. Lovatel GA et al (2013) Treadmill exercise induces age-related changes in aversive memory, neuroinflammatory and epigenetic processes in the rat hippocampus. Neurobiol Learn Mem 101:94–102. CrossRefPubMedGoogle Scholar
  78. Mao XY, Yu J, Liu ZQ, Zhou HH (2015) Apigenin attenuates diabetes-associated cognitive decline in rats via suppressing oxidative stress and nitric oxide synthase pathway. Int J Clin Exp Med 8:15506–15513PubMedPubMedCentralGoogle Scholar
  79. Meeusen R (2005) Exercise and the brain: insight in new therapeutic modalities. Ann Transplant 10:49–51PubMedGoogle Scholar
  80. Mohammadpour T, Hosseini M, Naderi A, Karami R, Sadeghnia HR, Soukhtanloo M, Vafaee F (2015) Protection against brain tissues oxidative damage as a possible mechanism for the beneficial effects of Rosa damascena hydroalcoholic extract on scopolamine induced memory impairment in rats. Nutr Neurosci 18:329–336. CrossRefPubMedGoogle Scholar
  81. Morgan JA, Corrigan F, Baune BT (2015) Effects of physical exercise on central nervous system functions: a review of brain region specific adaptations. J Mol Psychiatry 3(1):3. CrossRefPubMedPubMedCentralGoogle Scholar
  82. Mousavi SM, Niazmand S, Hosseini M, Hassanzadeh Z, Sadeghnia HR, Vafaee F, Keshavarzi Z (2015) Beneficial Effects of Teucrium polium and Metformin on Diabetes-Induced Memory Impairments and Brain Tissue Oxidative Damage in Rats. Int J Alzheimers Dis 2015:493729. CrossRefPubMedPubMedCentralGoogle Scholar
  83. Muller AP et al (2012) Physical exercise exacerbates memory deficits induced by intracerebroventricular STZ but improves insulin regulation of H(2)O(2) production in mice synaptosomes. J Alzheimers Dis 30:889–898. CrossRefPubMedGoogle Scholar
  84. Nazem A, Sankowski R, Bacher M, Al-Abed Y (2015) Rodent models of neuroinflammation for Alzheimer's disease. J Neuroinflammation 12:74. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Neves BH, Menezes J, Souza MA, Mello-Carpes PB (2015) Physical exercise prevents short and long-term deficits on aversive and recognition memory and attenuates brain oxidative damage induced by maternal deprivation. Physiol Behav 152:99–105. CrossRefPubMedGoogle Scholar
  86. Park CY, Lee SH, Kim BK, Shin MS, Kim CJ, Kim H (2013) Treadmill exercise ameliorates impairment of spatial learning ability through enhancing dopamine expression in hypoxic ischemia brain injury in neonatal rats. J Exerc Rehabil 9:406–412. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Park SH, Song M (2016) Effects of aerobic and anaerobic exercise on spatial learning ability in hypothyroid rats: a pilot study. J Phys Ther Sci 28:3489–3492. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Pimlott N (2010) The miracle drug. Can Fam Physician 56(5):407PubMedGoogle Scholar
  89. Puzzo D, Gulisano W, Palmeri A, Arancio O (2015) Rodent models for Alzheimer's disease drug discovery. Expert Opin Drug Discovery 10:703–711. CrossRefGoogle Scholar
  90. Roig M, Nordbrandt S, Geertsen SS, Nielsen JB (2013) The effects of cardiovascular exercise on human memory: a review with meta-analysis. Neurosci Biobehav Rev 37:1645–1666. CrossRefPubMedGoogle Scholar
  91. Saadati H, Esmaeili-Mahani S, Esmaeilpour K, Nazeri M, Mazhari S, Sheibani V (2015) Exercise improves learning and memory impairments in sleep deprived female rats. Physiol Behav 138:285–291. CrossRefPubMedGoogle Scholar
  92. Salari M, Sheibani V, Saadati H, Pourrahimi A, khaksarihadad M, Esmaeelpour K, Khodamoradi M (2015) The compensatory effect of regular exercise on long-term memory impairment in sleep deprived female rats. Behav Process 119:50–57. CrossRefGoogle Scholar
  93. Seo TB et al (2010) Effect of treadmill exercise on Purkinje cell loss and astrocytic reaction in the cerebellum after traumatic brain injury. Neurosci Lett 481:178–182. CrossRefPubMedGoogle Scholar
  94. Shafiee SM, Vafaei AA, Rashidy-Pour A (2016) Effects of maternal hypothyroidism during pregnancy on learning, memory and hippocampal BDNF in rat pups: Beneficial effects of exercise. Neuroscience 329:151–161. CrossRefPubMedGoogle Scholar
  95. Shih PC, Yang YR, Wang RY (2013) Effects of exercise intensity on spatial memory performance and hippocampal synaptic plasticity in transient brain ischemic rats. PloS one 8:e78163. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Shima T et al (2017) Moderate exercise ameliorates dysregulated hippocampal glycometabolism and memory function in a rat model of type 2 diabetes. Diabetologia 60:597–606. CrossRefPubMedGoogle Scholar
  97. Shimada H, Hamakawa M, Ishida A, Tamakoshi K, Nakashima H, Ishida K (2013) Low-speed treadmill running exercise improves memory function after transient middle cerebral artery occlusion in rats. Behav Brain Res 243:21–27. CrossRefPubMedGoogle Scholar
  98. Siette J, Westbrook RF, Cotman C, Sidhu K, Zhu W, Sachdev P, Valenzuela MJ (2013) Age-specific effects of voluntary exercise on memory and the older brain. Biol Psychiatry 73:435–442. CrossRefPubMedGoogle Scholar
  99. Sim YJ (2014) Treadmill exercise alleviates impairment of spatial learning ability through enhancing cell proliferation in the streptozotocin-induced Alzheimer's disease rats. J Exerc Rehabil 10:81–88. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Sim YJ, Kim SS, Kim JY, Shin MS, Kim CJ (2004) Treadmill exercise improves short-term memory by suppressing ischemia-induced apoptosis of neuronal cells in gerbils. Neurosci Lett 372:256–261. CrossRefPubMedGoogle Scholar
  101. Skriver K, Roig M, Lundbye-Jensen J, Pingel J, Helge JW, Kiens B, Nielsen JB (2014) Acute exercise improves motor memory: exploring potential biomarkers. Neurobiol Learn Mem 116:46–58. CrossRefPubMedGoogle Scholar
  102. Stranahan AM, Martin B, Maudsley S (2012) Anti-inflammatory effects of physical activity in relationship to improved cognitive status in humans and mouse models of Alzheimer's disease. Curr Alzheimer Res 9:86–92CrossRefGoogle Scholar
  103. Vanzella C et al (2017) Forced Treadmill Exercise Prevents Spatial Memory Deficits in Aged Rats Probably Through the Activation of Na+, K+-ATPase in the Hippocampus. Neurochem Res 42:1422–1429. CrossRefPubMedGoogle Scholar
  104. Voss MW, Vivar C, Kramer AF, van Praag H (2013) Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci 17:525–544. CrossRefPubMedPubMedCentralGoogle Scholar
  105. Wang J-Q et al (2014) Brain Aging and AD-Like Pathology in Streptozotocin-Induced Diabetic Rats. J Diabetes Res 2014:12. CrossRefGoogle Scholar
  106. Wang S et al (2015) Effects of long-term exercise on spatial learning, memory ability, and cortical capillaries in aged rats. Med Sci Monit 21:945–954. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Wu CW et al (2007) Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J Neurochem 103:2471–2481. CrossRefPubMedGoogle Scholar
  108. Xiong JY, Li SC, Sun YX, Zhang XS, Dong ZZ, Zhong P, Sun XR (2015) Long-term treadmill exercise improves spatial memory of male APPswe/PS1dE9 mice by regulation of BDNF expression and microglia activation. Biology Sport 32:295–300. CrossRefGoogle Scholar
  109. You JS, Kim CJ, Kim MY, Byun YG, Ha SY, Han BS, Yoon BC (2009) Long-term treadmill exercise-induced neuroplasticity and associated memory recovery of streptozotocin-induced diabetic rats: an experimenter blind, randomized controlled study. NeuroRehabilitation 24:291–297. CrossRefPubMedGoogle Scholar
  110. Zabihi H, Hosseini M, Pourganji M, Oryan S, Soukhtanloo M, Niazmand S (2014) The effects of tamoxifen on learning, memory and brain tissues oxidative damage in ovariectomized and naive female rats. Adv Biol Res 3:219. CrossRefGoogle Scholar
  111. Zagaar M, Dao A, Levine A, Alhaider I, Alkadhi K (2013) Regular exercise prevents sleep deprivation associated impairment of long-term memory and synaptic plasticity in the CA1 area of the hippocampus. Sleep 36:751–761. CrossRefPubMedPubMedCentralGoogle Scholar
  112. Zarrinkalam E, Heidarianpour A, Salehi I, Ranjbar K, Komaki A (2016) Effects of endurance, resistance, and concurrent exercise on learning and memory after morphine withdrawal in rats. Life Sci 157:19–24. CrossRefPubMedGoogle Scholar
  113. Zhou J et al (2011) Protective Role of Taurine Against Morphine-Induced Neurotoxicity in C6 Cells via Inhibition of Oxidative Stress. Neurotox Res 20:334. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Zahra Jahangiri
    • 1
    • 2
  • Zahra Gholamnezhad
    • 1
    • 2
    Email author
  • Mahmoud Hosseini
    • 3
  1. 1.Neurogenic Inflammation Research CenterMashhad University of Medical SciencesMashhadIran
  2. 2.Department of Physiology, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  3. 3.Division of Neurocognitive Sciences, Psychiatry and Behavioral Sciences Research CenterMashhad University of Medical SciencesMashhadIran

Personalised recommendations