Log in

The Interaction Effect of Sleep Deprivation and Treadmill Exercise in Various Durations on Spatial Memory with Respect to the Oxidative Status of Rats

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Sleep deprivation (SD) has deleterious effects on cognitive functions including learning and memory. However, some studies have shown that SD can improve cognitive functions. Interestingly, treadmill exercise has both impairment and improvement effects on memory function. In this study, we aimed to investigate the effect of SD for 4 (short-term) and 24 (long-term) hours, and two protocols of treadmill exercise (mild short-term and moderate long-term) on spatial memory performance, and oxidative and antioxidant markers in the serum of rats. Morris Water Maze apparatus was used to assess spatial memory performance. Also, SD was done using gentle handling method. In addition, the serum level of catalase (CAT), superoxide dismutase (SOD), malondialdehyde (MDA), and glutathione peroxidase (GSH-Px) was measured. The results showed that 24 h SD (but not 4 h) had negative effect on spatial memory performance, decreased SOD, CAT, and GSH-Px level, and increased MDA level. Long-term moderate (but not short-term mild) treadmill exercise had also negative effect on spatial memory performance, decreased SOD, CAT, and GSH-Px level, and increased MDA level. Interestingly, both protocols of treadmill exercise reversed spatial memory impairment and oxidative stress induced by 24 h SD. In conclusion, it seems that SD and treadmill exercise interact with each other, and moderate long-term exercise can reverse the negative effects of long-term SD on memory and oxidative status; although, it disrupted memory function and increased oxidative stress by itself.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

Will be made available upon a reasonable request.

References

  1. Torabi Z, Rezaie M, Aramvash A, Nasiri-Khalili MA, Nasehi M, Abedi B, Vaseghi S (2022) Interaction of lithium and sleep deprivation on memory performance and anxiety-like behavior in male Wistar rats. Behav Brain Res 113890. https://doi.org/10.1016/j.bbr.2022.113890

  2. Rezaie M, Nasehi M, Vaseghi S, Alimohammadzadeh K, Islami Vaghar M, Mohammadi-Mahdiabadi-Hasani MH, Zarrindast MR (2021) The interaction effect of sleep deprivation and cannabinoid type 1 receptor in the CA1 hippocampal region on passive avoidance memory, depressive-like behavior and locomotor activity in rats. Behav Brain Res 396:112901. https://doi.org/10.1016/j.bbr.2020.112901

    Article  CAS  PubMed  Google Scholar 

  3. Looti Bashiyan M, Nasehi M, Vaseghi S, Khalifeh S (2021) Investigating the effect of crocin on memory deficits induced by total sleep deprivation (TSD) with respect to the BDNF, TrkB and ERK levels in the hippocampus of male Wistar rats. J Psychopharmacol 2698811211000762. https://doi.org/10.1177/02698811211000762

  4. Edem EE, Nebo KE, Rimamchatin P, Bello A, Akinluyi E, Fafure A, Adeoluwa O, Adekeye A, Oremosu A (2022) Sleep disruption exacerbates cognitive dysfunction by promoting Lipid-Immune Dysregulation in the Corticohippocampal System of Pentylenetetrazol-Kindled rats. FASEB J 36(Suppl 1). https://doi.org/10.1096/fasebj.2022.36.S1.R2906

  5. Ke P, Zheng C, Liu F, Wu L, Tang Y, Wu Y, Lv D, Chen H, Qian L, Wu X, Zeng K (2022) Relationship between circadian genes and memory impairment caused by sleep deprivation. PeerJ 10:e13165. https://doi.org/10.7717/peerj.13165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hennecke E, Lange D, Steenbergen F, Fronczek-Poncelet J, Elmenhorst D, Bauer A, Aeschbach D, Elmenhorst EM (2021) Adverse interaction effects of chronic and acute sleep deficits on spatial working memory but not on verbal working memory or declarative memory. J Sleep Res 30(4):e13225. https://doi.org/10.1111/jsr.13225

    Article  PubMed  Google Scholar 

  7. Kurinec CA, Whitney P, Hinson JM, Hansen DA, Van Dongen HPA (2021) Sleep deprivation impairs binding of information with its context. Sleep 44(8). https://doi.org/10.1093/sleep/zsab113

  8. Santisteban JA, Brown TG, Ouimet MC, Gruber R (2019) Cumulative mild partial sleep deprivation negatively impacts working memory capacity but not sustained attention, response inhibition, or decision making: a randomized controlled trial. Sleep Health 5(1):101–108. https://doi.org/10.1016/j.sleh.2018.09.007

    Article  PubMed  Google Scholar 

  9. Guo B, Chen C, Yang L, Zhu R (2021) Effects of dexmedetomidine on postoperative cognitive function of sleep deprivation rats based on changes in inflammatory response. Bioengineered 12(1):7920–7928. https://doi.org/10.1080/21655979.2021.1981757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chen P, Wu H, Yao H, Zhang J, Fan W, Chen Z, Su W, Wang Y, Li P (2022) Multi-Omics Analysis reveals the systematic relationship between oral homeostasis and chronic sleep deprivation in rats. Front Immunol 13:847132. https://doi.org/10.3389/fimmu.2022.847132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lasisi TJ, Shittu ST, Abeje JI, Ogunremi KJ, Shittu SA (2021) Paradoxical sleep deprivation induces oxidative stress in the submandibular glands of Wistar rats. J Basic Clin Physiol Pharmacol. https://doi.org/10.1515/jbcpp-2020-0178

    Article  PubMed  Google Scholar 

  12. Massadeh AM, Alzoubi KH, Milhem AM, Rababa’h AM, Khabour OF (2021) Evaluating the effect of selenium on spatial memory Impairment Induced by Sleep Deprivation. Physiol Behav 113669. https://doi.org/10.1016/j.physbeh.2021.113669

  13. Khodaverdiloo A, Farhadi M, Jameie M, Jameie SB, Pirhajati V (2021) Neurogenesis in the rat neonate’s hippocampus with maternal short-term REM sleep deprivation restores by royal jelly treatment. Brain Behav 11(12):e2423. https://doi.org/10.1002/brb3.2423

    Article  PubMed  PubMed Central  Google Scholar 

  14. Lu Y, **ao Y, Tu Y, Dai W, **e Y (2022) Propofol-induced sleep ameliorates cognition impairment in sleep-deprived rats. Sleep Breath. https://doi.org/10.1007/s11325-022-02591-5

    Article  PubMed  Google Scholar 

  15. Marzabadi EA, Meftahi GH, Refahi S (2022) Pretreatment with combined low-level laser therapy and methylene blue improves learning and memory in sleep-deprived mice. Lasers Med Sci. https://doi.org/10.1007/s10103-021-03497-6

    Article  PubMed  Google Scholar 

  16. Arjmandi-Rad S, Ebrahimnejad M, Zarrindast MR, Vaseghi S (2022) Do sleep disturbances have a dual effect on Alzheimer’s Disease? Cell Mol Neurobiol. https://doi.org/10.1007/s10571-022-01228-1

    Article  PubMed  Google Scholar 

  17. Vecsey CG, Huang T, Abel T (2018) Sleep deprivation impairs synaptic tagging in mouse hippocampal slices. Neurobiol Learn Mem 154:136–140. https://doi.org/10.1016/j.nlm.2018.03.016

    Article  PubMed  PubMed Central  Google Scholar 

  18. Vaseghi S, Arjmandi-Rad S, Kholghi G, Nasehi M (2021) Inconsistent effects of sleep deprivation on memory function. EXCLI J 20:1011–1027. https://doi.org/10.17179/excli2021-3764

    Article  PubMed  PubMed Central  Google Scholar 

  19. Wu J, Dou Y, Ladiges WC (2020) Adverse neurological Effects of Short-Term Sleep Deprivation in Aging mice are prevented by SS31 peptide. Clocks Sleep 2(3):325–333. https://doi.org/10.3390/clockssleep2030024

    Article  PubMed  PubMed Central  Google Scholar 

  20. Vaccaro A, Kaplan Dor Y, Nambara K, Pollina EA, Lin C, Greenberg ME, Rogulja D (2020) Sleep loss can cause death through Accumulation of reactive oxygen species in the gut. Cell 181(6):1307–1328e1315. https://doi.org/10.1016/j.cell.2020.04.049

    Article  CAS  PubMed  Google Scholar 

  21. Zhou HR, Wu JR, Bei L, Wang BX, Xu H, Wang JT, Ma SX (2020) Hydroalcoholic extract from Abelmoschus manihot (Linn.) Medicus flower reverses sleep deprivation-evoked learning and memory deficit. Food Funct 11(10):8978–8986. https://doi.org/10.1039/d0fo02158j

    Article  CAS  PubMed  Google Scholar 

  22. Cheng O, Li R, Zhao L, Yu L, Yang B, Wang J, Chen B, Yang J (2015) Short-term sleep deprivation stimulates hippocampal neurogenesis in rats following global cerebral ischemia/reperfusion. PLoS ONE 10(6):e0125877. https://doi.org/10.1371/journal.pone.0125877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Mahboubi S, Nasehi M, Imani A, Sadat-Shirazi MS, Zarrindast MR, Vousooghi N, Noroozian M (2019) Benefit effect of REM-sleep deprivation on memory impairment induced by intensive exercise in male wistar rats: with respect to hippocampal BDNF and TrkB. Nat Sci Sleep 11:179–188. https://doi.org/10.2147/NSS.S207339

    Article  PubMed  PubMed Central  Google Scholar 

  24. Mueller AD, Meerlo P, McGinty D, Mistlberger RE (2015) Sleep and adult neurogenesis: implications for cognition and mood. Curr Top Behav Neurosci 25:151–181. https://doi.org/10.1007/7854_2013_251

    Article  PubMed  Google Scholar 

  25. El-Domiaty HF, El-Roghy ES, Salem HR (2022) Combination of magnesium supplementation with treadmill exercise improves memory deficit in aged rats by enhancing hippocampal neurogenesis and plasticity: a functional and histological study. Appl Physiol Nutr Metab 47(3):296–308. https://doi.org/10.1139/apnm-2021-0133

    Article  CAS  PubMed  Google Scholar 

  26. Yang L, Wu C, Li Y, Dong Y, Wu CY, Lee RH, Brann DW, Lin HW, Zhang Q (2022) Long-term exercise pre-training attenuates Alzheimer’s disease-related pathology in a transgenic rat model of Alzheimer’s disease. Geroscience. https://doi.org/10.1007/s11357-022-00534-2

    Article  PubMed  PubMed Central  Google Scholar 

  27. Navazani P, Vaseghi S, Hashemi M, Shafaati MR, Nasehi M (2021) Effects of Treadmill Exercise on the expression level of BAX, BAD, BCL-2, BCL-XL, TFAM, and PGC-1alpha in the Hippocampus of Thimerosal-Treated rats. Neurotox Res 39(4):1274–1284. https://doi.org/10.1007/s12640-021-00370-w

    Article  CAS  PubMed  Google Scholar 

  28. Park SS, Kim TW, Sung YH, Park YJ, Kim MK, Shin MS (2021) Treadmill Exercise ameliorates short-term memory impairment by suppressing hippocampal neuroinflammation in Poloxamer-407-Induced hyperlipidemia rats. Int Neurourol J 25(Suppl 2):S81–89. https://doi.org/10.5213/inj.2142342.171

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kim SH, Ko IG, ** JJ, Hwang L, Baek SS (2021) Treadmill exercise ameliorates impairment of spatial learning memory in pups born to old and obese mother rats. J Exerc Rehabil 17(4):234–240. https://doi.org/10.12965/jer.2142466.233

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ko YJ, Ko IG (2020) Voluntary Wheel running improves spatial learning memory by suppressing inflammation and apoptosis via inactivation of nuclear factor Kappa B in Brain inflammation rats. Int Neurourol J 24(Suppl 2):96–103. https://doi.org/10.5213/inj.2040432.216

    Article  PubMed  PubMed Central  Google Scholar 

  31. Mokhtari-Zaer A, Hosseini M, Roshan NM, Boskabady MH (2020) Treadmill exercise ameliorates memory deficits and hippocampal inflammation in ovalbumin-sensitized juvenile rats. Brain Res Bull 165:40–47. https://doi.org/10.1016/j.brainresbull.2020.09.016

    Article  CAS  PubMed  Google Scholar 

  32. Ebrahimnejad M, Azizi P, Alipour V, Zarrindast MR, Vaseghi S (2022) Complicated role of Exercise in modulating memory: a discussion of the Mechanisms involved. Neurochem Res. https://doi.org/10.1007/s11064-022-03552-w

    Article  PubMed  Google Scholar 

  33. He F, Li J, Liu Z, Chuang CC, Yang W, Zuo L (2016) Redox mechanism of reactive oxygen species in Exercise. Front Physiol 7:486. https://doi.org/10.3389/fphys.2016.00486

    Article  PubMed  PubMed Central  Google Scholar 

  34. Jahangiri Z, Gholamnezhad Z, Hosseini M, Beheshti F, Kasraie N (2019) The effects of moderate exercise and overtraining on learning and memory, hippocampal inflammatory cytokine levels, and brain oxidative stress markers in rats. J Physiol Sci 69(6):993–1004. https://doi.org/10.1007/s12576-019-00719-z

    Article  CAS  PubMed  Google Scholar 

  35. Silva RH, Abilio VC, Takatsu AL, Kameda SR, Grassl C, Chehin AB, Medrano WA, Calzavara MB, Registro S, Andersen ML, Machado RB, Carvalho RC, Ribeiro Rde A, Tufik S, Frussa-Filho R (2004) Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology 46(6):895–903. https://doi.org/10.1016/j.neuropharm.2003.11.032

    Article  CAS  PubMed  Google Scholar 

  36. De Lima MNM, Polydoro M, Laranja DC, Bonatto F, Bromberg E, Moreira JCF, Dal-Pizzol F, Schröder N (2005) Recognition memory impairment and brain oxidative stress induced by postnatal iron administration. Eur J Neurosci 21(9):2521–2528

    Article  PubMed  Google Scholar 

  37. Assaran AH, Akbarian M, Amirahmadi S, Salmani H, Shirzad S, Hosseini M, Beheshti F, Rajabian A (2022) Ellagic acid prevents oxidative stress and memory deficits in a rat model of scopolamine-induced Alzheimer’s Disease. Central Nervous System Agents in Medicinal Chemistry (formerly current Medicinal Chemistry-Central Nervous. Syst Agents) 22(3):214–227

    CAS  Google Scholar 

  38. Olayinka J, Eduviere A, Adeoluwa O, Fafure A, Adebanjo A, Ozolua R (2022) Quercetin mitigates memory deficits in scopolamine mice model via protection against neuroinflammation and neurodegeneration. Life Sci 292:120326

    Article  CAS  PubMed  Google Scholar 

  39. Souza LC, Andrade MK, Azevedo EM, Ramos DC, Bail EL, Vital MA (2022) Andrographolide attenuates short-term spatial and recognition memory impairment and neuroinflammation induced by a streptozotocin rat model of Alzheimer’s disease. Neurotox Res 40(5):1440–1454

    Article  CAS  PubMed  Google Scholar 

  40. Arjmandi-Rad S, Zarrindast MR, Shadfar S, Nasehi M (2022) The role of sleep deprivation in streptozotocin-induced Alzheimer’s disease-like sporadic dementia in rats with respect to the serum level of oxidative and inflammatory markers. Exp Brain Res. https://doi.org/10.1007/s00221-022-06471-y

    Article  PubMed  Google Scholar 

  41. Massadeh AM, Alzoubi KH, Milhem AM, Rababa’h AM, Khabour OF (2022) Evaluating the effect of selenium on spatial memory impairment induced by sleep deprivation. Physiol Behav 244:113669. https://doi.org/10.1016/j.physbeh.2021.113669

    Article  CAS  PubMed  Google Scholar 

  42. Konakanchi S, Raavi V, Ml HK, Shankar Ms V (2022) Effect of chronic sleep deprivation and sleep recovery on hippocampal CA3 neurons, spatial memory and anxiety-like behavior in rats. Neurobiol Learn Mem 187:107559. https://doi.org/10.1016/j.nlm.2021.107559

    Article  CAS  PubMed  Google Scholar 

  43. Kordestani-Moghadam P, Nasehi M, Vaseghi S, Khodagholi F, Zarrindast MR (2020) The role of sleep disturbances in depressive-like behavior with emphasis on alpha-ketoglutarate dehydrogenase activity in rats. Physiol Behav 224:113023. https://doi.org/10.1016/j.physbeh.2020.113023

    Article  CAS  PubMed  Google Scholar 

  44. In: Guide for the Care and Use of Laboratory Animals. The National Academies Collection: Reports funded by National Institutes of Health, 8th edn., Washington (DC). https://doi.org/10.17226/12910

  45. Shi HS, Luo YX, Xue YX, Wu P, Zhu WL, Ding ZB, Lu L (2011) Effects of sleep deprivation on retrieval and reconsolidation of morphine reward memory in rats. Pharmacol Biochem Behav 98(2):299–303. https://doi.org/10.1016/j.pbb.2011.01.006

    Article  CAS  PubMed  Google Scholar 

  46. Vaseghi S, Babapour V, Nasehi M, Zarrindast MR (2018) The role of CA1 CB1 receptors on lithium-induced spatial memory impairment in rats. EXCLI J 17:916–934. https://doi.org/10.17179/excli2018-1511

    Article  PubMed  PubMed Central  Google Scholar 

  47. Vaseghi S, Babapour V, Nasehi M, Zarrindast MR (2020) Synergistic but not additive effect between ACPA and lithium in the dorsal hippocampal region on spatial learning and memory in rats: isobolographic analyses. Chem Biol Interact 315:108895. https://doi.org/10.1016/j.cbi.2019.108895

    Article  CAS  PubMed  Google Scholar 

  48. Molaei P, Vaseghi S, Entezari M, Hashemi M, Nasehi M (2021) The Effect of NeuroAid (MLC901) on Cholestasis-Induced spatial memory impairment with respect to the expression of BAX, BCL-2, BAD, PGC-1alpha and TFAM genes in the Hippocampus of male Wistar rats. Neurochem Res 46(8):2154–2166. https://doi.org/10.1007/s11064-021-03353-7

    Article  CAS  PubMed  Google Scholar 

  49. Al-Dhuhli F, Al-Siyabi S, Al-Maamari H, Al-Farsi S, Albarwani S (2022) Moderate-intensity exercise training reduces vasorelaxation of mesenteric arteries: role of BKCa channels and nitric oxide. Physiol Res 71(1):67–77. https://doi.org/10.33549/physiolres.934671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gessner N, Shinbashi M, Chuluun B, Heller C, Pittaras E (2022) Handling, task complexity, time-of-day, and sleep deprivation as dynamic modulators of recognition memory in mice. Physiol Behav 251:113803

    Article  CAS  PubMed  Google Scholar 

  51. Li ZH, Cheng L, Wen C, Ding L, You QY, Zhang SB (2022) Activation of CNR1/PI3K/AKT pathway by Tanshinone IIA protects hippocampal neurons and ameliorates Sleep Deprivation-Induced Cognitive Dysfunction in rats. Front Pharmacol 13:823732. https://doi.org/10.3389/fphar.2022.823732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ghaheri S, Panahpour H, Abdollahzadeh M, Saadati H (2022) Adolescent enriched environment exposure alleviates cognitive impairments in sleep-deprived male rats: role of hippocampal brain-derived neurotrophic factor. Int J Dev Neurosci 82(2):133–145. https://doi.org/10.1002/jdn.10165

    Article  CAS  PubMed  Google Scholar 

  53. Han Y, Wang J, Zhao Q, **e X, Song R, **ao Y, Kang X, Zhang L, Zhang Y, Peng C, You Z (2020) Pioglitazone alleviates maternal sleep deprivation-induced cognitive deficits in male rat offspring by enhancing microglia-mediated neurogenesis. Brain Behav Immun 87:568–578. https://doi.org/10.1016/j.bbi.2020.02.002

    Article  CAS  PubMed  Google Scholar 

  54. Li Y, Zhang W, Liu M, Zhang Q, Lin Z, Jia M, Liu D, Lin L (2021) Imbalance of Autophagy and Apoptosis Induced by Oxidative Stress May Be Involved in Thyroid Damage Caused by Sleep Deprivation in Rats. Oxid Med Cell Longev 2021:5645090. https://doi.org/10.1155/2021/5645090

  55. Forouzanfar F, Gholami J, Foroughnia M, Payvar B, Nemati S, Khodadadegan MA, Saheb M, Hajali V (2021) The beneficial effects of green tea on sleep deprivation-induced cognitive deficits in rats: the involvement of hippocampal antioxidant defense. Heliyon 7(11):e08336. https://doi.org/10.1016/j.heliyon.2021.e08336

    Article  PubMed  PubMed Central  Google Scholar 

  56. Kang X, Jiang L, Lan F, Tang YY, Zhang P, Zou W, Chen YJ, Tang XQ (2021) Hydrogen sulfide antagonizes sleep deprivation-induced depression- and anxiety-like behaviors by inhibiting neuroinflammation in a hippocampal Sirt1-dependent manner. Brain Res Bull 177:194–202. https://doi.org/10.1016/j.brainresbull.2021.10.002

    Article  CAS  PubMed  Google Scholar 

  57. Yao ZY, Li XH, Zuo L, **ong Q, He WT, Li DX, Dong ZF (2022) Maternal sleep deprivation induces gut microbial dysbiosis and neuroinflammation in offspring rats. Zool Res 43(3):380–390. https://doi.org/10.24272/j.issn.2095-8137.2022.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tang H, Li K, Dou X, Zhao Y, Huang C, Shu F (2020) The neuroprotective effect of osthole against chronic sleep deprivation (CSD)-induced memory impairment in rats. Life Sci 263:118524. https://doi.org/10.1016/j.lfs.2020.118524

    Article  CAS  PubMed  Google Scholar 

  59. Havekes R, Bruinenberg VM, Tudor JC, Ferri SL, Baumann A, Meerlo P, Abel T (2014) Transiently increasing cAMP levels selectively in hippocampal excitatory neurons during sleep deprivation prevents memory deficits caused by sleep loss. J Neurosci 34(47):15715–15721. https://doi.org/10.1523/JNEUROSCI.2403-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Rajizadeh MA, Esmaeilpour K, Haghparast E, Ebrahimi MN, Sheibani V (2020) Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats. Brain Res 1729:146598. https://doi.org/10.1016/j.brainres.2019.146598

    Article  CAS  PubMed  Google Scholar 

  61. Peng Y, Wang W, Tan T, He W, Dong Z, Wang YT, Han H (2016) Maternal sleep deprivation at different stages of pregnancy impairs the emotional and cognitive functions, and suppresses hippocampal long-term potentiation in the offspring rats. Mol Brain 9:17. https://doi.org/10.1186/s13041-016-0197-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Junek A, Rusak B, Semba K (2010) Short-term sleep deprivation may alter the dynamics of hippocampal cell proliferation in adult rats. Neuroscience 170(4):1140–1152. https://doi.org/10.1016/j.neuroscience.2010.08.018

    Article  CAS  PubMed  Google Scholar 

  63. Grassi Zucconi G, Cipriani S, Balgkouranidou I, Scattoni R (2006) ‘one night’ sleep deprivation stimulates hippocampal neurogenesis. Brain Res Bull 69(4):375–381. https://doi.org/10.1016/j.brainresbull.2006.01.009

    Article  PubMed  Google Scholar 

  64. Moldovan M, Constantinescu AO, Balseanu A, Oprescu N, Zagrean L, Popa-Wagner A (2010) Sleep deprivation attenuates experimental stroke severity in rats. Exp Neurol 222(1):135–143. https://doi.org/10.1016/j.expneurol.2009.12.023

    Article  PubMed  Google Scholar 

  65. Fujihara H, Sei H, Morita Y, Ueta Y, Morita K (2003) Short-term sleep disturbance enhances brain-derived neurotrophic factor gene expression in rat hippocampus by acting as internal stressor. J Mol Neurosci 21(3):223–232. https://doi.org/10.1385/jmn:21:3:223

    Article  CAS  PubMed  Google Scholar 

  66. Hairston IS, Peyron C, Denning DP, Ruby NF, Flores J, Sapolsky RM, Heller HC, O’Hara BF (2004) Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J Neurophysiol 91(4):1586–1595. https://doi.org/10.1152/jn.00894.2003

    Article  CAS  PubMed  Google Scholar 

  67. Sahin L, Cevik OS, Cevik K, Guven C, Taskin E, Kocahan S (2021) Mild regular treadmill exercise ameliorated the detrimental effects of acute sleep deprivation on spatial memory. Brain Res 1759:147367. https://doi.org/10.1016/j.brainres.2021.147367

    Article  CAS  PubMed  Google Scholar 

  68. Gopalakrishnan A, Ji LL, Cirelli C (2004) Sleep deprivation and cellular responses to oxidative stress. Sleep 27(1):27–35. https://doi.org/10.1093/sleep/27.1.27

    Article  PubMed  Google Scholar 

  69. Melgarejo-Gutierrez M, Acosta-Pena E, Venebra-Munoz A, Escobar C, Santiago-Garcia J, Garcia-Garcia F (2013) Sleep deprivation reduces neuroglobin immunoreactivity in the rat brain. NeuroReport 24(3):120–125. https://doi.org/10.1097/WNR.0b013e32835d4b74

    Article  CAS  PubMed  Google Scholar 

  70. Ramanathan L, Hu S, Frautschy SA, Siegel JM (2010) Short-term total sleep deprivation in the rat increases antioxidant responses in multiple brain regions without impairing spontaneous alternation behavior. Behav Brain Res 207(2):305–309. https://doi.org/10.1016/j.bbr.2009.10.014

    Article  CAS  PubMed  Google Scholar 

  71. Hafedh M, Parnow A (2022) Exercise training improves memory and produces changes in the adrenal gland morphology in the experimental autoimmune encephalomyelitis. Endocr Regul 56(1):31–37. https://doi.org/10.2478/enr-2022-0004

    Article  PubMed  Google Scholar 

  72. Sun GC, Lee YJ, Lee YC, Yu HF, Wang DC (2021) Exercise prevents the impairment of learning and memory in prenatally phthalate-exposed male rats by improving the expression of plasticity-related proteins. Behav Brain Res 413:113444. https://doi.org/10.1016/j.bbr.2021.113444

    Article  PubMed  Google Scholar 

  73. Xu L, Zhu L, Zhu L, Chen D, Cai K, Liu Z, Chen A (2021) Moderate Exercise combined with enriched Environment enhances Learning and Memory through BDNF/TrkB signaling pathway in rats. Int J Environ Res Public Health 18(16). https://doi.org/10.3390/ijerph18168283

  74. Jeong JH, Koo JH, Yook JS, Cho JY, Kang EB (2021) Neuroprotective benefits of Exercise and MitoQ on memory function, mitochondrial Dynamics, oxidative stress, and Neuroinflammation in D-Galactose-Induced aging rats. Brain Sci 11(2). https://doi.org/10.3390/brainsci11020164

  75. Lan Y, Huang Z, Jiang Y, Zhou X, Zhang J, Zhang D, Wang B, Hou G (2018) Strength exercise weakens aerobic exercise-induced cognitive improvements in rats. PLoS ONE 13(10):e0205562. https://doi.org/10.1371/journal.pone.0205562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Vilela TC, Muller AP, Damiani AP, Macan TP, da Silva S, Canteiro PB, de Sena Casagrande A, Pedroso GDS, Nesi RT, de Andrade VM, de Pinho RA (2017) Strength and aerobic exercises improve spatial memory in aging rats through stimulating distinct neuroplasticity mechanisms. Mol Neurobiol 54(10):7928–7937. https://doi.org/10.1007/s12035-016-0272-x

    Article  CAS  PubMed  Google Scholar 

  77. Nokia MS, Lensu S, Ahtiainen JP, Johansson PP, Koch LG, Britton SL, Kainulainen H (2016) Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. J Physiol 594(7):1855–1873. https://doi.org/10.1113/JP271552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Duman RS, Aghajanian GK, Sanacora G, Krystal JH (2016) Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat Med 22(3):238–249. https://doi.org/10.1038/nm.4050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Gray JD, Milner TA, McEwen BS (2013) Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 239:214–227. https://doi.org/10.1016/j.neuroscience.2012.08.034

    Article  CAS  PubMed  Google Scholar 

  80. Rajizadeh MA, Sheibani V, Bejeshk MA, Mohtashami Borzadaran F, Saghari H, Esmaeilpour K (2019) The effects of high intensity exercise on learning and memory impairments followed by combination of sleep deprivation and demyelination induced by etidium bromide. Int J Neurosci 129(12):1166–1178. https://doi.org/10.1080/00207454.2019.1640695

    Article  CAS  PubMed  Google Scholar 

  81. Mohammadipoor-Ghasemabad L, Sangtarash MH, Esmaeili-Mahani S, Sheibani V, Sasan HA (2019) Abnormal hippocampal miR-1b expression is ameliorated by regular treadmill exercise in the sleep-deprived female rats. Iran J Basic Med Sci 22(5):485–490. https://doi.org/10.22038/ijbms.2019.31988.7734

    Article  PubMed  PubMed Central  Google Scholar 

  82. Rajizadeh MA, Esmaeilpour K, Masoumi-Ardakani Y, Bejeshk MA, Shabani M, Nakhaee N, Ranjbar MP, Borzadaran FM, Sheibani V (2018) Voluntary exercise impact on cognitive impairments in sleep-deprived intact female rats. Physiol Behav 188:58–66. https://doi.org/10.1016/j.physbeh.2017.12.030

    Article  CAS  PubMed  Google Scholar 

  83. 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 Processes 119:50–57. doi:https://doi.org/10.1016/j.beproc.2015.06.014

  84. Chen G-H, Wei R-M, Zhang Y-M, Li Y, Wu Q-T, Wang Y-T, Li X-Y, Li X-W (2022) Altered cognition and anxiety in adolescent offspring whose mothers underwent different-pattern maternal sleep deprivation, and cognition link to hippocampal expressions of Bdnf and Syt-1. Frontiers in Behavioral Neuroscience:483

  85. Zagaar M, Dao A, Alhaider I, Alkadhi K (2013) Regular treadmill exercise prevents sleep deprivation-induced disruption of synaptic plasticity and associated signaling cascade in the dentate gyrus. Mol Cell Neurosci 56:375–383. https://doi.org/10.1016/j.mcn.2013.07.011

    Article  CAS  PubMed  Google Scholar 

  86. Fernandes J, Baliego LGZ, Peixinho-Pena LF, de Almeida AA, Venancio DP, Scorza FA, de Mello MT, Arida RM (2013) Aerobic exercise attenuates inhibitory avoidance memory deficit induced by paradoxical sleep deprivation in rats. Brain Res 1529:66–73

    Article  CAS  PubMed  Google Scholar 

  87. Landers MR, Kinney JW, Allen DN, van Breukelen F (2013) A comparison of voluntary and forced exercise in protecting against behavioral asymmetry in a juvenile hemiparkinsonian rat model. Behav Brain Res 248:121–128

    Article  PubMed  Google Scholar 

  88. Van Dongen P, Baynard MD, Maislin G, Dinges DF (2004) Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 27(3):423–433

    PubMed  Google Scholar 

  89. Deurveilher S, Bush JE, Rusak B, Eskes GA, Semba K (2015) Psychomotor vigilance task performance during and following chronic sleep restriction in rats. Sleep 38(4):515–528

    Article  PubMed  PubMed Central  Google Scholar 

  90. Yang Y, Lagisz M, Foo YZ, Noble DW, Anwer H, Nakagawa S (2021) Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta-analysis of mean and variance. Biol Rev 96(4):1504–1527

    Article  PubMed  Google Scholar 

  91. Kronman CA, Kern KL, Nauer RK, Dunne MF, Storer TW, Schon K (2020) Cardiorespiratory fitness predicts effective connectivity between the hippocampus and default mode network nodes in young adults. Hippocampus 30(5):526–541

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

There is no providing financial support to this project.

Author information

Authors and Affiliations

Authors

Contributions

G. KH., V. A., and M. R. collected data. MR. Z. analyzed data, reviewing, and validations. S. V. designing the study, collecting data, writing the original draft, and review and editing. All authors approved the final version. The authors declare that all data were generated in-house and that no paper mill was used.

Corresponding author

Correspondence to Salar Vaseghi.

Ethics declarations

Ethics approval and consent to participate

N/A.

Consent for publication

N/A.

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kholghi, G., Alipour, V., Rezaie, M. et al. The Interaction Effect of Sleep Deprivation and Treadmill Exercise in Various Durations on Spatial Memory with Respect to the Oxidative Status of Rats. Neurochem Res 48, 2077–2092 (2023). https://doi.org/10.1007/s11064-023-03890-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-023-03890-3

Keywords

Navigation