382
Views
15
CrossRef citations to date
0
Altmetric
Original Articles

The effects of high intensity exercise on learning and memory impairments followed by combination of sleep deprivation and demyelination induced by etidium bromide

, ORCID Icon, , , &
Pages 1166-1178 | Received 02 Jan 2019, Accepted 11 Jun 2019, Published online: 15 Jul 2019

References

  • Rolak LA. Multiple sclerosis: it’s not the disease you thought it was. Clin Med Res. 2003;1:57–60.
  • McQualter JL, Bernard CC. Multiple sclerosis: a battle between destruction and repair. J Neurochem. 2007;100:295–306.
  • Jin J-J, Ko I-G, Kim S-E, et al. Swimming exercise ameliorates multiple sclerosis-induced impairment of short-term memory by suppressing apoptosis in the hippocampus of rats. J Exerc Rehabil. 2014;10:69.
  • Roosendaal S, Moraal B, Pouwels P, et al. Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler. 2009;15:708–714.
  • Sicotte N, Kern K, Giesser B, et al. Regional hippocampal atrophy in multiple sclerosis. Brain. 2008;131:1134–1141.
  • Elliott AS, Huber JD, O’Callaghan JP, et al. A review of sleep deprivation studies evaluating the brain transcriptome. SpringerPlus. 2014;3:728.
  • Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11:114
  • Goel N, Rao H, Durmer JS, et al. Neurocognitive consequences of sleep deprivation. Semin Neurol. 2009;29:320., editors. NIH Public Access.
  • Rahman A, Languille S, Lamberty Y, et al. Sleep deprivation impairs spatial retrieval but not spatial learning in the non-human primate grey mouse lemur. PLoS One. 2013;8:e64493
  • Colavito V, Fabene PF, Grassi Zucconi G, et al. Experimental sleep deprivation as a tool to test memory deficits in rodents. Front Syst Neurosci 2013;7:106.
  • Rajizadeh MA, Esmaeilpour K, Masoumi-Ardakani Y, et al. Voluntary exercise impact on cognitive impairments in sleep-deprived intact female rats. Physiol Behav 2018; May 1188:58–66.
  • McCoy JG, Strecker RE. The cognitive cost of sleep lost. Neurobiol Learn Mem. 2011;96:564–582.
  • Moreira N, Damasceno R, Medeiros C, et al. Restless leg syndrome, sleep quality and fatigue in multiple sclerosis patients. Braz J Med Biol Res. 2008;41:932–937.
  • Bamer AM, Johnson K, Amtmann D, et al. Prevalence of sleep problems in individuals with multiple sclerosis. Mult Scler. 2008;14:1127–1130.
  • Strober LB. Fatigue in multiple sclerosis: a look at the role of poor sleep. Front Neurol. 2015;6:21
  • Zielinski MR, Davis JM, Fadel JR, et al. Influence of chronic moderate sleep restriction and exercise training on anxiety, spatial memory, and associated neurobiological measures in mice. Behav Brain Res. 2013;250:74–80.
  • Tong L, Shen H, Perreau VM, et al. Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol Dis. 2001;8:1046–1056.
  • Laurin D, Verreault R, Lindsay J, et al. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol. 2001;58:498–504.
  • Rossi S, Furlan R, De Chiara V, et al. Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol Dis. 2009;36:51–59.
  • Salari M, Sheibani V, Saadati H, et al. The compensatory effect of regular exercise on long-term memory impairment in sleep deprived female rats. Behav Process. 2015;119:50–57.
  • Zagaar M, Dao A, Levine A, et al. Regular exercise prevents sleep deprivation associated impairment of long-term memory and synaptic plasticity in the CA1 area of the hippocampus. Sleep. 2013;36:751–761.
  • Saadati H, Esmaeili-Mahani S, Esmaeilpour K, et al. Exercise improves learning and memory impairments in sleep deprived female rats. Physiol Behav.. 2015;138:285–291.
  • Wens I, Dalgas U, Verboven K, et al. Impact of high intensity exercise on muscle morphology in EAE rats. Physiol Res. 2015;64:907
  • Ghaffari S, Hatami H, Dehghan G. Saffron ethanolic extract attenuates oxidative stress, spatial learning, and memory impairments induced by local injection of ethidium bromide. Res Pharm Sci. 2015;10:222.
  • Goudarzvand M, Javan M, Mirnajafi-Zadeh J, et al. Vitamins E and D3 attenuate demyelination and potentiate remyelination processes of hippocampal formation of rats following local injection of ethidium bromide. Cell Mol Neurobiol. 2010;30:289–299.
  • Hajali V, Sheibani V, Esmaeili-Mahani S, et al. Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance. Behav Brain Res. 2012;228:311–318.
  • Coll-Andreu M, Martí-Nicolovius M, Morgado-Bernal I. Facilitation of shuttle-box avoidance by the platform method: temporal effects. Physiol Behav. 1991;49:1211–1215.
  • Machado RB, Hipólide DC, Benedito-Silva AA, et al. Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 2004;1004:45–51.
  • Suchecki D, Tufik S. Social stability attenuates the stress in the modified multiple platform method for paradoxical sleep deprivation in the rat. Physiol Behav. 2000;68:309–316.
  • Hagewoud R, Havekes R, Novati A, et al. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J Sleep Res. 2009;19:280–288.
  • Campbell I, Guinan M, Horowitz J. Sleep deprivation impairs long-term potentiation in rat hippocampal slices. J Neurophysiol. 2002;88:1073–1076.
  • Kim EY, Mahmoud GS, Grover LM. REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus. Neurosci Lett. 2005;388:163–167.
  • Zagaar M, Alhaider I, Dao A, et al. The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence. Neurobiol Dis. 2012;45:1153–1162.
  • Saadati H, Sheibani V, Esmaeili-Mahani S, et al. Prior regular exercise reverses the decreased effects of sleep deprivation on brain-derived neurotrophic factor levels in the hippocampus of ovariectomized female rats. Regulatory Peptides. 2014;194:11–15.
  • Chen L, Tian S, Ke J. Rapid eye movement sleep deprivation disrupts consolidation but not reconsolidation of novel object recognition memory in rats. Neurosci Lett. 2014;563:12–16.
  • Van Hulzen Z, Coenen A. Effects of paradoxical sleep deprivation on two-way avoidance acquisition. Physiol Behav. 1982;29:581–587.
  • Vollert C, Zagaar M, Hovatta I, et al. Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav Brain Res. 2011;224:233–240.
  • Noseworthy J, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med. 2000;343:938–952.
  • Tomassini V, Pozzilli C. Sex hormones, brain damage and clinical course of multiple sclerosis. J Neurol Sci. 2009;286:35–39.
  • Sailer M, Fischl B, Salat D, et al. Focal thinning of the cerebral cortex in multiple sclerosis. Brain. 2003;126:1734–1744.
  • Gudi V. Regional differences of molecular factors during demyelination and early remyelination in the CNS. Hannover, Germany: University of Veterinary Medicine Hannover; 2010.
  • Goverman J, Brabb T. Rodent models of experimental allergic encephalomyelitis applied to the study of multiple sclerosis. Lab Anim Sci. 1996;46:482.
  • Mix E, Meyer-Rienecker H, Zettl UK. Animal models of multiple sclerosis for the development and validation of novel therapies–potential and limitations. J Neurol. 2008;255:7–14.
  • Yajima K, Suzuki K. Demyelination and remyelination in the rat central nervous system following ethidium bromide injection. Lab Invest. 1979;41:385–392.
  • Woodruff RH, Franklin RJ. Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti‐galactocerebroside: a comparative study. Glia. 1999;25:216–228.
  • Nassar CCS, Bondan EF, Alouche SR. Effects of aquatic exercises in a rat model of brainstem demyelination with ethidium bromide on the beam walking test. Arq Neuro-Psiquiatr. 2009;67:652–656.
  • Blakemore W, Franklin R. Remyelination in experimental models of toxin-induced demyelination. In: Advances in multiple sclerosis and experimental demyelinating diseases. Springer; 2008. p. 193–212.
  • Tarbali S, Khezri S. Vitamin D3 attenuates oxidative stress and cognitive deficits in a model of toxic demyelination. Ir J Basic Med Sci. 2016;19:80.
  • Khezri S, Dasht Bozorgi N, Rahmani F. The effect of caffeine on the myelin repair following experimental demyelination induction in the adult rat hippocampus. J Cell Mol Res. 2016;8:15–24.
  • Goudarzvand M, Choopani S, Shams A, et al. Focal injection of ethidium bromide as a simple model to study cognitive deficit and its improvement. Basic Clin Neurosci. 2016;7:63.
  • Cayre M, Courtès S, Martineau F, et al. Netrin 1 contributes to vascular remodeling in the subventricular zone and promotes progenitor emigration after demyelination. Development. 2013;140(15):3107–3117.
  • O’Sullivan C, Schubart A, Mir AK, et al. The dual S1PR1/S1PR5 drug BAF312 (Siponimod) attenuates demyelination in organotypic slice cultures. J Neuroinflamm. 2016;13:31.
  • Skripuletz T, Hackstette D, Bauer K, et al. Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain. 2013;136:147–167.
  • Brück W, Pförtner R, Pham T, et al. Reduced astrocytic NF-κB activation by laquinimod protects from cuprizone-induced demyelination. Acta Neuropathol. 2012;124:411–424.
  • Pourabdolhossein F, Mozafari S, Morvan-Dubois G, et al. Nogo receptor inhibition enhances functional recovery following lysolecithin-induced demyelination in mouse optic chiasm. PloS One. 2014;9:e106378.
  • de Paula Faria D, de Vries EF, Sijbesma JW, et al. PET imaging of glucose metabolism, neuroinflammation and demyelination in the lysolecithin rat model for multiple sclerosis. Mult Scler. 2014;20:1443–1452.
  • Martins-Júnior J, Bernardi M, Bondan E. Propentofylline treatment on open field behavior in rats with focal ethidium bromide-induced demyelination in the ventral surface of the brainstem. Life Sci. 2016;148:132–138.
  • Li Z, He Y, Fan S, et al. Clemastine rescues behavioral changes and enhances remyelination in the cuprizone mouse model of demyelination. Neurosci Bull. 2015;31:617–625.
  • Wang H, Li C, Wang H, et al. Cuprizone-induced demyelination in mice: age-related vulnerability and exploratory behavior deficit. Neurosci Bull. 2013;29:251–259.
  • Kim S-E, Ko I-G, Kim B-K, et al. Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol. 2010;45:357–365.
  • Van Praag H, Christie BR, Sejnowski TJ, et al. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci. 1999;96:13427–13431.
  • Choi J-H, Kim T-S, Park J-K, et al. Short-term treadmill exercise preserves sensory-motor function through inhibiting apoptosis in the hippocampus of hypoxic ischemia injury rat pups. J Exerc Rehabil. 2013;9:457.
  • Kim B-K, Shin M-S, Kim C-J, et al. Treadmill exercise improves short-term memory by enhancing neurogenesis in amyloid beta-induced Alzheimer disease rats. J Exerc Rehabil. 2014;10:2.
  • Sim Y-J, Kim H, Kim J-Y, et al. Long-term treadmill exercise overcomes ischemia-induced apoptotic neuronal cell death in gerbils. Physiol Behav. 2005;84:733–738.
  • Bernardes D, Brambilla R, Bracchi‐Ricard V, et al. Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis. J Neurochem. 2016;136:63–73.
  • Kim T-W, Sung Y-H. Regular exercise promotes memory function and enhances hippocampal neuroplasticity in experimental autoimmune encephalomyelitis mice. Neuroscience. 2017;346:173–181.
  • Soya H, Nakamura T, Deocaris CC, et al. BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun. 2007;358:961–967.
  • Griffin ÉW, Bechara RG, Birch AM, et al. Exercise enhances hippocampal‐dependent learning in the rat: evidence for a BDNF‐related mechanism. Hippocampus. 2009;19:973–980.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.