375
Views
23
CrossRef citations to date
0
Altmetric
Original Research

Benefit effect of REM-sleep deprivation on memory impairment induced by intensive exercise in male wistar rats: with respect to hippocampal BDNF and TrkB

, , , , , & show all
Pages 179-188 | Published online: 24 Sep 2019

References

  • Vina J, Sanchis‐Gomar F, Martinez‐Bello V, Gomez‐Cabrera M. Exercise acts as a drug; the pharmacological benefits of exercise. Br J Pharmacol. 2012;167(1):1–12. doi:10.1111/j.1476-5381.2012.01970.x22486393
  • Pontifex MB, Hillman CH, Fernhall B, Thompson KM, Valentini TA. The effect of acute aerobic and resistance exercise on working memory. Med Sci Sports Exercise. 2009;41(4):927–934. doi:10.1249/MSS.0b013e3181907d69
  • Berchtold N, Chinn G, Chou M, Kesslak J, Cotman C. Exercise primes a molecular memory for brain-derived neurotrophic factor protein induction in the rat hippocampus. Neuroscience. 2005;133(3):853–861. doi:10.1016/j.neuroscience.2005.03.02615896913
  • Bherer L, Erickson KI, Liu-Ambrose T. A review of the effects of physical activity and exercise on cognitive and brain functions in older adults. J Aging Res. 2013;2013:5–6.
  • Aguiar A Jr, Pinho R. The brain redox paradox of physical exercise In: Kozyrev D, Slutsky V, editors. Handbook of Free Radicals: Formation, Types and Effects. New York: Nova Science Publishers Company; 2010:153–166.
  • Aguiar AS, Tuon T, Pinho CA, et al. Intense exercise induces mitochondrial dysfunction in mice brain. Neurochem Res. 2008;33(1):51–58. doi:10.1007/s11064-007-9406-x17619145
  • Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82(1):47–95.11773609
  • Radak Z, Taylor AW, Ohno H, Goto S. Adaptation to exercise-induced oxidative stress: from muscle to brain. Exerc Immunol Rev. 2001;7:90–107.11579750
  • Diederich K, Bastl A, Wersching H, et al. Effects of different exercise strategies and intensities on memory performance and neurogenesis. Front Behav Neurosci. 2017;11:47. doi:10.3389/fnbeh.2017.0024628360847
  • Hu S, Ying Z, Gomez-Pinilla F, Frautschy SA. Exercise can increase small heat shock proteins (sHSP) and pre-and post-synaptic proteins in the hippocampus. Brain Res. 2009;1249:191–201. doi:10.1016/j.brainres.2008.10.05419014914
  • 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(5):357–365. doi:10.1016/j.exger.2010.02.00520156544
  • Ahlskog JE, Geda YE, Graff-Radford NR, Petersen RC Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Paper presented at: Mayo Clinic Proceedings; 2011.
  • Sofi F, Valecchi D, Bacci D, et al. Physical activity and risk of cognitive decline: a meta‐analysis of prospective studies. J Intern Med. 2011;269(1):107–117. doi:10.1111/j.1365-2796.2010.02281.x20831630
  • Verburgh L, Königs M, Scherder EJ, Oosterlaan J. Physical exercise and executive functions in preadolescent children, adolescents and young adults: a meta-analysis. Br J Sports Med. 2014;48(12):973–979. doi:10.1136/bjsports-2012-09144123467962
  • Carek PJ, Laibstain SE, Carek SM. Exercise for the treatment of depression and anxiety. Int J Psychiatry Med. 2011;41(1):15–28. doi:10.2190/PM.41.1.c21495519
  • Cooney GM, Dwan K, Greig CA, et al. Exercise for depression. Cochrane Database Sys Rev. 2013;9:9.
  • Erickson KI, Gildengers AG, Butters MA. Physical activity and brain plasticity in late adulthood. Dialogues Clin Neurosci. 2013;15(1):99.23576893
  • Erickson KI, Miller DL, Weinstein AM, Akl SL, Banducci S. Physical activity and brain plasticity in late adulthood: a conceptual and comprehensive review. Ageing Res. 2012;3(1):e6–e6. doi:10.4081/ar.2012.e6
  • Lou S-J, Liu J-Y, Chang H, Chen P-J. Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats. Brain Res. 2008;1210:48–55. doi:10.1016/j.brainres.2008.02.08018423578
  • Siamilis S, Jakus J, Nyakas C, et al. The effect of exercise and oxidant–antioxidant intervention on the levels of neurotrophins and free radicals in spinal cord of rats. Spinal Cord. 2009;47(6):453. doi:10.1038/sc.2008.10418936770
  • Grebot C, Groslambert A, Pernin J-N, Burtheret A, Rouillon J-D. Effects of exercise on perceptual estimation and short-term recall of shooting performance in a biathlon. Percept Mot Skills. 2003;97(3_suppl):1107–1114. doi:10.2466/pms.2003.97.3f.110715002854
  • Rhodes JS, Van Praag H, Jeffrey S, et al. Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci. 2003;117(5):1006. doi:10.1037/0735-7044.117.5.100614570550
  • Rosa EF, Takahashi S, Aboulafia J, Nouailhetas VL, Oliveira MG. Oxidative stress induced by intense and exhaustive exercise impairs murine cognitive function. J Neurophysiol. 2007;98(3):1820–1826. doi:10.1152/jn.01158.200617625057
  • Taverniers J, Van Ruysseveldt J, Smeets T, von Grumbkow J. High-intensity stress elicits robust cortisol increases, and impairs working memory and visuo-spatial declarative memory in special forces candidates: a field experiment. Stress. 2010;13(4):324–334. doi:10.3109/10253891003642394
  • Brem A-K, Ran K, Pascual-Leone A. Learning and memory In: Lozano AM, Hallett M, editors. Handbook of Clinical Neurology. Vol. 116 Elsevier; 2013: 693–737. doi: 10.1016/B978-0-444-53497-2.00055-324112934
  • Churchwell JC, Morris AM, Musso ND, Kesner RP. Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol Learn Mem. 2010;93(3):415–421. doi:10.1016/j.nlm.2009.12.00820074655
  • Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 2001;24(1):677–736. doi:10.1146/annurev.neuro.24.1.67711520916
  • Yamada K, Nabeshima T. Brain-derived neurotrophic factor/TrkB signaling in memory processes. J Pharmacol Sci. 2003;91(4):267–270.12719654
  • Cunha C, Brambilla R, Thomas KL. A simple role for BDNF in learning and memory? Front Mol Neurosci. 2010;3:1.20162032
  • Coles K, Tomporowski PD. Effects of acute exercise on executive processing, short-term and long-term memory. J Sports Sci. 2008;26(3):333–344. doi:10.1080/0264041070159141718074301
  • Parkhurst CN, Yang G, Ninan I, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155(7):1596–1609. doi:10.1016/j.cell.2013.11.03024360280
  • Vivar C, Potter MC, van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis In: Belzung C, Wigmore P, editors. Neurogenesis and Neural Plasticity. Springer; 2012:189–210.
  • Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10(1):49–62. doi:10.1016/j.smrv.2005.05.00216376591
  • Sei H, Saitoh D, Yamamoto K, Morita K, Morita Y. Differential effect of short-term REM sleep deprivation on NGF and BDNF protein levels in the rat brain. Brain Res. 2000;877(2):387–390. doi:10.1016/s0006-8993(00)02708-610986357
  • Plihal W, Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci. 1997;9(4):534–547. doi:10.1162/jocn.1997.9.4.53423968216
  • Mizuno M, Yamada K, Takei N, et al. Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol Psychiatry. 2003;8(2):217. doi:10.1038/sj.mp.400122412610654
  • Gais S, Lucas B, Born J. Sleep after learning aids memory recall. Learn Memory. 2006;13(3):259–262. doi:10.1101/lm.132106
  • Plihal W, Born J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology. 1999;36(5):571–582.10442025
  • Lim J, Dinges DF. Sleep deprivation and vigilant attention. Ann N Y Acad Sci. 2008;1129(1):305–322. doi:10.1196/annals.1417.00218591490
  • Chee MW, Chuah LY. Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol. 2008;21(4):417–423. doi:10.1097/WCO.0b013e3283052cf718607201
  • Stickgold R, Walker MP. Sleep-dependent memory consolidation and reconsolidation. Sleep Med. 2007;8(4):331–343. doi:10.1016/j.sleep.2007.03.01117470412
  • Maquet P. The role of sleep in learning and memory. science. 2001;294(5544):1048–1052. doi:10.1126/science.106285611691982
  • Nilsson JP, Söderström M, Karlsson AU, et al. Less effective executive functioning after one night’s sleep deprivation. J Sleep Res. 2005;14(1):1–6. doi:10.1111/j.1365-2869.2005.00442.x15743327
  • Harrison Y, Horne JA. The impact of sleep deprivation on decision making: a review. J Exp Psychol Appl. 2000;6(3):236.11014055
  • Lautenbacher S, Kundermann B, Krieg J-C. Sleep deprivation and pain perception. Sleep Med Rev. 2006;10(5):357–369. doi:10.1016/j.smrv.2005.08.00116386930
  • Gillin JC, Buchsbaum M, Wu J, Clark C, Bunney W Jr. Sleep deprivation as a model experimental antidepressant treatment: findings from functional brain imaging. Depress Anxiety. 2001;14(1):37–49.11568981
  • Jiang Y, Zhu J. Effects of sleep deprivation on behaviors and abnormal hippocampal BDNF/miR-10B expression in rats with chronic stress depression. Int J Clin Exp Pathol. 2015;8(1):586.25755749
  • Hines D, Schmitt L, Hines R, Moss S, Haydon P. Antidepressant effects of sleep deprivation require astrocyte-dependent adenosine mediated signaling. Transl Psychiatry. 2013;3(1):e212. doi:10.1038/tp.2012.13623321809
  • Alkadhi K, Zagaar M, Alhaider I, Salim S, Aleisa A. Neurobiological consequences of sleep deprivation. Curr Neuropharmacol. 2013;11(3):231–249. doi:10.2174/1570159X1131103000124179461
  • Aghajani M, Faghihi M, Imani A, et al. Post-infarct sleep disruption and its relation to cardiac remodeling in a rat model of myocardial infarction. Chronobiol Int. 2017;34(5):587–600. doi:10.1080/07420528.2017.128182328156163
  • D’Hooge R, De Deyn PP. Applications of the morris water maze in the study of learning and memory. Brain Res Brain Res Rev. 2001;36(1):60–90.11516773
  • Alijanpour S, Tirgar F, Zarrindast MR. Role of dorsal hippocampal orexin-1 receptors in memory restoration induced by morphine sensitization phenomenon. Neuroscience. 2016;312:215–226. doi:10.1016/j.neuroscience.2015.11.02326592714
  • Ashabi G, Sadat-Shirazi M-S, Khalifeh S, Elhampour L, Zarrindast M-R. NMDA receptor adjusted co-administration of ecstasy and cannabinoid receptor-1 agonist in the amygdala via stimulation of BDNF/Trk-B/CREB pathway in adult male rats. Brain Res Bull. 2017;130:221–230. doi:10.1016/j.brainresbull.2017.01.02028167133
  • Ide K, Secher NH. Cerebral blood flow and metabolism during exercise. Prog Neurobiol. 2000;61(4):397–414.10727781
  • Aguiar A Jr, Boemer G, Rial D, et al. High-intensity physical exercise disrupts implicit memory in mice: involvement of the striatal glutathione antioxidant system and intracellular signaling. Neuroscience. 2010;171(4):1216–1227. doi:10.1016/j.neuroscience.2010.09.05320888397
  • Blustein JE, McLaughlin M, Hoffman JR. Exercise effects stress-induced analgesia and spatial learning in rats. Physiol Behav. 2006;89(4):582–586. doi:10.1016/j.physbeh.2006.07.01716945396
  • García-Capdevila S, Portell-Cortés I, Torras-Garcia M, Coll-Andreu M, Costa-Miserachs D. Effects of long-term voluntary exercise on learning and memory processes: dependency of the task and level of exercise. Behav Brain Res. 2009;202(2):162–170. doi:10.1016/j.bbr.2009.03.02019463697
  • Kennard JA, Woodruff-Pak DS. A comparison of low-and high-impact forced exercise: effects of training paradigm on learning and memory. Physiol Behav. 2012;106(4):423–427. doi:10.1016/j.physbeh.2012.02.02322402029
  • Chang Y-K, Chi L, Etnier JL, Wang -C-C, Chu C-H, Zhou C. Effect of acute aerobic exercise on cognitive performance: role of cardiovascular fitness. Psychol Sport Exerc. 2014;15(5):464–470. doi:10.1016/j.psychsport.2014.04.007
  • Kashihara K, Maruyama T, Murota M, Nakahara Y. Positive effects of acute and moderate physical exercise on cognitive function. J Physiol Anthropol. 2009;28(4):155–164.19652447
  • Chmura J, Nazar K, Kaciuba-Uścilko H. Choice reaction time during graded exercise in relation to blood lactate and plasma catecholamine thresholds. Int J Sports Med. 1994;15(04):172–176. doi:10.1055/s-2007-10210428063464
  • Kemppainen J, Aalto S, Fujimoto T, et al. High intensity exercise decreases global brain glucose uptake in humans. J Physiol. 2005;568(1):323–332. doi:10.1113/jphysiol.2005.09135516037089
  • Secher NH, Quistorff B. Brain glucose and lactate uptake during exhaustive exercise. J Physiol. 2005;568(1):3. doi:10.1113/jphysiol.2005.09578616096335
  • Vaynman S, Ying Z, Wu A, Gomez-Pinilla F. Coupling energy metabolism with a mechanism to support brain-derived neurotrophic factor-mediated synaptic plasticity. Neuroscience. 2006;139(4):1221–1234. doi:10.1016/j.neuroscience.2006.01.06216580138
  • Hoffman-Goetz L, Spagnuolo P, Guan J. Repeated exercise in mice alters expression of IL-10 and TNF-α in intestinal lymphocytes. Brain Behav Immun. 2008;22(2):195–199. doi:10.1016/j.bbi.2007.07.00217720362
  • Aguiló A, Tauler P, Fuentespina E, Tur JA, Córdova A, Pons A. Antioxidant response to oxidative stress induced by exhaustive exercise. Physiol Behav. 2005;84(1):1–7. doi:10.1016/j.physbeh.2004.07.03415642600
  • Coleman MA, Garland T Jr, Marler CA, Newton SS, Swallow JG, Carter PA. Glucocorticoid response to forced exercise in laboratory house mice (Mus domesticus). Physiol Behav. 1998;63(2):279–285. doi:10.1016/S0031-9384(97)00441-19423970
  • Kohut M, Davis J, Jackson D, et al. Exercise effects on IFN-β expression and viral replication in lung macrophages after HSV-1 infection. Am J Physiol Lung Cell Mol Physiol. 1998;275(6):L1089–L1094.
  • Hansson A, Sommer W, Metsis M, Strömberg I, Agnati L, Fuxe K. Corticosterone actions on the hippocampal brain‐derived neurotrophic factor expression are mediated by exon IV promoter. J Neuroendocrinol. 2006;18(2):104–114.16420279
  • Luine V, Villegas M, Martinez C, McEwen BS. Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 1994;639(1):167–170.8180832
  • McEwen BS, Weiss JM, Schwartz LS. Selective retention of corticosterone by limbic structures in rat brain. Nature. 1968;220(5170):911. doi:10.1038/220911a04301849
  • Gray J, Milner T, McEwen B. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience. 2013;239:214–227. doi:10.1016/j.neuroscience.2012.08.03422922121
  • Duman RS, Aghajanian GK, Sanacora G, Krystal JH. Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat Med. 2016;22(3):238. doi:10.1038/nm.405026937618
  • Schiavone S, Jaquet V, Trabace L, Krause K-H. Severe life stress and oxidative stress in the brain: from animal models to human pathology. Antioxid Redox Signal. 2013;18(12):1475–1490.22746161
  • Jesse C, Donato F, Giacomeli R, et al. Chronic unpredictable mild stress decreases BDNF and NGF levels and Na+, K+-ATPase activity in the hippocampus and prefrontal cortex of mice: antidepressant effect of chrysin. Neuroscience. 2015;289:367–380. doi:10.1016/j.neuroscience.2014.12.04825592430
  • Ibi M, Liu J, Arakawa N, et al. Depressive-like behaviors are regulated by NOX1/NADPH oxidase by redox modification of NMDA receptor 1. J Neurosci. 2017;37(15):4200–4212. doi:10.1523/JNEUROSCI.2988-16.201728314819
  • Murínová J, Hlaváčová N, Chmelová M, Riečanský I. The evidence for altered BDNF expression in the brain of rats reared or housed in social isolation: a systematic review. Front Behav Neurosci. 2017;11:101. doi:10.3389/fnbeh.2017.0024628620285
  • Ota KT, Liu R-J, Voleti B, et al. REDD1 is essential for stress-induced synaptic loss and depressive behavior. Nat Med. 2014;20(5):531.24728411
  • Zhou W, Wang N, Yang C, Li X-M, Zhou Z-Q, Yang J-J. Ketamine-induced antidepressant effects are associated with AMPA receptors-mediated upregulation of mTOR and BDNF in rat hippocampus and prefrontal cortex. Eur Psychiatry. 2014;29(7):419–423. doi:10.1016/j.eurpsy.2013.10.00524321772
  • Patki G, Solanki N, Atrooz F, Allam F, Salim S. Depression, anxiety-like behavior and memory impairment are associated with increased oxidative stress and inflammation in a rat model of social stress. Brain Res. 2013;1539:73–86. doi:10.1016/j.brainres.2013.09.03324096214
  • Graves LA, Heller EA, Pack AI, Abel T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Memory. 2003;10(3):168–176. doi:10.1101/lm.48803
  • Fishbein W. Disruptive effects of rapid eye movement sleep deprivation on long-term memory. Physiol Behav. 1971;6(4):279–282. doi:10.1016/0031-9384(71)90155-74337286
  • Silva R, Abilio V, Takatsu A, et al. Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacology. 2004;46(6):895–903. doi:10.1016/j.neuropharm.2003.11.03215033349
  • Wirz-Justice A, Van Den Hoofdakker RH. Sleep deprivation in depression: what do we know, where do we go? Biol Psychiatry. 1999;46(4):445–453.10459393
  • Walker MP, van Der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychol Bull. 2009;135(5):731. doi:10.1037/a001657019702380
  • Giedke H, Schwärzler F. Therapeutic use of sleep deprivation in depression. Sleep Med Rev. 2002;6(5):361–377. doi:10.1053/smrv.2002.023512531127
  • Ibrahim L, Duncan W, Luckenbaugh DA, Yuan P, Machado-Vieira R, Zarate CA Jr. Rapid antidepressant changes with sleep deprivation in major depressive disorder are associated with changes in vascular endothelial growth factor (VEGF): a pilot study. Brain Res Bull. 2011;86(1–2):129–133. doi:10.1016/j.brainresbull.2011.06.00321704134
  • Wu JC, Bunney WE. The biological basis of an antidepressant response to sleep deprivation and relapse: review and hypothesis. Am J Psychiatry. 1990;147(1):14. doi:10.1176/ajp.147.1.142403471
  • Zucconi GG, Cipriani S, Balgkouranidou I, Scattoni R. ‘One night’sleep deprivation stimulates hippocampal neurogenesis. Brain Res Bull. 2006;69(4):375–381. doi:10.1016/j.brainresbull.2006.01.00916624668
  • Landsness EC, Goldstein MR, Peterson MJ, Tononi G, Benca RM. Antidepressant effects of selective slow wave sleep deprivation in major depression: a high-density EEG investigation. J Psychiatr Res. 2011;45(8):1019–1026. doi:10.1016/j.jpsychires.2011.02.00321397252
  • Taishi P, Sanchez C, Wang Y, Fang J, Harding J, Krueger J. Conditions that affect sleep alter the expression of molecules associated with synaptic plasticity. Am J Physiol Regul Integr Comp Physiol. 2001;281(3):R839–R845. doi:10.1152/ajpregu.2001.281.3.R83911506999
  • Fujihara H, Sei H, Morita Y, Ueta Y, Morita K. Short-term sleep disturbance enhances brain-derived neurotrophic factor gene expression in rat hippocampus by acting as internal stressor. J Mol Neurosci. 2003;21(3):223–231.14645989
  • Guzman‐Marin R, Ying Z, Suntsova N, et al. Suppression of hippocampal plasticity‐related gene expression by sleep deprivation in rats. J Physiol. 2006;575(3):807–819. doi:10.1113/jphysiol.2006.11528716825295
  • Peyron C, Wurts S, Srere H, Heller H, Edgar D, Kilduff T mRNA level of brain-derived neurotrophic factor increases in several brain regions after sleep deprivation. Paper presented at: Society for Neuroscience Abstracts; 1998.
  • Mendelson WB, Guthrie RD, Frederick G, Wyatt RJ. The flower pot technique of rapid eye movement (REM) sleep deprivation. Pharmacol Biochem Behav. 1974;2(4):553–556. doi:10.1016/0091-3057(74)90018-54371007
  • Clark CP, Brown GG, Archibald SL, et al. Does amygdalar perfusion correlate with antidepressant response to partial sleep deprivation in major depression? Psychiatry Res. 2006;146(1):43–51. doi:10.1016/j.pscychresns.2005.09.00716380239
  • Kavčič P, Rojc B, Dolenc-Grošelj L, Claustrat B, Fujs K. The impact of sleep deprivation and nighttime light exposure on clock gene expression in humans. Croat Med J. 2011;52(5):594–603. doi:10.3325/cmj.2011.52.59421990077
  • Dallaspezia S, Benedetti F. Sleep deprivation therapy for depression In: Meerlo P, Benca RM, Abel T, editors. Sleep, Neuronal Plasticity and Brain Function. Springer; 2014:483–502.