Effect of Acute and Chronic Sleep Deficit on Working and Long-Term Memory in Rats
- Autores: Chernyshev M.1, Guseev M.1, Ekimova I.1
-
Afiliações:
- Sechenov Institute of Evolutionary Physiology and Bichemistry, RAS
- Edição: Volume 109, Nº 11 (2023)
- Páginas: 1635-1649
- Seção: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
- URL: https://journals.rcsi.science/0869-8139/article/view/232279
- DOI: https://doi.org/10.31857/S0869813923110031
- EDN: https://elibrary.ru/HGZTDH
- ID: 232279
Citar
Resumo
It is known that insufficient sleep or diurnal rhythm disturbances of sleep and wakefulness exert a detrimental effect on cognitive functions. It was thought for a long period that memory consolidation is the most vulnerable link, i.e., information transfer from short-term/working memory to long-term memory. However, there is a progressive number of studies indicating that the most negative consequences of sleep loss are observed in working memory. In our study, we undertook an effort to assess possible disturbances in working memory and long-term memory following sleep loss impact with different protocols in acute and chronic experiment in rats. Sleep in Wistar rats was deprived/restricted by swinging platform technique according to the following protocols: 1 – total sleep deprivation for 18 h; 2 – partial sleep restriction for 24 h (3 h of sleep deprivation alternated with 1 h of sleep opportunity – totally 18 h of sleep deprivation); 3 – chronic partial sleep restriction (conditions 2 for five consistent days). Total sleep deprivation in Y-maze test was shown to result in a significant decrease in spontaneous alternations of maze arms that indicates working memory impairment. This impact in Barnes test did not exert an effect on long-term memory – time spent for seeking a shelter did not change in this task. Acute and chronic sleep restriction induced no changes in working memory and long-term memory. The results obtained allow us to come to conclusion that working memory (in contrast to long-term memory) is a vulnerable component of cognitive function under total sleep deprivation conditions. This negative effect was abolished if periods of sleep deprivation alternated with short periods of sleep opportunities that indicate protective significance of short sleep periods for cognitive functions during sleep deficit. Hence, short-term sleep is helpful for cognitive health and protects working memory, whereas continuous long-term wakefulness impairs it.
Palavras-chave
Sobre autores
M. Chernyshev
Sechenov Institute of Evolutionary Physiology and Bichemistry, RAS
Autor responsável pela correspondência
Email: netmisha@mail.ru
Russia, St. Petersburg
M. Guseev
Sechenov Institute of Evolutionary Physiology and Bichemistry, RAS
Email: netmisha@mail.ru
Russia, St. Petersburg
I. Ekimova
Sechenov Institute of Evolutionary Physiology and Bichemistry, RAS
Email: netmisha@mail.ru
Russia, St. Petersburg
Bibliografia
- Полуэктов М (2019) Загадки сна: от бессонницы до летаргии М. Альпина Пабл. [Poluektov M (2019) Mysteries of sleep: from insomnia to lethargy. M. Al’pina Pabl. (In Russ)].
- Alhola P, Polo-Kantola P (2007) Sleep deprivation: Impact on cognitive performance. Neuropsychiatr Dis Treat 3(5): 553–567.
- Lo JC, Groeger JA, Santhi N, Arbon EL, Lazar AS, Hasan S, von Schantz M, Archer SN, Dijk DJ (2012) Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS One 7(9): e45987. https://doi.org/10.1371/journal.pone.0045987
- Balkin TJ, Rupp T, Picchioni D, Wesensten NJ (2008) Sleep loss and sleepiness: current issues. Chest 134(3): 653–660. https://doi.org/10.1378/chest.08-1064
- McCoy JG, Strecker RE (2011) The cognitive cost of sleep lost. Neurobiol Learn Mem 96(4): 564–582. https://doi.org/10.1016/j.nlm.2011.07.004
- Born J, Wagner U (2004) Awareness in memory: being explicit about the role of sleep. Trends Cogn Sci 8: 242–244.
- Gais S, Plihal W, Wagner U, Born J (2000) Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3: 1335–1339.
- Jenkins JG, Dallenbach KM (1924) Obliviscence during Sleep and Waking. Am J Psychol 35(4): 605. https://doi.org/10.2307/1414040
- Rasch B, Born J (2013) About Sleep’s Role in Memory. Physiol Rev 93(2): 681–766. https://doi.org/10.1152/physrev.00032.2012
- Hennecke E, Lange D, Steenbergen F, Fronczek-Poncelet J, Elmenhorst, D, Bauer A, Elmenhorst EM (2020) 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
- Gais S, Lucas B, Born J (2006) Sleep after learning aids memory recall. Learn Mem 13(3): 259–262.
- Payne JD, Tucker MA, Ellenbogen JM, Wamsley EJ, Walker MP, Schacter DL, Stickgold R (2012) Memory for semantically related and unrelated declarative information: the benefit of sleep, the cost of wake. PLoS One 7(3): e33079. https://doi.org/10.1371/journal.pone.0033079
- Palchykova S, Winskysommerer R, Meerlo P, Durr R, Tobler I (2006) Sleep deprivation impairs object recognition in mice. Neurobiol Learn Mem 85(3): 263–271. https://doi.org/10.1016/j.nlm.2005.11.005
- Guan Z, Peng X, Fang J (2004) Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res 1018(1): 38–47. https://doi.org/10.1016/j.brainres.2004.05.032
- McCoy JG, Christie MA, Kim Y, Brennan R, Poeta DL, McCarley RW, Strecker RE (2013) Chronic sleep restriction impairs spatial memory in rats. NeuroReport 24(2): 91–95. https://doi.org/10.1097/wnr.0b013e32835cd97a
- Siegel JM (2021) Memory Consolidation Is Similar in Waking and Sleep. Current Sleep Med Rep 7(1): 15–18. https://doi.org/10.1007/s40675-020-00199-3
- McDevitt EA, Zhang J, MacKenzie KJ, Fiser J, Mednick SC (2022) The effect of interference, offline sleep, and wake on spatial statistical learning. Neurobiol Learn Mem 193: 107650. https://doi.org/10.1016/j.nlm.2022.107650
- Bailes C, Caldwell M, Wamsley EJ, Tucker MA (2020) Does sleep protect memories against interference? A failure to replicate. PLoS One 15(2): e0220419. https://doi.org/10.1371/journal.pone.0220419
- Kovalzon VM (2023) Cerebral information processing during sleep: evolutionary and ecological approaches. J Evol Biochem Phys 59(2): 79–89.
- Lim J, Dinges DF (2010) A meta-analysis of the impact of short-term sleep deprivation on cognitive variables. Psychol Bull 136(3): 375–389. https://doi.org/10.1037/a0018883
- Lowe CJ, Safati A, Hall PA (2017) The neurocognitive consequences of sleep restriction: A meta-analytic review. Neurosci Biobehav Rev 80: 586–604. https://doi.org/10.1016/j.neubiorev.2017.07.010
- Peng Z, Dai C, Ba Y, Zhang L, Shao Y, Tian J (2020) Effect of Sleep Deprivation on the Working Memory-Related N2-P3 Components of the Event-Related Potential Waveform. Front Neurosci 14: 469. https://doi.org/10.3389/fnins.2020.00469
- Krause AJ, Simon EB, Mander BA, Greer SM, Saletin JM, Goldstein-Piekarski AN, Walker MP (2017) The sleep-deprived human brain. Nat Rev Neurosci 18(7): 404–418. https://doi.org/10.1038/nrn.2017.55
- 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
- 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
- Colavito V, Fabene PF, Grassi-Zucconi G, Pifferi F, Lamberty Y, Bentivoglio M, Bertini G (2013) Experimental sleep deprivation as a tool to test memory deficits in rodents. Front Syst Neurosci 7: 106. https://doi.org/10.3389/fnsys.2013.00106
- 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
- Beaulieu I, Godbout R (2000) Spatial learning on the Morris Water Maze Test after a short-term paradoxical sleep deprivation in the rat. Brain and Cognit 43(1-3): 27–31.
- Le Marec N, Beaulieu I, Godbout R (2001) Four hours of paradoxical sleep deprivation impairs alternation performance in a water maze in the rat. Brain and Cognit 46(1–2): 195–197. https://doi.org/10.1016/s0278-2626(01)80064-6
- Ward CP, McCarley RW, Strecker RE (2009) Experimental sleep fragmentation impairs spatial reference but not working memory in Fischer/Brown Norway rats. J Sleep Res 18(2): 238–244. https://doi.org/10.1111/j.1365-2869.2008.00714.x
- Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB (1997) Sleep deprivation by the ‘‘flower pot’’ technique and spatial reference memory. Physiol & Behav 61(2): 249–256. https://doi.org/10.1016/s0031-9384(96)00363-0
- Porcu S, Casagrande M, Ferrara M, Bellatreccia A (1998) Sleep and Alertness During Alternating Monophasic and Poliphasic Rest-Activity Cycles. Int J Neurosci 95(1-2): 43–50. https://doi.org/10.3109/00207459809000648
- Roach GD, Zhou X, Darwent D, Kosmadopoulos A, Dawson D, Sargent C (2017) Are two halves better than one whole? A comparison of the amount and quality of sleep obtained by healthy adult males living on split and consolidated sleep–wake schedules. Accident Analysis & Prevent 99: 428–433. https://doi.org/10.1016/j.aap.2015.10.012
- 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. https://doi.org/10.5665/sleep.4562
- Deurveilher S, Semba K (2019) Physiological and Neurobehavioral Consequences of Chronic Sleep Restriction in Rodent Models. In: Handbook Behav Neurosci 30: 557–567. https://doi.org/10.1016/B978-0-12-813743-7.00037-2
- Bjorness TE, Kelly CL, Gao T, Poffenberger V, Greene RW (2009). Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci 29(5): 1267–1276. https://doi.org/10.1523/JNEUROSCI.2942-08.2009
- Гузеев МА, Курмазов НС, Симонова ВВ, Пастухов ЮФ, Екимова ИВ (2021) Создание модели хронического недосыпания для трансляционных исследований. Журн неврол психиатр им CC Корсакова 121(4-2): 6–13. [Guzeev MA, Kurmazov NS, Simonova VV, Pastukhov YF, Ekimova IV (2021) Modeling of chronic sleep restriction for translational studies. Zh Nevrol Psikhiatr im SS Korsakova 121(4-2): 6–13. (In Russ)]. https://doi.org/10.17116/jnevro20211214026
- Sinton CM, Kovakkattu D, Friese RS (2009) Validation of a novel method to interrupt sleep in the mouse. J Neurosci Methods 184(1): 71–78. https://doi.org/10.1016/j.jneumeth.2009.07.026
- Bertrand SJ, Zhang Z, Patel R, O’Ferrell C, Punjabi NM, Kudchadkar SR, Kannan S (2020) Transient neonatal sleep fragmentation results in long-term neuroinflammation and cognitive impairment in a rabbit model. Exp Neurol 327: 113212. https://doi.org/10.1016/j.expneurol.2020.113212
- Hidaka N, Suemaru K, Takechi K, Li B, Araki H (2011) Inhibitory effects of valproate on impairment of Y-maze alternation behavior induced by repeated electroconvulsive seizures and c-Fos protein levels in rat brains. Acta Med Okayama 65(4): 269–277. https://doi.org/10.18926/AMO/46853
- Garcia Y, Esquivel N (2018) Comparison of the Response of Male BALB/c and C57BL/6 Mice in Behavioral Tasks to Evaluate Cognitive Function. Behav Sci (Basel) 8(1): 14. https://doi.org/10.3390/bs8010014
- Attar A, Liu T, Chan W-T C, Hayes J, Nejad M, Lei K, Bitan G (2013) A shortened Barnes maze protocol reveals memory deficits at 4-months of age in the triple-transgenic mouse model of Alzheimer’s disease. PLoS One 8(11): e80355. https://doi.org/10.1371/journal.pone.0080355
- Gawel K, Gibula E, Marszalek-Grabska M, Filarowska J, Kotlinska JH (2019) Assessment of spatial learning and memory in the Barnes maze task in rodents-methodological consideration. Naunyn Schmiedebergs Arch Pharmacol 392(1): 1–18. https://doi.org/10.1007/s00210-018-1589-y
- Wang L, Wu H, Dai C, Peng Z, Song T, Xu L, Xu M, Shao Y, Li S, Fu W (2022) Dynamic hippocampal functional connectivity responses to varying working memory loads following total sleep deprivation. J Sleep Res: e13797. https://doi.org/10.1111/jsr.13797
- Piérard C, Liscia P, Philippin JN, Mons N, Lafon T, Chauveau F, Van Beers P, Drouet I, Serra A, Jouanin JC, Béracochéa D (2007) Modafinil restores memory performance and neural activity impaired by sleep deprivation in mice. Pharmacol Biochem Behav 88(1): 55–63. https://doi.org/10.1016/j.pbb.2007.07.006
- Chauveau F, Laudereau K, Libourel PA, Gervasoni D, Thomasson J, Poly B, Pierard C, Beracochea D (2014) Ciproxifan improves working memory through increased prefrontal cortex neural activity in sleep-restricted mice. Neuropharmacology 85: 349–356. https://doi.org/10.1016/j.neuropharm.2014.04.017
- Thomasson J, Canini F, Poly-Thomasson B, Trousselard M, Granon S, Chauveau F (2017) Neuropeptide S overcomes short term memory deficit induced by sleep restriction by increasing prefrontal cortex activity. Eur Neuropsychopharmacol 27(12): 1308–1318. https://doi.org/10.1016/j.euroneuro.2017.08.431
- Sportiche N, Suntsova N, Methippara M, Bashi T, Mitrani B, Szymusiak R, McGinty D (2010) Sustained sleep fragmentation results in delayed changes in hippocampal-dependent cognitive function associated with reduced dentate gyrus neurogenesis. Neuroscience 170(1): 247–258. https://doi.org/10.1016/j.neuroscience.2010.06
- Yin M, Chen Y, Zheng, H, Pu T, Marshall C, Wu T, Xiao M (2017) Assessment of mouse cognitive and anxiety-like behaviors and hippocampal inflammation following a repeated and intermittent paradoxical sleep deprivation procedure. Behav Brain Res 15(321): 69–78. https://doi.org/10.1016/j.bbr.2016.12.034
- Zamore Z, Veasey SC (2022) Neural consequences of chronic sleep disruption. Trends Neurosci 45(9): 678–691. https://doi.org/10.1016/j.tins.2022.05.007
- Looti Bashiyan Karabeg MM, Grauthoff S, Kollert SY, Weidner M, Heiming RS, Jansen F, Lewejohann L (2013) 5-HTT deficiency affects neuroplasticity and increases stress sensitivity resulting in altered spatial learning performance in the Morris water maze but not in the Barnes maze. PloS One 8(10): e78238. https://doi.org/10.1371/journal.pone.0078238
- Harrison FE, Hosseini AH, McDonald MP (2009) Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav Brain Res 198(1): 247–251. https://doi.org/10.1016/j.bbr.2008.10.015
- Meerlo P, Sgoifo A, Suchecki D (2008) Restricted and disrupted sleep: Effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Med Rev 12(3): 197–210. https://doi.org/10.1016/j.smrv.2007.07.007
- Украинцева ЮВ, Левкович КМ (2022) Негативное влияние нарушений сна на рабочую память может быть опосредовано изменениями углеводного обмена. Журн неврол психиатр им СС Корсакова Спецвыпуски 122(5-2): 11–17. [Ukraintseva YuV, Liaukovich KM (2022) The negative impact of sleep disorders on working memory may be mediated by changes in carbohydrate metabolism. Zhurn Nevrol I Psikhiatrii im SS Korsakova 122(5-2): 11–17. (In Russ)]. https://doi.org/10.17116/jnevro202212205211