SpringerLink
Log in

Effect of Acute and Chronic Sleep Deficit on Working and Long-Term Memory in Rats

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Insufficient sleep or circadian rhythm sleep-wake disorders have a detrimental effect on cognitive functions. It has long been thought that the weakest spot is memory consolidation, i.e., information transfer from short-term/working memory to long-term memory. However, there is a growing body of evidence showing that sleep disorders affect working memory most negatively. Here, we undertook an attempt to assess possible disturbances in working memory and long-term memory following the impact of sleep loss in acute and chronic experiments on rats. An orbital shaker was used to cause sleep deprivation/restriction according to the following protocols: 1—acute sleep deprivation for 18 h; 2—acute sleep restriction for 24 h (3 h of sleep deprivation alternated continuously with 1 h of sleep opportunity, with a total sleep loss of 18 h); 3—chronic sleep restriction (protocol 2 for five consecutive days). Acute sleep deprivation in the Y-maze test led to a significant decrease in the percentage of spontaneous alternations of the maze arms, indicating working memory impairment. In the Barnes maze test, the same exposure had no effect on long-term memory, as the time to enter the escape chamber (escape latency) did not change in this task. Acute and chronic sleep restriction caused no changes in both working and long-term memory. The results allow us to conclude that working memory (in contrast to long-term memory) is a vulnerable element of cognitive functions under conditions of acute sleep deprivation. This negative effect was abolished if sleep deprivation periods alternated with short sleep opportunity periods, indicating a protective significance of short rest/sleep periods for cognitive functions under conditions of sleep deficit. Hence, short-term sleep is beneficial for cognitive health as it protects working memory, whereas continuous long-term wakefulness impairs it.

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

Access this article

Log in via an institution

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 (Germany)

Instant access to the full article PDF.

Institutional subscriptions

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

REFERENCES

  1. Poluektov M (2019) Mysteries of sleep: from insomnia to lethargy. Al’pina Pabl, M. (In Russ).

    Google Scholar 

  2. Alhola P, Polo-Kantola P (2007) Sleep deprivation: Impact on cognitive performance. Neuropsychiatr Dis Treat 3(5): 553–567.

    PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  PubMed Central  Google Scholar 

  6. Born J, Wagner U (2004) Awareness in memory: being explicit about the role of sleep. Trends Cogn Sci 8: 242–244.

    Article  PubMed  Google Scholar 

  7. Gais S, Plihal W, Wagner U, Born J (2000) Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3: 1335–1339.

    Article  CAS  PubMed  Google Scholar 

  8. Jenkins JG, Dallenbach KM (1924) Obliviscence during Sleep and Waking. Am J Psychol 35(4): 605. https://doi.org/10.2307/1414040

    Article  Google Scholar 

  9. Rasch B, Born J (2013) About Sleep’s Role in Memory. Physiological Reviews 93(2): 681–766. https://doi.org/10.1152/physrev.00032.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. Gais S, Lucas B, Born J (2006) Sleep after learning aids memory recall. Learn Mem 13(3): 259–262.

    Article  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kovalzon VM (2023) Cerebral information processing during sleep: evolutionary and ecological approaches. J Evol Biochem Phys 59(2): 79–89.

    Article  Google Scholar 

  20. 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

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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

    Article  PubMed  Google Scholar 

  22. 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

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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 

  25. 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 

  26. 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

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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 

  28. 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.

    CAS  Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. 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

    Article  PubMed  PubMed Central  Google Scholar 

  31. Youngblood BD, Zhou J, Smagin GN, Ryan DH, Harris RB (1997) Sleep deprivation by the “flower pot” technique and spatial reference memory. Physiol and Behav 61(2): 249–256. https://doi.org/10.1016/s0031-9384(96)00363-0

    Article  CAS  Google Scholar 

  32. 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

    Article  CAS  PubMed  Google Scholar 

  33. 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 and Prevent 99: 428–433. https://doi.org/10.1016/j.aap.2015.10.012

    Article  Google Scholar 

  34. 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

    Article  PubMed  PubMed Central  Google Scholar 

  35. Deurveilher S, Semba K (2019) Physiological and Neurobehavioral Consequences of Chronic Sleep Restriction in Rodent Models. Handbook Behav Neurosci 30: 557–567. https://doi.org/10.1016/B978-0-12-813743-7.00037-2

    Article  Google Scholar 

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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. https://doi.org/10.17116/jnevro20211214026

    Article  CAS  Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. 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

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. 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

  42. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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

    Article  CAS  PubMed  Google Scholar 

  44. 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

  45. 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

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  CAS  PubMed  Google Scholar 

  49. Yin M, Chen Y, Zheng H, Pu T, Marshall C, Wu T, **ao 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

    Article  Google Scholar 

  50. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  CAS  Google Scholar 

  52. 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

    Article  CAS  PubMed  Google Scholar 

  53. 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

    Article  PubMed  Google Scholar 

  54. 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. https://doi.org/10.17116/jnevro202212205211

    Article  Google Scholar 

Download references

Funding

This work was State budget funded within the governmental assignment to IEPhB RAS (no. 075-00967-23-00).

Author information

Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    M. V. Chernyshev, M. A. Guseev & I. V. Ekimova

Authors
  1. M. V. Chernyshev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. A. Guseev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. V. Ekimova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization (I.V.E.), data collection (M.V.Ch., M.A.G.), data analysis (M.V.Ch., M.A.G., I.V.E.), writing and editing a manuscript (M.V.Ch., M.A.G., I.V.E.).

Corresponding author

Correspondence to M. V. Chernyshev.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Manipulations with animals were carried out in compliance with ethical standards approved by legal acts of the Russian Federation, the principles of the Basel Declaration, and recommendations approved by the Bioethics Committee of Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences (IEPhB RAS, meeting minutes No. 7 of July 22, 2021).

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

Additional information

Translated by A. Polyanovsky

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Russian Text © The Author(s), 2023, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2023, Vol. 59, No. 11, pp. 1635–1649https://doi.org/10.31857/S0869813923110031.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chernyshev, M.V., Guseev, M.A. & Ekimova, I.V. Effect of Acute and Chronic Sleep Deficit on Working and Long-Term Memory in Rats. J Evol Biochem Phys 59, 2129–2140 (2023). https://doi.org/10.1134/S0022093023060182

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093023060182

Keywords:

Search

Navigation