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Repeated pre-training sleep restriction in adolescent rats impaired spatial performance

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Abstract

Chronic sleep deprivation (SD) is an overwhelming problem in young students. Firstly, we investigated whether different levels of pre-training SD had effects on spatial performance in adolescent rats. Rats were subjected to 2 or 4 h/day SD for 15 consecutive days. Morris water maze tests were conducted immediately after SD on experimental days 9–15. During the last 3 trials on the first training day, compared with their respective control animals, the rats with prior 4 h SD, but not 2 h SD, showed a significant reduction in percentage of the trials landing the platform without guidance (landing rate). During the whole 6 training days, the rats subjected to 4 h SD, not 2 h SD, spent longer time to locate the platform than the control rats did. In the probe test, the rats with 4 h SD and 2 h SD showed no significant difference with their respective control in time spent in the target quadrant and numbers of platform crossings. These results indicated that chronic prior 4 h SD, but not 2 h SD, impaired spatial acquisition capability in adolescent rats. Secondly, we explored whether huperzine A (Hup A), which has been proved to improve cognitive impairment in dementia, could prevent adolescent rats from chronic 4 h SD-induced learning decline. Hup A (0.1 mg/kg/day) was administered by gavage 30 min before the end of 4 h SD. With hup A treatment, the reduced landing rate was increased and the prolonged escape latency and distance were shortened, which suggested that hup A was promising in preventing the spatial cognitive deficits induced by repeated sleep restriction in adolescents.

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References

  1. Schonauer M, Pawlizki A, Kock C, Gais S. Exploring the effect of sleep and reduced interference on different forms of declarative memory. Sleep. 2014;37(12):1995–2007.

    PubMed  PubMed Central  Google Scholar 

  2. Esposito MJ, Occhionero M, Cicogna P. Sleep deprivation and time-based prospective memory. Sleep. 2015;38(11):1823–6.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Louca M, Short MA. The effect of one night’s sleep deprivation on adolescent neurobehavioral performance. Sleep. 2014;37(11):1799–807.

    PubMed  PubMed Central  Google Scholar 

  4. Scullin MK, Bliwise DL. Sleep, cognition, and normal aging: integrating a half century of multidisciplinary research. Perspect Psychol Sci. 2015;10(1):97–137.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Loessl B, Valerius G, Kopasz M, Hornyak M, Riemann D, Voderholzer U. Are adolescents chronically sleep-deprived? An investigation of sleep habits of adolescents in the Southwest of Germany. Child Care Health Dev (Multicenter Study Research Support, Non-U.S. Gov’t). 2008;34(5):549–56.

    Article  CAS  PubMed  Google Scholar 

  6. Moore M. Behavioral sleep problems in children and adolescents. J Clin Psychol Med Settings. 2012;19(1):77–83.

    Article  PubMed  Google Scholar 

  7. Mednick SC, Cai DJ, Shuman T, Anagnostaras S, Wixted JT. An opportunistic theory of cellular and systems consolidation. Trends Neurosci (Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t). 2011;34(10):504–14.

    CAS  Google Scholar 

  8. Tononi G, Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron. 2014;81(1):12–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hagewoud R, Havekes R, Novati A, Keijser JN, Van der Zee EA, Meerlo P. Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J Sleep Res (Research Support, Non-U.S. Gov’t). 2010;19(2):280–8.

    Google Scholar 

  10. Yoo SS, Hu PT, Gujar N, Jolesz FA, Walker MP. A deficit in the ability to form new human memories without sleep. Nat Neurosci (Comparative Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t). 2007;10(3):385–92.

    CAS  Google Scholar 

  11. Van Der Werf YD, Altena E, Schoonheim MM, Sanz-Arigita EJ, Vis JC, De Rijke W, et al. Sleep benefits subsequent hippocampal functioning. Nat Neurosci (Research Support, Non-U.S. Gov’t). 2009;12(2):122–3.

    Google Scholar 

  12. Kirszenblat L, van Swinderen B. The Yin and Yang of sleep and attention. Trends Neurosci. 2015;38(12):776–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kalonia H, Bishnoi M, Kumar A. Possible mechanism involved in sleep deprivation-induced memory dysfunction. Methods Find Exp Clin Pharmacol. 2008;30(7):529–35.

    Article  CAS  PubMed  Google Scholar 

  14. Bowers MB Jr, Hartmann EL, Freedman DX. Sleep deprivation and brain acetylcholine. Science. 1966;153(3742):1416–7.

    Article  CAS  PubMed  Google Scholar 

  15. **ng SH, Zhu CX, Zhang R, An L. Huperzine a in the treatment of Alzheimer’s disease and vascular dementia: a meta-analysis. Evid Based Complement Altern Med. 2014;2014:363985.

    Article  Google Scholar 

  16. Damar U, Gersner R, Johnstone JT, Schachter S, Rotenberg A. Huperzine A as a neuroprotective and antiepileptic drug: a review of preclinical research. Expert Rev Neurother. 2016;16(6):671–80.

    Article  CAS  PubMed  Google Scholar 

  17. Zheng W, **ang YQ, Li XB, Ungvari GS, Chiu HF, Sun F, et al. Adjunctive huperzine A for cognitive deficits in schizophrenia: a systematic review and meta-analysis. Hum Psychopharmacol. 2016;31(4):286–95.

    Article  CAS  PubMed  Google Scholar 

  18. Yang SR, Sun H, Huang ZL, Yao MH, Qu WM. Repeated sleep restriction in adolescent rats altered sleep patterns and impaired spatial learning/memory ability. Sleep (Research Support, Non-U.S. Gov’t). 2012;35(6):849–59.

    Google Scholar 

  19. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev. 2000;24(4):417–63.

    Article  CAS  PubMed  Google Scholar 

  20. Wang J, Zhang HY, Tang XC. Huperzine a improves chronic inflammation and cognitive decline in rats with cerebral hypoperfusion. J Neurosci Res (Research Support, Non-U.S. Gov’t). 2010;88(4):807–15.

    CAS  Google Scholar 

  21. Tobler I, Deboer T, Fischer M. Sleep and sleep regulation in normal and prion protein-deficient mice. J Neurosci (Research Support, Non-U.S. Gov’t). 1997;17(5):1869–79.

    CAS  Google Scholar 

  22. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848–58.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Qureshi AI, Giles WH, Croft JB, Bliwise DL. Habitual sleep patterns and risk for stroke and coronary heart disease: a 10-year follow-up from NHANES I. Neurology. 1997;48(4):904–11.

    Article  CAS  PubMed  Google Scholar 

  24. Luyster FS, Strollo PJ Jr, Zee PC, Walsh JK. Boards of Directors of the American Academy of Sleep M, the Sleep Research S. Sleep: a health imperative. Sleep. 2012;35(6):727–34.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Novati A, Hulshof HJ, Koolhaas JM, Lucassen PJ, Meerlo P. Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience (Research Support, Non-U.S. Gov’t). 2011;8(190):145–55.

    Google Scholar 

  26. Soto-Rodriguez S, Lopez-Armas G, Luquin S, Ramos-Zuniga R, Jauregui-Huerta F, Gonzalez-Perez O, et al. Rapid eye movement sleep deprivation produces long-term detrimental effects in spatial memory and modifies the cellular composition of the subgranular zone. Front Cell Neurosci. 2016;10(132):1–13.

    Google Scholar 

  27. Tartar JL, Ward CP, McKenna JT, Thakkar M, Arrigoni E, McCarley RW, et al. Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation. Eur J Neurosci (Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, Non-P.H.S.). 2006;23(10):2739–48.

    Google Scholar 

  28. Guan Z, Peng X, Fang J. Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus. Brain Res (Research Support, U.S. Gov’t, P.H.S.). 2004;1018(1):38–47.

    CAS  Google Scholar 

  29. Ward CP, McCoy JG, McKenna JT, Connolly NP, McCarley RW, Strecker RE. Spatial learning and memory deficits following exposure to 24 h of sleep fragmentation or intermittent hypoxia in a rat model of obstructive sleep apnea. Brain Res. 2009;19(1294):128–37.

    Article  Google Scholar 

  30. 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.

    Article  PubMed  Google Scholar 

  31. Ohba T, Yoshino Y, Ishisaka M, Abe N, Tsuruma K, Shimazawa M, et al. Japanese Huperzia serrata extract and the constituent, huperzine A, ameliorate the scopolamine-induced cognitive impairment in mice. Biosci Biotechnol Biochem. 2015;79(11):1838–44.

    Article  CAS  PubMed  Google Scholar 

  32. Mao XY, Cao DF, Li X, Yin JY, Wang ZB, Zhang Y, et al. Huperzine A ameliorates cognitive deficits in streptozotocin-induced diabetic rats. Int J Mol Sci. 2014;15(5):7667–83.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Tang LL, Wang R, Tang XC. Huperzine A protects SHSY5Y neuroblastoma cells against oxidative stress damage via nerve growth factor production. Eur J Pharmacol. 2005;519(1–2):9–15.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to students of Shanghai Medical College of Fudan University **ang-Da Meng, Zheng-Liang Li, **ao-** Malin, Wan-Na Chen, Ren-Jie Wang, Jie Chen, Bu-Qing Liang, Yin Wang, and Lin Lin for their contributions to the experimental work. We thank professor Zhi-Li Huang, Department of Pharmacology, School of Basic Medical Sciences, State Key Laboratory of Medical Neurobiology and Institutes of Brain Science, Fudan University for his critical comments.

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Correspondence to Su-Rong Yang.

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Conflict of interest

Author Su-Rong Yang declares that she has no conflict of interest. Author Huan-**n Sun declares that she has no conflict of interest. Author Zhen-zhen Hu declares that she has no conflict of interest. Author Si-Heng Wang declares that he has no conflict of interest. Author Hui Sun declares that she has no conflict of interest. Author Yin-Jia Xue declares that he has no conflict of interest. Author Chen-Bo Ye declares that he has no conflict of interest.

Disclosure statement

This was not an industry supported study. None of the authors has any financial interest or conflicts of interest related to this work.

Ethical approval

Experimental protocols were approved by the Shanghai Medical Experimental Animal Administrative Committee.

Source of funding

This study was supported by National Natural Science Foundation of China (81571296), Shanghai Committee of Science and Technology (11ZR1402000), and Shanghai Leading Academic Discipline Project (B119).

Additional information

S.-R. Yang, H.-X. Sun, and Z.-Z. Hu contributed equally to this work.

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Yang, SR., Sun, HX., Hu, ZZ. et al. Repeated pre-training sleep restriction in adolescent rats impaired spatial performance. Sleep Biol. Rhythms 15, 57–65 (2017). https://doi.org/10.1007/s41105-016-0080-8

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