Shiraz E-Medical Journal

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Aversive Memory, Anxiety-Related Behaviors, and Serum Neurochemical Levels in a Rat Model of Labored Sleep Loss

Mohammad Torabi-Nami 1 , * , Mohammad Nasehi 2 , Samira Razavi 3 and Mohammad Reza Zarrindast 4 , 5 , 6 , 7
Authors Information
1 Department of Neuroscience, School of Advanced Medical Sciences and technologies, Shiraz University of Medical Sciences, Shiraz, IR Iran
2 Department of Biology, Faculty of Basic Sciences, Islamic Azad University, Garmsar Branch, Semnan, IR Iran
3 Department of Biology, Science and Research Branch, Islamic Azad University, Tehran, IR Iran
4 Neuroscience Department, Advanced School of Medical Technologies and Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, IR Iran
5 Iranian National Center for Addiction Studies, Tehran University of Medical Sciences, Tehran, IR Iran
6 Institute for Studies in Theoretical Physics and Mathematics, School of Cognitive Sciences, Tehran, IR Iran
7 Institute for Cognitive Sciences Studies, Tehran, IR Iran
Article information
  • Shiraz E-Medical Journal: July 01, 2014, 15 (3); e22358
  • Published Online: July 20, 2014
  • Article Type: Research Article
  • Received: September 10, 2013
  • Revised: November 20, 2014
  • Accepted: June 30, 2014
  • DOI: 10.17795/semj22358

To Cite: Torabi-Nami M, Nasehi M, Razavi S, Zarrindast M R. Aversive Memory, Anxiety-Related Behaviors, and Serum Neurochemical Levels in a Rat Model of Labored Sleep Loss, Shiraz E-Med J. 2014 ; 15(3):e22358. doi: 10.17795/semj22358.

Copyright © 2014, Shiraz University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Materials and Methods
4. Results
5. Discussion
  • 1. Alhola P, Polo-Kantola P. Sleep deprivation: Impact on cognitive performance. Neuropsychiatr Dis Treat. 2007; 3(5): 553-67[PubMed]
  • 2. Ellenbogen JM. Cognitive benefits of sleep and their loss due to sleep deprivation. Neurology. 2005; 64(7)-7[DOI][PubMed]
  • 3. Deak MC, Stickgold R. Sleep and cognition. Wiley Interdiscip Rev Cogn Sci. 2010; 1(4): 491-500
  • 4. Kondratova AA, Kondratov RV. The circadian clock and pathology of the ageing brain. Nat Rev Neurosci. 2012; 13(5): 325-35[DOI][PubMed]
  • 5. Bueno OF, Lobo LL, Oliveira MG, Gugliano EB, Pomarico AC, Tufik S. Dissociated paradoxical sleep deprivation effects on inhibitory avoidance and conditioned fear. Physiol Behav. 1994; 56(4): 775-9[PubMed]
  • 6. Smith C, Rose GM. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol Behav. 1996; 59(1): 93-7[PubMed]
  • 7. Graves LA, Heller EA, Pack AI, Abel T. Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem. 2003; 10(3): 168-76[DOI][PubMed]
  • 8. Maquet P. The role of sleep in learning and memory. Science. 2001; 294(5544): 1048-52[DOI][PubMed]
  • 9. Esumi LA, Palma BD, Gomes VL, Tufik S, Hipolide DC. Inflammatory markers are associated with inhibitory avoidance memory deficit induced by sleep deprivation in rats. Behav Brain Res. 2011; 221(1): 7-12[DOI][PubMed]
  • 10. Havekes R, Vecsey CG, Abel T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell Signal. 2012; 24(6): 1251-60[PubMed]
  • 11. Rodgers RJ, Johnson NJ, Cole JC, Dewar CV, Kidd GR, Kimpson PH. Plus-maze retest profile in mice: importance of initial stages of trail 1 and response to post-trail cholinergic receptor blockade. Pharmacol Biochem Behav. 1996; 54(1): 41-50[PubMed]
  • 12. File SE. The interplay of learning and anxiety in the elevated plus-maze. Behav Brain Res. 1993; 58(1-2): 199-202[PubMed]
  • 13. Wall PM, Messier C. Concurrent modulation of anxiety and memory. Behav Brain Res. 2000; 109(2): 229-41[PubMed]
  • 14. Bertoglio LJ, Joca SR, Guimaraes FS. Further evidence that anxiety and memory are regionally dissociated within the hippocampus. Behav Brain Res. 2006; 175(1): 183-8[DOI][PubMed]
  • 15. Zarrindast MR, Naghdi-Sedeh N, Nasehi M, Sahraei H, Bahrami F, Asadi F. The effects of dopaminergic drugs in the ventral hippocampus of rats in the nicotine-induced anxiogenic-like response. Neurosci Lett. 2010; 475(3): 156-60[DOI][PubMed]
  • 16. Carvalho MC, Albrechet-Souza L, Masson S, Brandao ML. Changes in the biogenic amine content of the prefrontal cortex, amygdala, dorsal hippocampus, and nucleus accumbens of rats submitted to single and repeated sessions of the elevated plus-maze test. Braz J Med Biol Res. 2005; 38(12): 1857-66[PubMed]
  • 17. Carobrez AP, Bertoglio LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev. 2005; 29(8): 1193-205[DOI][PubMed]
  • 18. Gianlorenco AC, Canto-de-Souza A, Mattioli R. Microinjection of histamine into the cerebellar vermis impairs emotional memory consolidation in mice. Brain Res Bull. 2011; 86(1-2): 134-8[DOI][PubMed]
  • 19. Singh R, Kiloung J, Singh S, Sharma D. Effect of paradoxical sleep deprivation on oxidative stress parameters in brain regions of adult and old rats. Biogerontology. 2008; 9(3): 153-62[DOI][PubMed]
  • 20. Alzoubi KH, Khabour OF, Rashid BA, Damaj IM, Salah HA. The neuroprotective effect of vitamin E on chronic sleep deprivation-induced memory impairment: the role of oxidative stress. Behav Brain Res. 2012; 226(1): 205-10[DOI][PubMed]
  • 21. Laske C, Stransky E, Leyhe T, Eschweiler GW, Maetzler W, Wittorf A, et al. BDNF serum and CSF concentrations in Alzheimer's disease, normal pressure hydrocephalus and healthy controls. J Psychiatr Res. 2007; 41(5): 387-94[DOI][PubMed]
  • 22. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, et al. Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med. 2009; 15(3): 331-7[DOI][PubMed]
  • 23. 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(3): 309-16[PubMed]
  • 24. Hairston IS, Peyron C, Denning DP, Ruby NF, Flores J, Sapolsky RM, et al. Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J Neurophysiol. 2004; 91(4): 1586-95[DOI][PubMed]
  • 25. Everson CA, Bergmann BM, Rechtschaffen A. Sleep deprivation in the rat: III. Total sleep deprivation. Sleep. 1989; 12(1): 13-21[PubMed]
  • 26. Rechtschaffen A, Bergmann BM. Sleep deprivation in the rat by the disk-over-water method. Behav Brain Res. 1995; 69(1-2): 55-63[PubMed]
  • 27. Zarrindast MR, Nasehi M, Khansari M, Bananej M. Influence of nitric oxide agents in the rat amygdala on anxiogenic-like effect induced by histamine. Neurosci Lett. 2011; 489(1): 38-42[DOI][PubMed]
  • 28. Stern CA, Do Monte FH, Gazarini L, Carobrez AP, Bertoglio LJ. Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience. 2010; 170(1): 214-22[DOI][PubMed]
  • 29. Casarrubea M, Sorbera F, Crescimanno G. Structure of rat behavior in hole-board: I) multivariate analysis of response to anxiety. Physiol Behav. 2009; 96(1): 174-9[DOI][PubMed]
  • 30. Eslimi D, Oryan S, Nasehi M, Zarrindast MR. Effects of opioidergic systems upon anxiolytic-like behaviors induced in cholestatic rats. Eur J Pharmacol. 2011; 670(1): 180-5[DOI][PubMed]
  • 31. Haller J, Alicki M. Current animal models of anxiety, anxiety disorders, and anxiolytic drugs. Curr Opin Psychiatry. 2012; 25(1): 59-64[DOI][PubMed]
  • 32. Violle N, Balandras F, Le Roux Y, Desor D, Schroeder H. Variations in illumination, closed wall transparency and/or extramaze space influence both baseline anxiety and response to diazepam in the rat elevated plus-maze. Behav Brain Res. 2009; 203(1): 35-42[DOI][PubMed]
  • 33. Kumar T, Jha SK. Sleep deprivation impairs consolidation of cued fear memory in rats. PLoS One. 2012; 7(10)[DOI][PubMed]
  • 34. Pierard C, Liscia P, Chauveau F, Coutan M, Corio M, Krazem A, et al. Differential effects of total sleep deprivation on contextual and spatial memory: modulatory effects of modafinil. Pharmacol Biochem Behav. 2011; 97(3): 399-405[DOI][PubMed]
  • 35. Dorokhov VB, Kozhedub RG, Arsen'ev GN, Kozhechkin SN, Ukraintseva Iu V, Kulikov MA, et al. [Sleep deprivation effect upon spatial memory consolidation in rats after one-day learning in a Morris water maze]. Zh Vyssh Nerv Deiat Im I P Pavlova. 2011; 61(3): 322-31[PubMed]
  • 36. Chowdhury A, Chandra R, Jha SK. Total sleep deprivation impairs the encoding of trace-conditioned memory in the rat. Neurobiol Learn Mem. 2011; 95(3): 355-60[DOI][PubMed]
  • 37. 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. 2010; 19(2): 280-8[DOI][PubMed]
  • 38. Patti CL, Zanin KA, Sanday L, Kameda SR, Fernandes-Santos L, Fernandes HA, et al. Effects of sleep deprivation on memory in mice: role of state-dependent learning. Sleep. 2010; 33(12): 1669-79[PubMed]
  • 39. Ramanathan L, Hu S, Frautschy SA, Siegel JM. Short-term total sleep deprivation in the rat increases antioxidant responses in multiple brain regions without impairing spontaneous alternation behavior. Behav Brain Res. 2010; 207(2): 305-9[DOI][PubMed]
  • 40. Vollert C, Zagaar M, Hovatta I, Taneja M, Vu A, Dao A, et al. Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms. Behav Brain Res. 2011; 224(2): 233-40[DOI][PubMed]
  • 41. Babson KA, Trainor CD, Feldner MT, Blumenthal H. A test of the effects of acute sleep deprivation on general and specific self-reported anxiety and depressive symptoms: an experimental extension. J Behav Ther Exp Psychiatry. 2010; 41(3): 297-303[DOI][PubMed]
  • 42. Tartar JL, Ward CP, Cordeira JW, Legare SL, Blanchette AJ, McCarley RW, et al. Experimental sleep fragmentation and sleep deprivation in rats increases exploration in an open field test of anxiety while increasing plasma corticosterone levels. Behav Brain Res. 2009; 197(2): 450-3[DOI][PubMed]
  • 43. Zagaar M, Alhaider I, Dao A, Levine A, Alkarawi A, Alzubaidy M, et al. The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence. Neurobiol Dis. 2012; 45(3): 1153-62[DOI][PubMed]
  • 44. Cakir B, Kasimay O, Kolgazi M, Ersoy Y, Ercan F, Yegen BC. Stress-induced multiple organ damage in rats is ameliorated by the antioxidant and anxiolytic effects of regular exercise. Cell Biochem Funct. 2010; 28(6): 469-79[DOI][PubMed]
  • 45. Lopez-Rodriguez F, Wilson CL, Maidment NT, Poland RE, Engel J. Total sleep deprivation increases extracellular serotonin in the rat hippocampus. Neuroscience. 2003; 121(2): 523-30[PubMed]
  • 46. Lopez-Rodriguez F, Kim J, Poland RE. Total sleep deprivation decreases immobility in the forced-swim test. Neuropsychopharmacology. 2004; 29(6): 1105-11[DOI][PubMed]
  • 47. Clark CP, Golshan S. Antidepressant response to partial sleep deprivation in unipolar depression is not related to state anxiety. Depress Anxiety. 2008; 25(7)-4[DOI][PubMed]
  • 48. Curtis AL, Bello NT, Valentino RJ. Evidence for functional release of endogenous opioids in the locus ceruleus during stress termination. J Neurosci. 2001; 21(13)[PubMed]
  • 49. Redwine L, Hauger RL, Gillin JC, Irwin M. Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J Clin Endocrinol Metab. 2000; 85(10): 3597-603[DOI][PubMed]
  • 50. Lac G, Chamoux A. Elevated salivary cortisol levels as a result of sleep deprivation in a shift worker. Occup Med (Lond). 2003; 53(2): 143-5[PubMed]
  • 51. Angelucci F, Gelfo F, De Bartolo P, Caltagirone C, Petrosini L. BDNF concentrations are decreased in serum and parietal cortex in immunotoxin 192 IgG-Saporin rat model of cholinergic degeneration. Neurochem Int. 2011; 59(1): 1-4[DOI][PubMed]
  • 52. Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA. Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Mol Cell Neurosci. 2011; 46(4): 742-51[DOI][PubMed]
  • 53. 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): 387-90[PubMed]
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