Critical Role of CA1 Nicotinic Receptors on Memory Acquisition Deficit Under Induction of Total Sleep Deprivation and REM Sleep Deprivation
International Clinical Neuroscience Journal,
Vol. 5 No. 1 (2018),
15 March 2018
Objective: Sleep disorder or sleep deprivation (SD) is a common issue in today’s society. Numerous evidences show that sleep is essential for proper brain performance and cognitive processes; on the other hand, cognitive functions have a broad range with learning and long-term memory as the most important ones related to attention. Since many studies show that cholinergic system has a significant role in sleep, learning, and memory, this study aims to investigate the impacts of CA1 Cholinergic Nicotinic Receptors on memory acquisition deficit which is stimulated by total sleep deprivation (TSD) and REM sleep deprivation (RSD).
Methodology: In this study a water box or a multi-platform apparatus was used in order to induce total sleep deprivation (TSD) or REM sleep deprivation (RSD). In order to investigate interactions of cholinergic system and hippocampus-dependent memory, nicotinic receptor agonist (nicotine) or nicotinic receptor antagonist (mecamylamine) was injected in hippocampal CA1.
Results: According to the results of this study, 24 hours TSD or RSD decreased memory acquisition and injection of nicotine (0.0001 or mecamylamine (0.001 in TSD and RSD sham groups didn’t change memory acquisition. However, injection of sub-threshold dose of nicotine (0.0001 and mecamylamine (0.001 could reduce negative effects of SD in both TSD and RSD.
Discussion; According to the present study, cholinergic nicotinic receptors are effective in learning and memory improvement.
How to Cite
Alhola P, Polo-Kantola P. Sleep deprivation: Impact on cognitive performance. Neuropsychiatric disease and treatment. 2007;3(5):553-67.
Lesku JA, Roth TC, 2nd, Amlaner CJ, Lima SL. A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology. The American naturalist. 2006;168(4):441-53.
Lesku JA, Roth TC, Rattenborg NC, Amlaner CJ, Lima SL. Phylogenetics and the correlates of mammalian sleep: a reappraisal. Sleep medicine reviews. 2008;12(3):229-44.
Maquet P. The role of sleep in learning and memory. Science. 2001;294(5544):1048-52.
Havekes R, Vecsey CG, Abel T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cellular signalling. 2012;24(6):1251-60.
Abel T, Havekes R, Saletin JM, Walker MP. Sleep, plasticity and memory from molecules to whole-brain networks. Current biology : CB. 2013;23(17):R774-88.
Lac G, Chamoux A. Elevated salivary cortisol levels as a result of sleep deprivation in a shift worker. Occupational medicine. 2003;53(2):143-5.
Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. Sleep loss: a novel risk factor for insulin resistance and Type 2 diabetes. Journal of applied physiology. 2005;99(5):2008-19.
Philibert I. Sleep loss and performance in residents and nonphysicians: a meta-analytic examination. Sleep. 2005;28(11):1392-402.
Lavenex P, Banta Lavenex P, Amaral DG. Postnatal development of the primate hippocampal formation. Developmental neuroscience. 2007;29(1-2):179-92.
Kreutzmann JC, Havekes R, Abel T, Meerlo P. Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience. 2015;309:173-90.
Ishikawa A, Kanayama Y, Matsumura H, Tsuchimochi H, Ishida Y, Nakamura S. Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus. The European journal of neuroscience. 2006;24(1):243-8.
Vecsey CG, Baillie GS, Jaganath D, Havekes R, Daniels A, Wimmer M, et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature. 2009;461(7267):1122-5.
Ravassard P, Pachoud B, Comte JC, Mejia-Perez C, Scote-Blachon C, Gay N, et al. Paradoxical (REM) sleep deprivation causes a large and rapidly reversible decrease in long-term potentiation, synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation in the dorsal hippocampus. Sleep. 2009;32(2):227-40.
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. Journal of sleep research. 2010;19(2):280-8.
Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA. Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Molecular and cellular neurosciences. 2011;46(4):742-51.
Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiological reviews. 2012;92(3):1087-187.
Watson CJ, Baghdoyan HA, Lydic R. Neuropharmacology of Sleep and Wakefulness: 2012 Update. Sleep medicine clinics. 2012;7(3):469-86.
Benedito MA, Camarini R. Rapid eye movement sleep deprivation induces an increase in acetylcholinesterase activity in discrete rat brain regions. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas / Sociedade Brasileira de Biofisica [et al]. 2001;34(1):103-9.
Irmak SO, de Lecea L. Basal forebrain cholinergic modulation of sleep transitions. Sleep. 2014;37(12):1941-51.
Rand JB. Acetylcholine. WormBook : the online review of C elegans biology. 2007:1-21.
Doyle DA. Structural changes during ion channel gating. Trends in neurosciences. 2004;27(6):298-302.
Pohanka M. Alpha7 nicotinic acetylcholine receptor is a target in pharmacology and toxicology. International journal of molecular sciences. 2012;13(2):2219-38.
Hefco V, Yamada K, Hefco A, Hritcu L, Tiron A, Olariu A, et al. Effects of nicotine on memory impairment induced by blockade of muscarinic, nicotinic and dopamine D2 receptors in rats. European journal of pharmacology. 2003;474(2-3):227-32.
Parfitt GM, Campos RC, Barbosa AK, Koth AP, Barros DM. Participation of hippocampal cholinergic system in memory persistence for inhibitory avoidance in rats. Neurobiology of learning and memory. 2012;97(2):183-8.
Paxinos G WC. The rat brain in stereotaxic coordinates. 6th ed ed. London, UK: Academic Press; 2007.
Hosseini N, Nasehi M, Radahmadi M, Zarrindast MR. Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats. Behavioural brain research. 2013;256:636-45.
Naseri MH, Hesami-Tackallou S, Torabi-Nami M, Zarrindast MR, Nasehi M. Involvement of the CA1 GABAA receptors in MK-801-induced anxiolytic-like effects: an isobologram analysis. Behavioural pharmacology. 2014;25(3):197-205.
Norozpour Y, Nasehi M, Sabouri-Khanghah V, Torabi-Nami M, Zarrindast MR. The effect of CA1 alpha2 adrenergic receptors on memory retention deficit induced by total sleep deprivation and the reversal of circadian rhythm in a rat model. Neurobiology of learning and memory. 2016;133:53-60.
Hajali V, Sheibani V, Ghazvini H, Ghadiri T, Valizadeh T, Saadati H, et al. Effect of castration on the susceptibility of male rats to the sleep deprivation-induced impairment of behavioral and synaptic plasticity. Neurobiology of learning and memory. 2015;123:140-8.
Ahmadi-Mahmoodabadi N, Nasehi M, Emam Ghoreishi M, Zarrindast MR. Synergistic effect between prelimbic 5-HT3 and CB1 receptors on memory consolidation deficit in adult male Sprague-Dawley rats: An isobologram analysis. Neuroscience. 2016;317:173-83.
Nascimento DC, Andersen ML, Hipolide DC, Nobrega JN, Tufik S. Pain hypersensitivity induced by paradoxical sleep deprivation is not due to altered binding to brain mu-opioid receptors. Behavioural brain research. 2007;178(2):216-20.
Nasehi M, Tabatabaie M, Khakpai F, Zarrindast MR. The effects of CA1 5HT4 receptors in MK801-induced amnesia and hyperlocomotion. Neuroscience letters. 2015;587:73-8.
Gould TJ, Wilkinson DS, Yildirim E, Poole RL, Leach PT, Simmons SJ. Nicotine shifts the temporal activation of hippocampal protein kinase A and extracellular signal-regulated kinase 1/2 to enhance long-term, but not short-term, hippocampus-dependent memory. Neurobiol Learn Mem. 2014;109:151-9.
Gold PE. Coordination of multiple memory systems. Neurobiology of learning and memory. 2004;82(3):230-42.
Hasselmo ME, McGaughy J. High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Progress in brain research. 2004;145:207-31.
James JR, Nordberg A. Genetic and environmental aspects of the role of nicotinic receptors in neurodegenerative disorders: emphasis on Alzheimer's disease and Parkinson's disease. Behavior genetics. 1995;25(2):149-59.
Hasselmo ME. The role of acetylcholine in learning and memory. Current opinion in neurobiology. 2006;16(6):710-5.
Dumas JA, Newhouse PA. The cholinergic hypothesis of cognitive aging revisited again: cholinergic functional compensation. Pharmacology, biochemistry, and behavior. 2011;99(2):254-61.
Bentley P, Driver J, Dolan RJ. Cholinergic modulation of cognition: insights from human pharmacological functional neuroimaging. Progress in neurobiology. 2011;94(4):360-88.
Glick SD, Greenstein S. Differential effects of scopolamine and mecamylamine on passive avoidance behavior. Life sciences Pt 1: Physiology and pharmacology. 1972;11(4):169-79.
Parikh V, Cole RD, Patel PJ, Poole RL, Gould TJ. Cognitive control deficits during mecamylamine-precipitated withdrawal in mice: Possible links to frontostriatal BDNF imbalance. Neurobiology of learning and memory. 2016;128:110-6.
Nickell JR, Grinevich VP, Siripurapu KB, Smith AM, Dwoskin LP. Potential therapeutic uses of mecamylamine and its stereoisomers. Pharmacology, biochemistry, and behavior. 2013;108:28-43.
Tadavarty R, Kaan TK, Sastry BR. Long-term depression of excitatory synaptic transmission in rat hippocampal CA1 neurons following sleep-deprivation. Experimental neurology. 2009;216(1):239-42.
Foster TC, Kumar A. Susceptibility to induction of long-term depression is associated with impaired memory in aged Fischer 344 rats. Neurobiology of learning and memory. 2007;87(4):522-35.
Kopp C, Longordo F, Nicholson JR, Luthi A. Insufficient sleep reversibly alters bidirectional synaptic plasticity and NMDA receptor function. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2006;26(48):12456-65.
Basheer R, Strecker RE, Thakkar MM, McCarley RW. Adenosine and sleep-wake regulation. Progress in neurobiology. 2004;73(6):379-96.
Bjorness TE, Greene RW. Adenosine and sleep. Current neuropharmacology. 2009;7(3):238-45.
Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW. Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science. 1997;276(5316):1265-8.
Schmitt LI, Sims RE, Dale N, Haydon PG. Wakefulness affects synaptic and network activity by increasing extracellular astrocyte-derived adenosine. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2012;32(13):4417-25.
Florian C, Vecsey CG, Halassa MM, Haydon PG, Abel T. Astrocyte-derived adenosine and A1 receptor activity contribute to sleep loss-induced deficits in hippocampal synaptic plasticity and memory in mice. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2011;31(19):6956-62.
Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annual review of neuroscience. 2001;24:677-736.
Park H, Poo MM. Neurotrophin regulation of neural circuit development and function. Nature reviews Neuroscience. 2013;14(1):7-23.
Hernandez PJ, Abel T. A molecular basis for interactions between sleep and memory. Sleep medicine clinics. 2011;6(1):71-84.
Cao X, Cui Z, Feng R, Tang YP, Qin Z, Mei B, et al. Maintenance of superior learning and memory function in NR2B transgenic mice during ageing. The European journal of neuroscience. 2007;25(6):1815-22.
Morris RG, Anderson E, Lynch GS, Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature. 1986;319(6056):774-6.
Cortese BM, Mitchell TR, Galloway MP, Prevost KE, Fang J, Moore GJ, et al. Region-specific alteration in brain glutamate: possible relationship to risk-taking behavior. Physiology & behavior. 2010;99(4):445-50.
Dash MB, Douglas CL, Vyazovskiy VV, Cirelli C, Tononi G. Long-term homeostasis of extracellular glutamate in the rat cerebral cortex across sleep and waking states. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2009;29(3):620-9.
Kruk-Slomka M, Budzynska B, Biala G. Involvement of cholinergic receptors in the different stages of memory measured in the modified elevated plus maze test in mice. Pharmacological reports : PR. 2012;64(5):1066-80.
Beer AL, Vartak D, Greenlee MW. Nicotine facilitates memory consolidation in perceptual learning. Neuropharmacology. 2013;64:443-51.
Shen JX, Yakel JL. Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system. Acta Pharmacol Sin. 2009;30(6):673-80.
Fu H, Dou J, Li W, Luo J, Li KC, Lam CS, et al. Mecamylamine prevents neuronal apoptosis induced by glutamate and low potassium via differential anticholinergic-independent mechanisms. Neuropharmacology. 2008;54(4):755-65.
Lima MM, Andersen ML, Reksidler AB, Silva A, Zager A, Zanata SM, et al. Blockage of dopaminergic D(2) receptors produces decrease of REM but not of slow wave sleep in rats after REM sleep deprivation. Behavioural brain research. 2008;188(2):406-11.
Beaulieu JM, Gainetdinov RR. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacological reviews. 2011;63(1):182-217.
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