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Post-learning REM sleep deprivation impairs long-term memory: Reversal by acute nicotine treatment
Neuroscience Letters 499 (2011) 28–31
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Post-learning REM sleep deprivation impairs long-term memory: Reversal by acute nicotine treatment A.M. Aleisa a , K.H. Alzoubi b , K.A. Alkadhi c,∗ a b c
Department of Pharmacology, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia Department of Clinical Pharmacy, Faculty of Pharmacy, Jordan University of Science and Technology, Irbid, Jordan Department of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5037, United States
a r t i c l e
i n f o
Article history: Received 3 February 2011 Received in revised form 28 April 2011 Accepted 13 May 2011 Keywords: Nicotine Sleep deprivation Post-learning Memory Hippocampus Maze
a b s t r a c t Rapid eye movement sleep deprivation (REM-SD) is associated with spatial learning and memory impairment. During REM-SD, an increase in nicotine consumption among habitual smokers and initiation of tobacco use by non-smokers have been reported. We have shown recently that nicotine treatment prevented learning and memory impairments associated with REM-SD. We now report the interactive effects of post-learning REM-SD and/or nicotine. The animals were first trained on the radial arm water maze (RAWM) task, then they were REM-sleep deprived using the modified multiple platform paradigm for 24 h. During REM-SD period, the rats were injected with saline or nicotine (1 mg/kg s.c. every 12 h: a total of 3 injections). The animals were tested for long-term memory in the RAWM at the end of the REMSD period. The 24 h post-learning REM-SD significantly impaired long-term memory. However, nicotine treatment reversed the post-learning REM-SD-induced impairment of long-term memory. On the other hand, post-learning treatment of normal rats with nicotine for 24 h enhanced long-term memory. These results indicate that post-learning acute nicotine treatment prevented the deleterious effect of REM-SD on cognitive abilities. © 2011 Elsevier Ireland Ltd. All rights reserved.
Rapid eye movement (REM) sleep, has an essential role in learning and memory formation in the hippocampus [48]. This has been studied in both humans and experimental animals using REM-sleep-deprivation (REM-SD) as a model [81,62,30,52,3–5]. Previous studies have shown that REM-SD impairs hippocampusdependent learning and memory [81,30,3–5,66,49,74]. We have recently reported that the negative effects of REM-SD may be related to alteration in the levels of important signaling molecules involved in memory and synaptic plasticity [4,5]. Increased frequency of nicotine consumption has been reported in REM-sleep-deprived smokers [56,31]. Nicotine is also known to alleviate impairment of memory associated with psychosocial stress [1,2,12], aging [17], hypothyroidism [8,9,13], Alzheimer’s disease [36,79,69,70], Parkinson’s disease [38], schizophrenia [67,32,37], and attention deficit/hyperactivity disorder (ADHD) [58,61]. Additionally, nicotine facilitates the induction of LTP, the cellular correlates for memory, in rat hippocampal slices [26,33] and induces long lasting potentiation in the mouse dentate gyrus (DG) region of the hippocampus [65]. Furthermore, nicotine treatment attenuates impairment of hippocampal LTP caused by chronic psychosocial stress [1], hypothyroidism [9] and aging [25]. Therefore, the reported increase in nicotine use among smokers and
∗ Corresponding author. Tel.: +1 713 743 1212; fax: +1 713 743 1229. E-mail address: [email protected] (K.A. Alkadhi). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.05.025
the initiation of smoking among non-smokers during REM-SD [56,31,60] could be a form of self-medication to correct the impairment of cognition and synaptic plasticity. We have recently reported that acute nicotine treatment prevented REM-SD induced impairment of short-term memory and synaptic plasticity of hippocampal CA1 [3]. In the present communication, we report the effect of post-learning REM-SD and/or acute nicotine treatment on long-term memory. Nicotine is a nAChRs agonist with beneficial effects on cognition, mediated mainly through activation of ␣7nAChRs (e.g., see [20] for review). Adult male Wistar rats (200–250 g), housed 6 per cage with free access to food and water, were subjected to a 12 h light/dark (lights on at 7:00 am) cycle at 25 ◦ C. All procedures involving animals were carried out in accordance with the National Research Council’s Guide for the Care and Use of Laboratory Animals and on approval of the University of Houston Institutional Animal Care and Use Committee. All behavioral and electrophysiological experiments were started at 9 am, and were terminated no later than 5 pm. There were four treatment groups in this study: postlearning control, post-learning REM-SD, post-learning nicotine, and post-learning nicotine plus post-learning REM-SD (post-learning Nic/REM-SD). Post-learning nicotine and post-learning Nic/REMSD groups were treated with nicotine (Sigma, St. Louis, MO) during REM-SD only (1 mg/kg/12 h s.c.: a total of 3 injections during the 24 h of REM-SD). This dose is known to produce blood nicotine levels similar to those of chronic smokers [45,15], and was previously
A.M. Aleisa et al. / Neuroscience Letters 499 (2011) 28–31
used in several studies showing neuroprotective properties of the drug in animals (e.g., [1,9,69,3]). Both the post-learning REM-SD and post-learning Nic/REM-SD groups were sleep deprived for 24 h using columns-in-water (modified multiple platform) model as described [3–5,50]. Animals in each group were REM sleep-deprived together to eliminate isolation stress. Immediately after the end of the training (learning) phase, animals were placed on platforms (20 platforms; 20 cm high and 5 cm diameter, 7 cm apart edge-to-edge) in an aquarium where water and food were accessible to animals. The water level in the aquarium (24 ± 1 ◦ C) was about 2 cm below the edge of the platform. This method has been reported to interfere with total sleep, but it mainly eliminates REM sleep [28,46]. Loss of muscle tone during REM sleep caused the rat’s snout to dip into the water, or occasionally, the rat, to fall into the water, and awaken. Immediately after REM-SD, animals were tested for long-term memory. The RAWM consists of a black circular water tank with 6 Vshaped stainless steel structures arranged to form a swimming field of an open central area and 6 arms. The RAWM design [22,54] resembles a radial arm maze inserted into a Morris maze (a circular tank filled with water). The water temperature was maintained at 24 ± 1 ◦ C. The goal arm was one that contained a black removable platform submerged 1 cm below the water level. The RAWM task was conducted as reported [3,5]. Briefly, animals were first trained on the RAWM task; beginning from a start arm (any arm other than the goal arm); the rat must find the submerged platform by swimming to the end of the goal arm. Each rat was allowed twelve consecutive training trials (learning phase: 2 blocks of 6 trials interspersed by a 5-min rest period). Thereafter, post-learning REM-SD and post-learning Nic/REM-SD groups were sleep deprived for 24 h, followed by a long-term memory test (24 h after trial # 12). Rats were allowed 1 min per RAWM trial to find the submerged platform. A trial ended when the rat located the submerged platform, where it was allowed a 15 s stay on the platform before removal to start the next trial in a different start arm. If the rat did not find the submerged platform in the goal arm within 1 min, the experimenter would guide the rat to the goal arm and allow it to stay on the platform for 15 s before removal to begin the next trial. A correct selection occurred when the rat swam into the goal arm, while error was registered each time the rat entered into an arm other than the goal arm. All experiments were done in a dimly lit room with visual cues on the walls. Data are expressed as means ± SEM. All statistics were carried out using two-way ANOVA followed by Tukey posttest. P ≤ 0.05 was considered statistically significant. Before any treatment, the four groups of naïve rats were first trained on the RAWM to finish the 12 learning trials where each rat in each group successfully learned to find the hidden platform (Fig. 1). Memory test after 24 h REM-SD, showed markedly impaired long-term memory. This is indicated by the observation that 24 h post-learning REM-SD group (Fig. 2) made significantly (P < 0.01) more errors in long-term memory trial to locate the hidden platform than the post-learning control group. Acute nicotine treatment, clearly, prevented REM-SD-induced impairment of long-term memory as tested in the RAWM. In the long-term memory test, rats in the post-learning Nic/REM-SD group made significantly (P < 0.001) fewer errors to locate the hidden platform than the untreated 24 h post-learning REM-SD group (Fig. 2). Interestingly, post-learning rats treated with nicotine alone made significantly (P < 0.05) fewer errors compared to the untreated postlearning control rats (Fig. 2). The major finding of this study is that acute nicotine treatment during post-learning REM-SD prevents impairment of long-term memory. Additionally, acute nicotine enhanced long-term memory in post-learning control animals. Sleep loss impairs learning and memory in human [59,77,51] and animal studies [81,30,3,5,66,49]. In addition, REM-SD blocks hippocampal LTP [3–5,56,50,40,34]. We
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Fig. 1. Effect of acute nicotine treatment (1 mg/kg/12 h s.c.: a total of 3 injections during the 24 h of SD). Without sleep deprivation, all groups performed similarly during learning phase in the RAWM. After post-learning 24 h sleep deprivation, the REM-SD rats committed more errors in finding the hidden platform than control rats. Interestingly, acute nicotine treatment significantly (P < 0.05) improved longterm memory in control rats that have gone through RAWM training. *Significant difference from control, Nic and REM-SD/Nic group (P < 0.01). #Significant difference from control group (P < 0.05). Data are presented as mean ± SEM (N = 8–10).
have previously, shown that REM-SD impairs short-term memory [3,5]. In parallel, the present work demonstrates that, when induced after learning, REM-SD impairs hippocampus-dependent long-term memory. When adrenal stress response was eliminated by corticosterone synthesis inhibitor, metyrapone [75] or by adrenalectomy [64], the negative effect of REM-SD on learning and memory persisted suggesting that this effect was not due to the release of stress hormones. Additionally, the modified multiple platform method eliminates immobilization and isolation stresses. Moreover, when wide columns that allowed rats to sleep, were used in the same aquarium, animals did not show impairment of spatial learning and memory [4,5]. Furthermore, it is possible that the anxiety and stress resulting from possible tumbling into water may have contributed to the memory deficits. However, we propose that REM-SD may
Fig. 2. Effect of acute nicotine treatment on sleep deprivation-impaired long-term memory. This graph summarizes the average number of errors made by each of the four groups in the long-term memory test. Each point is the mean ± SEM of 8–10 rats. *Significant difference from all other groups (P < 0.01) and #significant difference from all other groups (P < 0.05).
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be the major factor that causes long-term memory impairment. We have shown that stress affects the hippocampus in a considerably different manner than REM-SD; for example, whereas, REM-SD impairs learning [3,6], exposure to psychosocial stress for six weeks does not influence this function [1]. Findings of the current and previous studies [3–5] showing that REM-SD impairs hippocampus-dependent learning and memory, are in agreement with the results obtained by studies concerning the effect of total sleep deprivation on cognitive functions [30,39,27,19,57]. In fact, it should be noted that sleep deprivation methods, including the multiple platform method, induce deprivation of both sleep phases to a varying degree [46]. The multiple platform method has been shown to decrease slow-wave sleep and abolishes REM sleep [28,46]. Therefore, results of the current study and similar previous studies mainly represent REM-SD [3–5]. Reports on the effect of nicotine on memory in normal subjects are variable. While some investigators show enhancement of normal memory as a result of nicotine treatment ([78,41–43,14,16,44,71] for review), others report no effect [1,24,55,9], or even memory impairment [68,53]. The inconsistency in the reported effect of nicotine on memory could be related to the nicotine dosing level, duration of treatment, route of administration and experimental procedures used. In this study, acute nicotine enhanced long-term memory in post-learning control animals. Nicotine-induced enhancement of long-term memory in control animals may be related to the fact that these animals are not normal controls; they have gone through learning trials, which may suggest that nicotine strengths memory following learning. Results of the current study show that acute nicotine prevents post-learning REM-SD-induced long-term memory impairment. Similarly, we have recently reported that nicotine prevented the effects of REM-SD on learning and memory, when REM-SD and nicotine are administered before learning. In agreement, previous studies have shown beneficial effects for nicotine on memory impairment associated with several brain disorders including chronic mental stress [1,12], Alzheimer’s disease [69,70] and hypothyroidism [8,10]. The neuroprotective effects of nicotine may be attributed to a number of possible mechanisms. Nicotine activates presynaptic nAChR (mainly ␣7nAChR), which increases the influx of calcium, and, thus, enhances glutamate release from presynaptic nerve terminals at the pyramidal cells in area CA1 of the hippocampus [29,35]. Nicotine therefore, increases the probability of coincidence between presynaptic release and postsynaptic depolarization, and therefore raises the probability of LTP induction [35,47]. In addition, highly localized calcium influx through nAChR activates protein kinases and phosphatases cascades, which modulate neurotransmitter release. Other studies show that in cultured CA1 neurons, nicotine treatment desensitizes ␣7nAChR on the GABAergic interneurons resulting in reduced release of GABA from these interneurons, thus indirectly increasing excitability of the pyramidal cell [7]. This, in turn, facilitates LTP by decreasing its threshold of induction [26]. It is well known that glutamatergic NMDA receptor plays a crucial role in spatial memory (e.g., [73]). Sleep loss reduces hippocampal NMDA receptor expression [50,73,72], lowers excitatory postsynaptic currents [18] and decreases levels of NR1 subunit of NMDA receptor in area CA1 [63]. In contrast, nicotine treatment enhances the expression of hippocampal NMDA receptor subunit 2A and 2B (NR2A, NR2B) [21,11], enhances the NMDA receptormediated currents and increases tyrosine phosphorylation of NR2B subunit [80]. Therefore, countering the negative effect of sleep loss on NMDA receptors could be another mechanism of the observed nicotine action. There are many implications of the interactive effect of nicotine and REM-SD. Nicotine affect various brain regions, especially the
cortex and the hippocampus, where it enhances cognitive functions in these regions (reviewed in [76]). In addition, nicotine and other nAChRs agonists have been reported to ameliorate symptoms of schizophrenia [23] and other mental disorders [20]. These findings support the results of the current study. Collectively, the findings of this study indicate that, when both instituted after learning, acute nicotine treatment antagonizes the deleterious effect of REM-SD on long-term memory.
References [1] A.M. Aleisa, K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Nicotine blocks stressinduced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region, Int. J. Neuropsychopharmacol. 9 (2006) 417–426. [2] A.M. Aleisa, K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Chronic psychosocial stressinduced impairment of hippocampal LTP: possible role of BDNF, Neurobiol. Dis. 22 (2006) 453–462. [3] A.M. Aleisa, G. Helal, I.A. Alhaider, K.H. Alzoubi, M. Srivareerat, T.T. Tran, S.S. Al-Rejaie, K.A. Alkadhi, Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat, Hippocampus (2011), doi:10.1002/hipo.20806. [4] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.A. Alkadhi, Caffeine prevents sleep lossinduced deficits in long-term potentiation and related signaling molecules in the dentate gyrus, Eur. J. Neurosci. 31 (2010) 1368–1376. [5] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.H. Alzoubi, K.A. Alkadhi, Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity, Sleep 33 (2010) 437–444. [6] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.A. Alkadhi, Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine, Mol. Cell. Neurosci. 46 (4) (2011) 742–751. [7] M. Alkondon, M.F. Braga, E.F. Pereira, A. Maelicke, Albuquerque EX alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus, Eur. J. Pharmacol. 393 (2000) 59–67. [8] K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Levothyroxin restores hypothyroidisminduced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies, Exp. Neurol. 195 (2005) 330–341. [9] K.H. Alzoubi, A.M. Aleisa, N.Z. Gerges, K.A. Alkadhi, Nicotine reverses adultonset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies, J. Neurosci. Res. 84 (2006) 944–953. [10] K.H. Alzoubi, A.M. Aleisa, K.A. Alkadhi, Molecular studies on the protective effect of nicotine in adult-onset hypothyroidism-induced impairment of long-term potentiation, Hippocampus 16 (2006) 861–874. [11] K.H. Alzoubi, A.M. Aleisa, K.A. Alkadhi, Adult-onset hypothyroidism facilitates and enhances LTD: reversal by chronic nicotine treatment, Neurobiol. Dis. 26 (2007) 264–272. [12] K.H. Alzoubi, K.K. Abdul-Razzak, O.F. Khabour, G.M. Al-Tuweiq, M.A. Alzubi, K.A. Alkadhi, Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats, Behav. Brain Res. 204 (2009) 117–123. [13] K.H. Alzoubi, N.Z. Gerges, A.M. Aleisa, K.A. Alkadhi, Levothyroxin restores hypothyroidism-induced impairment of hippocampus-dependent learning and memory: behavioral, electrophysiological, and molecular studies, Hippocampus 19 (2009) 66–78. [14] A. Bancroft, E.D. Levin, Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory, Neuropharmacology 39 (2000) 2770–2778. [15] N.L. Benowitz, P. Jacob 3rd, C. Denaro, R. Jenkins, Stable isotope studies of nicotine kinetics and bioavailability, Clin Pharmacol Ther. 49 (1991) 270–277. [16] J.H. Bettany, E.D. Levin, Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze, Pharmacol. Biochem. Behav. 70 (2001) 467–474. [17] C. Carrasco, P. Vicens, R. Redolat, Neuroprotective effects of behavioural training and nicotine on age-related deficits in spatial learning, Behav. Pharmacol. 17 (2006) 441–452. [18] C. Chen, M. Hardy, J. Zhang, G.J. LaHoste, N.G. Bazan, Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments, Biochem. Biophys. Res. Commun. 340 (2006) 435–440. [19] A. Chowdhury, R. Chandra, S.K. Jha, Total sleep deprivation impairs the encoding of trace-conditioned memory in the rat, Neurobiol. Learn. Mem. 95 (2011) 355–360. [20] S.L. Cincotta, M.S. Yorek, T.M. Moschak, S.R. Lewis, J.S. Rodefer, Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction, Curr. Opin. Investig. Drugs 9 (2008) 47–56. [21] N. Delibas, D.K. Doguc, R. Sutcu, E. Eroglu, O. Gokalp, Effect of nicotine on hippocampal nicotinic acetylcholine alpha7 receptor and NMDA receptor subunits 2A and 2B expression in young and old rats, Int. J. Neurosci. 115 (2005) 1151–1163. [22] D.M. Diamond, C.R. Park, K.L. Heman, G.M. Rose, Exposing rats to a predator impairs spatial working memory in the radial arm water maze, Hippocampus 9 (1999) 542–552.
A.M. Aleisa et al. / Neuroscience Letters 499 (2011) 28–31 [23] M.S. D’Souza, A. Markou, Schizophrenia and tobacco smoking comorbidity: nAChR agonists in the treatment of schizophrenia-associated cognitive deficits, Neuropharmacology (2011), doi:10.1016/j.neuropharm.2011.01044. [24] M.P. Dunne, D. Macdonald, L.R. Hartley, The effects of nicotine upon memory and problem solving performance, Physiol. Behav. 37 (1986) 849–854. [25] S. Fujii, K. Sumikawa, Acute and chronic nicotine exposure reverse age-related declines in the induction of long-term potentiation in the rat hippocampus, Brain Res. 894 (2001) 347–353. [26] S. Fujii, Z. Ji, N. Morita, K. Sumikawa, Acute and chronic nicotine exposure differentially facilitate the induction of LTP, Brain Res. 846 (1999) 137–143. [27] A. Gosselin, J. De Koninck, K.B. Campbell, Total sleep deprivation and novelty processing: implications for frontal lobe functioning, Clin. Neurophysiol. 116 (2005) 211–222. [28] S. Grahnstedt, R. Ursin, Platform sleep deprivation affects deep slow wave sleep in addition to REM sleep, Behav. Brain Res. 18 (1985) 233–239. [29] R. Gray, A.S. Rajan, K.A. Radcliffe, M. Yakehiro, J.A. Dani, Hippocampal synaptic transmission enhanced by low concentrations of nicotine, Nature 383 (1996) 713–716. [30] Z. Guan, X. Peng, J. Fang, Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus, Brain Res. 1018 (2004) 38–47. [31] A. Hamidovic, H. de Wit, Sleep deprivation increases cigarette smoking, Pharmacol. Biochem. Behav. 93 (2009) 263–269. [32] J.G. Harris, S. Kongs, D. Allensworth, L. Martin, J. Tregellas, B. Sullivan, G. Zerbe, R. Freedman, Effects of nicotine on cognitive deficits in schizophrenia, Neuropsychopharmacology 29 (2004) 1378–1385. [33] J. He, C.Y. Deng, X.N. Zhu, J.P. Yu, R.Z. Chen, Different synaptic mechanisms of long-term potentiation induced by nicotine and tetanic stimulation in hippocampal CA1 region of rats, Acta Pharmacol. Sin. 24 (2003) 398–402. [34] A. Ishikawa, Y. Kanayama, H. Matsumura, H. Tsuchimochi, Y. Ishida, S. Nakamura, Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus, Eur. J. Neurosci. 24 (2006) 243–248. [35] D. Ji, R. Lape, J.A. Dani, Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity, Neuron 31 (2001) 131–141. [36] G.M. Jones, B.J. Sahakian, R. Levy, D.M. Warburton, J.A. Gray, Effects of acute subcutaneous nicotine on attention, information processing and shortterm memory in Alzheimer’s disease, Psychopharmacology (Berl) 108 (1992) 485–494. [37] L.E. Jubelt, R.S. Barr, D.C. Goff, T. Logvinenko, A.P. Weiss, A.E. Evins, Effects of transdermal nicotine on episodic memory in non-smokers with and without schizophrenia, Psychopharmacology (Berl) 199 (2008) 89–98. [38] M.C. Kelton, H.J. Kahn, C.L. Conrath, P.A. Newhouse, The effects of nicotine on Parkinson’s disease, Brain Cogn. 43 (2000) 274–282. [39] D.J. Kim, H.P. Lee, M.S. Kim, Y.J. Park, H.J. Go, K.S. Kim, S.P. Lee, J.H. Chae, C.T. Lee, The effect of total sleep deprivation on cognitive functions in normal adult male subjects, Int. J. Neurosci. 109 (2001) 127–137. [40] E.Y. Kim, G.S. Mahmoud, L.M. Grover, REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus, Neurosci. Lett. 388 (2005) 163–167. [41] E.D. Levin, M. Castonguay, G.D. Ellison, Effects of the nicotinic receptor blocker mecamylamine on radial-arm maze performance in rats, Behav. Neural Biol. 48 (1987) 206–212. [42] E.D. Levin, S.J. Briggs, N.C. Christopher, J.E. Rose, Chronic nicotinic stimulation and blockade effects on working memory, Behav. Pharmacol. 4 (1993) 179–182. [43] E.D. Levin, N.C. Christopher, S.J. Briggs, Chronic nicotinic agonist and antagonist effects on T-maze alternation, Physiol. Behav. 61 (1997) 863–866. [44] E.D. Levin, C.K. Conners, D. Silva, W. Canu, J. March, Effects of chronic nicotine and methylphenidate in adults with attention deficit/hyperactivity disorder, Exp. Clin. Psychopharmacol. 9 (2001) 83–90. [45] J. Le Houezec, P. Jacob 3rd, N.L. Benowitz, A clinical pharmacological study of subcutaneous nicotine, Eur J Clin Pharmacol. 44 (1993) 225–230. [46] R.B. Machado, D.C. Hipolide, A.A. Benedito-Silva, S. Tufik, Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery, Brain Res. 1004 (2004) 45–51. [47] H.D. Mansvelder, D.S. McGehee, Long-term potentiation of excitatory inputs to brain reward areas by nicotine, Neuron 27 (2000) 349–357. [48] L. Marshall, J. Born, The contribution of sleep to hippocampus-dependent memory consolidation, Trends Cogn. Sci. 11 (2007) 442–450. [49] C.M. McDermott, G.J. LaHoste, C. Chen, A. Musto, N.G. Bazan, J.C. Magee, Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons, J. Neurosci. 23 (2003) 9687–9695. [50] C.M. McDermott, M.N. Hardy, N.G. Bazan, J.C. Magee, Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus, J. Physiol. 570 (2006) 553–565. [51] M.A. Mograss, F. Guillem, V. Brazzini-Poisson, R. Godbout, The effects of total sleep deprivation on recognition memory processes: a study of event-related potential, Neurobiol. Learn. Mem. 91 (2009) 343–352. [52] S. Palchykova, R. Winsky-Sommerer, P. Meerlo, R. Durr, I. Tobler, Sleep deprivation impairs object recognition in mice, Neurobiol. Learn. Mem. 85 (2006) 263–271. [53] S. Park, C. Knopick, S. McGurk, H.Y. Meltzer, Nicotine impairs spatial working memory while leaving spatial attention intact, Neuropsychopharmacology 22 (2000) 200–209. [54] C.R. Park, A.M. Campbell, D.M. Diamond, Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats, Biol. Psychiatry 50 (2001) 994–1004.
31
[55] A.C. Parrott, G. Winder, Nicotine chewing gum (2 mg, 4 mg) and cigarette smoking: comparative effects upon vigilance and heart rate, Psychopharmacology (Berl) 97 (1989) 257–261. [56] P. Philip, J. Taillard, D. Leger, K. Diefenbach, T. Akerstedt, B. Bioulac, C. Guilleminault, Work and rest sleep schedules of 227 European truck drivers, Sleep Med. 3 (2002) 507–511. [57] C. Pierard, P. Liscia, F. Chauveau, M. Coutan, M. Corio, A. Krazem, D. Beracochea, Differential effects of total sleep deprivation on contextual and spatial memory: modulatory effects of modafinil, Pharmacol. Biochem. Behav. 97 (2011) 399–405. [58] D.V. Poltavski, T. Petros, Effects of transdermal nicotine on attention in adult non-smokers with and without attentional deficits, Physiol. Behav. 87 (2006) 614–624. [59] D.J. Polzella, Effects of sleep deprivation on short-term recognition memory, J. Exp. Psychol. Hum. Learn. 104 (1975) 194–200. [60] W.S. Poston, J.E. Taylor, K.M. Hoffman, A.L. Peterson, H.A. Lando, S. Shelton, C.K. Haddock, Smoking and deployment: perspectives of junior-enlisted U.S. Air Force and U.S. Army personnel and their supervisors, Mil. Med. 173 (2008) 441–447. [61] A.S. Potter, P.A. Newhouse, Acute nicotine improves cognitive deficits in young adults with attention-deficit/hyperactivity disorder, Pharmacol. Biochem. Behav. 88 (2008) 407–417. [62] N. Quigley, J.F. Green, D. Morgan, C. Idzikowski, D.J. King, The effect of sleep deprivation on memory and psychomotor function in healthy volunteers, Hum. Psychopharmacol. 15 (2000) 171–177. [63] P. Ravassard, B. Pachoud, J.C. Comte, C. Mejia-Perez, C. Scote-Blachon, N. Gay, B. Claustrat, M. Touret, P.H. Luppi, P.A. Salin, 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 32 (2009) 227–240. [64] D.N. Ruskin, K.E. Dunn, I. Billiot, N.G. Bazan, G.J. LaHoste, Eliminating the adrenal stress response does not affect sleep deprivation-induced acquisition deficits in the water maze, Life Sci. 78 (2006) 2833–2838. [65] S. Sawada, C. Yamamoto, T. Ohno-Shosaku, Long-term potentiation and depression in the dentate gyrus, and effects of nicotine, Neurosci. Res. 20 (1994) 323–329. [66] C.T. Smith, J.M. Conway, G.M. Rose, Brief paradoxical sleep deprivation impairs reference, but not working, memory in the radial arm maze task, Neurobiol. Learn. Mem. 69 (1998) 211–217. [67] R.C. Smith, A. Singh, M. Infante, A. Khandat, A. Kloos, Effects of cigarette smoking and nicotine nasal spray on psychiatric symptoms and cognition in schizophrenia, Neuropsychopharmacology 27 (2002) 479–497. [68] C.A. Sorenson, L.A. Raskin, Y. Suh, The effects of prenatal nicotine on radial-arm maze performance in rats, Pharmacol. Biochem. Behav. 40 (1991) 991–993. [69] M. Srivareerat, T.T. Tran, K.H. Alzoubi, K.A. Alkadhi, Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer’s disease, Biol. Psychiatry 65 (2009) 918–926. [70] M. Srivareerat, T.T. Tran, S. Salim, A.M. Aleisa, K.A. Alkadhi, Chronic nicotine restores normal Abeta levels and prevents short-term memory and E-LTP impairment in Abeta rat model of Alzheimer’s disease, Neurobiol. Aging 32 (2011) 834–844. [71] G.E. Swan, C.N. Lessov-Schlaggar, The effects of tobacco smoke and nicotine on cognition and the brain, Neuropsychol. Rev. 17 (2007) 259–273. [72] Y.P. Tang, E. Shimizu, G.R. Dube, C. Rampon, G.A. Kerchner, M. Zhuo, G. Liu, J.Z. Tsien, Genetic enhancement of learning and memory in mice, Nature 401 (1999) 63–69. [73] Y.P. Tang, H. Wang, R. Feng, M. Kyin, J.Z. Tsien, Differential effects of enrichment on learning and memory function in NR2B transgenic mice, Neuropharmacology 41 (2001) 779–790. [74] J.L. Tartar, C.P. Ward, J.T. McKenna, M. Thakkar, E. Arrigoni, R.W. McCarley, R.E. Brown, R.E. Strecker, Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation, Eur. J. Neurosci. 23 (2006) 2739–2748. [75] P.A. Tiba, M.G. Oliveira, V.C. Rossi, S. Tufik, D. Suchecki, Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments, Sleep 31 (2008) 505–515. [76] A. Toledano, M.I. Alvarez, A. Toledano-Diaz, Diversity and variability of the effects of nicotine on different cortical regions of the brain – therapeutic and toxicological implications, Cent. Nerv. Syst. Agents Med. Chem. 10 (2011) 180–206. [77] T.H. Turner, S.P. Drummond, J.S. Salamat, G.G. Brown, Effects of 42 hr of total sleep deprivation on component processes of verbal working memory, Neuropsychology 21 (2007) 787–795. [78] K. Wesnes, D.M. Warburton, Effects of scopolamine and nicotine on human rapid information processing performance, Psychopharmacology (Berl) 82 (1984) 147–150. [79] H.K. White, E.D. Levin, Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer’s disease, Psychopharmacology (Berl) 143 (1999) 158–165. [80] Y. Yamazaki, Y. Jia, R. Niu, K. Sumikawa, Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus, Eur. J. Neurosci. 23 (2006) 1819–1828. [81] B.D. Youngblood, J. Zhou, G.N. Smagin, D.H. Ryan, R.B. Harris, Sleep deprivation by the “flower pot” technique and spatial reference memory, Physiol. Behav. 61 (1997) 249–256.
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Post-learning REM sleep deprivation impairs long-term memory: Reversal by acute nicotine treatment A.M. Aleisa a , K.H. Alzoubi b , K.A. Alkadhi c,∗ a b c
Department of Pharmacology, College of Pharmacy, King Saud University, Riyadh, Saudi Arabia Department of Clinical Pharmacy, Faculty of Pharmacy, Jordan University of Science and Technology, Irbid, Jordan Department of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, Houston, TX 77204-5037, United States
a r t i c l e
i n f o
Article history: Received 3 February 2011 Received in revised form 28 April 2011 Accepted 13 May 2011 Keywords: Nicotine Sleep deprivation Post-learning Memory Hippocampus Maze
a b s t r a c t Rapid eye movement sleep deprivation (REM-SD) is associated with spatial learning and memory impairment. During REM-SD, an increase in nicotine consumption among habitual smokers and initiation of tobacco use by non-smokers have been reported. We have shown recently that nicotine treatment prevented learning and memory impairments associated with REM-SD. We now report the interactive effects of post-learning REM-SD and/or nicotine. The animals were first trained on the radial arm water maze (RAWM) task, then they were REM-sleep deprived using the modified multiple platform paradigm for 24 h. During REM-SD period, the rats were injected with saline or nicotine (1 mg/kg s.c. every 12 h: a total of 3 injections). The animals were tested for long-term memory in the RAWM at the end of the REMSD period. The 24 h post-learning REM-SD significantly impaired long-term memory. However, nicotine treatment reversed the post-learning REM-SD-induced impairment of long-term memory. On the other hand, post-learning treatment of normal rats with nicotine for 24 h enhanced long-term memory. These results indicate that post-learning acute nicotine treatment prevented the deleterious effect of REM-SD on cognitive abilities. © 2011 Elsevier Ireland Ltd. All rights reserved.
Rapid eye movement (REM) sleep, has an essential role in learning and memory formation in the hippocampus [48]. This has been studied in both humans and experimental animals using REM-sleep-deprivation (REM-SD) as a model [81,62,30,52,3–5]. Previous studies have shown that REM-SD impairs hippocampusdependent learning and memory [81,30,3–5,66,49,74]. We have recently reported that the negative effects of REM-SD may be related to alteration in the levels of important signaling molecules involved in memory and synaptic plasticity [4,5]. Increased frequency of nicotine consumption has been reported in REM-sleep-deprived smokers [56,31]. Nicotine is also known to alleviate impairment of memory associated with psychosocial stress [1,2,12], aging [17], hypothyroidism [8,9,13], Alzheimer’s disease [36,79,69,70], Parkinson’s disease [38], schizophrenia [67,32,37], and attention deficit/hyperactivity disorder (ADHD) [58,61]. Additionally, nicotine facilitates the induction of LTP, the cellular correlates for memory, in rat hippocampal slices [26,33] and induces long lasting potentiation in the mouse dentate gyrus (DG) region of the hippocampus [65]. Furthermore, nicotine treatment attenuates impairment of hippocampal LTP caused by chronic psychosocial stress [1], hypothyroidism [9] and aging [25]. Therefore, the reported increase in nicotine use among smokers and
∗ Corresponding author. Tel.: +1 713 743 1212; fax: +1 713 743 1229. E-mail address: [email protected] (K.A. Alkadhi). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.05.025
the initiation of smoking among non-smokers during REM-SD [56,31,60] could be a form of self-medication to correct the impairment of cognition and synaptic plasticity. We have recently reported that acute nicotine treatment prevented REM-SD induced impairment of short-term memory and synaptic plasticity of hippocampal CA1 [3]. In the present communication, we report the effect of post-learning REM-SD and/or acute nicotine treatment on long-term memory. Nicotine is a nAChRs agonist with beneficial effects on cognition, mediated mainly through activation of ␣7nAChRs (e.g., see [20] for review). Adult male Wistar rats (200–250 g), housed 6 per cage with free access to food and water, were subjected to a 12 h light/dark (lights on at 7:00 am) cycle at 25 ◦ C. All procedures involving animals were carried out in accordance with the National Research Council’s Guide for the Care and Use of Laboratory Animals and on approval of the University of Houston Institutional Animal Care and Use Committee. All behavioral and electrophysiological experiments were started at 9 am, and were terminated no later than 5 pm. There were four treatment groups in this study: postlearning control, post-learning REM-SD, post-learning nicotine, and post-learning nicotine plus post-learning REM-SD (post-learning Nic/REM-SD). Post-learning nicotine and post-learning Nic/REMSD groups were treated with nicotine (Sigma, St. Louis, MO) during REM-SD only (1 mg/kg/12 h s.c.: a total of 3 injections during the 24 h of REM-SD). This dose is known to produce blood nicotine levels similar to those of chronic smokers [45,15], and was previously
A.M. Aleisa et al. / Neuroscience Letters 499 (2011) 28–31
used in several studies showing neuroprotective properties of the drug in animals (e.g., [1,9,69,3]). Both the post-learning REM-SD and post-learning Nic/REM-SD groups were sleep deprived for 24 h using columns-in-water (modified multiple platform) model as described [3–5,50]. Animals in each group were REM sleep-deprived together to eliminate isolation stress. Immediately after the end of the training (learning) phase, animals were placed on platforms (20 platforms; 20 cm high and 5 cm diameter, 7 cm apart edge-to-edge) in an aquarium where water and food were accessible to animals. The water level in the aquarium (24 ± 1 ◦ C) was about 2 cm below the edge of the platform. This method has been reported to interfere with total sleep, but it mainly eliminates REM sleep [28,46]. Loss of muscle tone during REM sleep caused the rat’s snout to dip into the water, or occasionally, the rat, to fall into the water, and awaken. Immediately after REM-SD, animals were tested for long-term memory. The RAWM consists of a black circular water tank with 6 Vshaped stainless steel structures arranged to form a swimming field of an open central area and 6 arms. The RAWM design [22,54] resembles a radial arm maze inserted into a Morris maze (a circular tank filled with water). The water temperature was maintained at 24 ± 1 ◦ C. The goal arm was one that contained a black removable platform submerged 1 cm below the water level. The RAWM task was conducted as reported [3,5]. Briefly, animals were first trained on the RAWM task; beginning from a start arm (any arm other than the goal arm); the rat must find the submerged platform by swimming to the end of the goal arm. Each rat was allowed twelve consecutive training trials (learning phase: 2 blocks of 6 trials interspersed by a 5-min rest period). Thereafter, post-learning REM-SD and post-learning Nic/REM-SD groups were sleep deprived for 24 h, followed by a long-term memory test (24 h after trial # 12). Rats were allowed 1 min per RAWM trial to find the submerged platform. A trial ended when the rat located the submerged platform, where it was allowed a 15 s stay on the platform before removal to start the next trial in a different start arm. If the rat did not find the submerged platform in the goal arm within 1 min, the experimenter would guide the rat to the goal arm and allow it to stay on the platform for 15 s before removal to begin the next trial. A correct selection occurred when the rat swam into the goal arm, while error was registered each time the rat entered into an arm other than the goal arm. All experiments were done in a dimly lit room with visual cues on the walls. Data are expressed as means ± SEM. All statistics were carried out using two-way ANOVA followed by Tukey posttest. P ≤ 0.05 was considered statistically significant. Before any treatment, the four groups of naïve rats were first trained on the RAWM to finish the 12 learning trials where each rat in each group successfully learned to find the hidden platform (Fig. 1). Memory test after 24 h REM-SD, showed markedly impaired long-term memory. This is indicated by the observation that 24 h post-learning REM-SD group (Fig. 2) made significantly (P < 0.01) more errors in long-term memory trial to locate the hidden platform than the post-learning control group. Acute nicotine treatment, clearly, prevented REM-SD-induced impairment of long-term memory as tested in the RAWM. In the long-term memory test, rats in the post-learning Nic/REM-SD group made significantly (P < 0.001) fewer errors to locate the hidden platform than the untreated 24 h post-learning REM-SD group (Fig. 2). Interestingly, post-learning rats treated with nicotine alone made significantly (P < 0.05) fewer errors compared to the untreated postlearning control rats (Fig. 2). The major finding of this study is that acute nicotine treatment during post-learning REM-SD prevents impairment of long-term memory. Additionally, acute nicotine enhanced long-term memory in post-learning control animals. Sleep loss impairs learning and memory in human [59,77,51] and animal studies [81,30,3,5,66,49]. In addition, REM-SD blocks hippocampal LTP [3–5,56,50,40,34]. We
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Fig. 1. Effect of acute nicotine treatment (1 mg/kg/12 h s.c.: a total of 3 injections during the 24 h of SD). Without sleep deprivation, all groups performed similarly during learning phase in the RAWM. After post-learning 24 h sleep deprivation, the REM-SD rats committed more errors in finding the hidden platform than control rats. Interestingly, acute nicotine treatment significantly (P < 0.05) improved longterm memory in control rats that have gone through RAWM training. *Significant difference from control, Nic and REM-SD/Nic group (P < 0.01). #Significant difference from control group (P < 0.05). Data are presented as mean ± SEM (N = 8–10).
have previously, shown that REM-SD impairs short-term memory [3,5]. In parallel, the present work demonstrates that, when induced after learning, REM-SD impairs hippocampus-dependent long-term memory. When adrenal stress response was eliminated by corticosterone synthesis inhibitor, metyrapone [75] or by adrenalectomy [64], the negative effect of REM-SD on learning and memory persisted suggesting that this effect was not due to the release of stress hormones. Additionally, the modified multiple platform method eliminates immobilization and isolation stresses. Moreover, when wide columns that allowed rats to sleep, were used in the same aquarium, animals did not show impairment of spatial learning and memory [4,5]. Furthermore, it is possible that the anxiety and stress resulting from possible tumbling into water may have contributed to the memory deficits. However, we propose that REM-SD may
Fig. 2. Effect of acute nicotine treatment on sleep deprivation-impaired long-term memory. This graph summarizes the average number of errors made by each of the four groups in the long-term memory test. Each point is the mean ± SEM of 8–10 rats. *Significant difference from all other groups (P < 0.01) and #significant difference from all other groups (P < 0.05).
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be the major factor that causes long-term memory impairment. We have shown that stress affects the hippocampus in a considerably different manner than REM-SD; for example, whereas, REM-SD impairs learning [3,6], exposure to psychosocial stress for six weeks does not influence this function [1]. Findings of the current and previous studies [3–5] showing that REM-SD impairs hippocampus-dependent learning and memory, are in agreement with the results obtained by studies concerning the effect of total sleep deprivation on cognitive functions [30,39,27,19,57]. In fact, it should be noted that sleep deprivation methods, including the multiple platform method, induce deprivation of both sleep phases to a varying degree [46]. The multiple platform method has been shown to decrease slow-wave sleep and abolishes REM sleep [28,46]. Therefore, results of the current study and similar previous studies mainly represent REM-SD [3–5]. Reports on the effect of nicotine on memory in normal subjects are variable. While some investigators show enhancement of normal memory as a result of nicotine treatment ([78,41–43,14,16,44,71] for review), others report no effect [1,24,55,9], or even memory impairment [68,53]. The inconsistency in the reported effect of nicotine on memory could be related to the nicotine dosing level, duration of treatment, route of administration and experimental procedures used. In this study, acute nicotine enhanced long-term memory in post-learning control animals. Nicotine-induced enhancement of long-term memory in control animals may be related to the fact that these animals are not normal controls; they have gone through learning trials, which may suggest that nicotine strengths memory following learning. Results of the current study show that acute nicotine prevents post-learning REM-SD-induced long-term memory impairment. Similarly, we have recently reported that nicotine prevented the effects of REM-SD on learning and memory, when REM-SD and nicotine are administered before learning. In agreement, previous studies have shown beneficial effects for nicotine on memory impairment associated with several brain disorders including chronic mental stress [1,12], Alzheimer’s disease [69,70] and hypothyroidism [8,10]. The neuroprotective effects of nicotine may be attributed to a number of possible mechanisms. Nicotine activates presynaptic nAChR (mainly ␣7nAChR), which increases the influx of calcium, and, thus, enhances glutamate release from presynaptic nerve terminals at the pyramidal cells in area CA1 of the hippocampus [29,35]. Nicotine therefore, increases the probability of coincidence between presynaptic release and postsynaptic depolarization, and therefore raises the probability of LTP induction [35,47]. In addition, highly localized calcium influx through nAChR activates protein kinases and phosphatases cascades, which modulate neurotransmitter release. Other studies show that in cultured CA1 neurons, nicotine treatment desensitizes ␣7nAChR on the GABAergic interneurons resulting in reduced release of GABA from these interneurons, thus indirectly increasing excitability of the pyramidal cell [7]. This, in turn, facilitates LTP by decreasing its threshold of induction [26]. It is well known that glutamatergic NMDA receptor plays a crucial role in spatial memory (e.g., [73]). Sleep loss reduces hippocampal NMDA receptor expression [50,73,72], lowers excitatory postsynaptic currents [18] and decreases levels of NR1 subunit of NMDA receptor in area CA1 [63]. In contrast, nicotine treatment enhances the expression of hippocampal NMDA receptor subunit 2A and 2B (NR2A, NR2B) [21,11], enhances the NMDA receptormediated currents and increases tyrosine phosphorylation of NR2B subunit [80]. Therefore, countering the negative effect of sleep loss on NMDA receptors could be another mechanism of the observed nicotine action. There are many implications of the interactive effect of nicotine and REM-SD. Nicotine affect various brain regions, especially the
cortex and the hippocampus, where it enhances cognitive functions in these regions (reviewed in [76]). In addition, nicotine and other nAChRs agonists have been reported to ameliorate symptoms of schizophrenia [23] and other mental disorders [20]. These findings support the results of the current study. Collectively, the findings of this study indicate that, when both instituted after learning, acute nicotine treatment antagonizes the deleterious effect of REM-SD on long-term memory.
References [1] A.M. Aleisa, K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Nicotine blocks stressinduced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region, Int. J. Neuropsychopharmacol. 9 (2006) 417–426. [2] A.M. Aleisa, K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Chronic psychosocial stressinduced impairment of hippocampal LTP: possible role of BDNF, Neurobiol. Dis. 22 (2006) 453–462. [3] A.M. Aleisa, G. Helal, I.A. Alhaider, K.H. Alzoubi, M. Srivareerat, T.T. Tran, S.S. Al-Rejaie, K.A. Alkadhi, Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat, Hippocampus (2011), doi:10.1002/hipo.20806. [4] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.A. Alkadhi, Caffeine prevents sleep lossinduced deficits in long-term potentiation and related signaling molecules in the dentate gyrus, Eur. J. Neurosci. 31 (2010) 1368–1376. [5] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.H. Alzoubi, K.A. Alkadhi, Chronic caffeine treatment prevents sleep deprivation-induced impairment of cognitive function and synaptic plasticity, Sleep 33 (2010) 437–444. [6] I.A. Alhaider, A.M. Aleisa, T.T. Tran, K.A. Alkadhi, Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine, Mol. Cell. Neurosci. 46 (4) (2011) 742–751. [7] M. Alkondon, M.F. Braga, E.F. Pereira, A. Maelicke, Albuquerque EX alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus, Eur. J. Pharmacol. 393 (2000) 59–67. [8] K.H. Alzoubi, N.Z. Gerges, K.A. Alkadhi, Levothyroxin restores hypothyroidisminduced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies, Exp. Neurol. 195 (2005) 330–341. [9] K.H. Alzoubi, A.M. Aleisa, N.Z. Gerges, K.A. Alkadhi, Nicotine reverses adultonset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies, J. Neurosci. Res. 84 (2006) 944–953. [10] K.H. Alzoubi, A.M. Aleisa, K.A. Alkadhi, Molecular studies on the protective effect of nicotine in adult-onset hypothyroidism-induced impairment of long-term potentiation, Hippocampus 16 (2006) 861–874. [11] K.H. Alzoubi, A.M. Aleisa, K.A. Alkadhi, Adult-onset hypothyroidism facilitates and enhances LTD: reversal by chronic nicotine treatment, Neurobiol. Dis. 26 (2007) 264–272. [12] K.H. Alzoubi, K.K. Abdul-Razzak, O.F. Khabour, G.M. Al-Tuweiq, M.A. Alzubi, K.A. Alkadhi, Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats, Behav. Brain Res. 204 (2009) 117–123. [13] K.H. Alzoubi, N.Z. Gerges, A.M. Aleisa, K.A. Alkadhi, Levothyroxin restores hypothyroidism-induced impairment of hippocampus-dependent learning and memory: behavioral, electrophysiological, and molecular studies, Hippocampus 19 (2009) 66–78. [14] A. Bancroft, E.D. Levin, Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory, Neuropharmacology 39 (2000) 2770–2778. [15] N.L. Benowitz, P. Jacob 3rd, C. Denaro, R. Jenkins, Stable isotope studies of nicotine kinetics and bioavailability, Clin Pharmacol Ther. 49 (1991) 270–277. [16] J.H. Bettany, E.D. Levin, Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze, Pharmacol. Biochem. Behav. 70 (2001) 467–474. [17] C. Carrasco, P. Vicens, R. Redolat, Neuroprotective effects of behavioural training and nicotine on age-related deficits in spatial learning, Behav. Pharmacol. 17 (2006) 441–452. [18] C. Chen, M. Hardy, J. Zhang, G.J. LaHoste, N.G. Bazan, Altered NMDA receptor trafficking contributes to sleep deprivation-induced hippocampal synaptic and cognitive impairments, Biochem. Biophys. Res. Commun. 340 (2006) 435–440. [19] A. Chowdhury, R. Chandra, S.K. Jha, Total sleep deprivation impairs the encoding of trace-conditioned memory in the rat, Neurobiol. Learn. Mem. 95 (2011) 355–360. [20] S.L. Cincotta, M.S. Yorek, T.M. Moschak, S.R. Lewis, J.S. Rodefer, Selective nicotinic acetylcholine receptor agonists: potential therapies for neuropsychiatric disorders with cognitive dysfunction, Curr. Opin. Investig. Drugs 9 (2008) 47–56. [21] N. Delibas, D.K. Doguc, R. Sutcu, E. Eroglu, O. Gokalp, Effect of nicotine on hippocampal nicotinic acetylcholine alpha7 receptor and NMDA receptor subunits 2A and 2B expression in young and old rats, Int. J. Neurosci. 115 (2005) 1151–1163. [22] D.M. Diamond, C.R. Park, K.L. Heman, G.M. Rose, Exposing rats to a predator impairs spatial working memory in the radial arm water maze, Hippocampus 9 (1999) 542–552.
A.M. Aleisa et al. / Neuroscience Letters 499 (2011) 28–31 [23] M.S. D’Souza, A. Markou, Schizophrenia and tobacco smoking comorbidity: nAChR agonists in the treatment of schizophrenia-associated cognitive deficits, Neuropharmacology (2011), doi:10.1016/j.neuropharm.2011.01044. [24] M.P. Dunne, D. Macdonald, L.R. Hartley, The effects of nicotine upon memory and problem solving performance, Physiol. Behav. 37 (1986) 849–854. [25] S. Fujii, K. Sumikawa, Acute and chronic nicotine exposure reverse age-related declines in the induction of long-term potentiation in the rat hippocampus, Brain Res. 894 (2001) 347–353. [26] S. Fujii, Z. Ji, N. Morita, K. Sumikawa, Acute and chronic nicotine exposure differentially facilitate the induction of LTP, Brain Res. 846 (1999) 137–143. [27] A. Gosselin, J. De Koninck, K.B. Campbell, Total sleep deprivation and novelty processing: implications for frontal lobe functioning, Clin. Neurophysiol. 116 (2005) 211–222. [28] S. Grahnstedt, R. Ursin, Platform sleep deprivation affects deep slow wave sleep in addition to REM sleep, Behav. Brain Res. 18 (1985) 233–239. [29] R. Gray, A.S. Rajan, K.A. Radcliffe, M. Yakehiro, J.A. Dani, Hippocampal synaptic transmission enhanced by low concentrations of nicotine, Nature 383 (1996) 713–716. [30] Z. Guan, X. Peng, J. Fang, Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus, Brain Res. 1018 (2004) 38–47. [31] A. Hamidovic, H. de Wit, Sleep deprivation increases cigarette smoking, Pharmacol. Biochem. Behav. 93 (2009) 263–269. [32] J.G. Harris, S. Kongs, D. Allensworth, L. Martin, J. Tregellas, B. Sullivan, G. Zerbe, R. Freedman, Effects of nicotine on cognitive deficits in schizophrenia, Neuropsychopharmacology 29 (2004) 1378–1385. [33] J. He, C.Y. Deng, X.N. Zhu, J.P. Yu, R.Z. Chen, Different synaptic mechanisms of long-term potentiation induced by nicotine and tetanic stimulation in hippocampal CA1 region of rats, Acta Pharmacol. Sin. 24 (2003) 398–402. [34] A. Ishikawa, Y. Kanayama, H. Matsumura, H. Tsuchimochi, Y. Ishida, S. Nakamura, Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus, Eur. J. Neurosci. 24 (2006) 243–248. [35] D. Ji, R. Lape, J.A. Dani, Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity, Neuron 31 (2001) 131–141. [36] G.M. Jones, B.J. Sahakian, R. Levy, D.M. Warburton, J.A. Gray, Effects of acute subcutaneous nicotine on attention, information processing and shortterm memory in Alzheimer’s disease, Psychopharmacology (Berl) 108 (1992) 485–494. [37] L.E. Jubelt, R.S. Barr, D.C. Goff, T. Logvinenko, A.P. Weiss, A.E. Evins, Effects of transdermal nicotine on episodic memory in non-smokers with and without schizophrenia, Psychopharmacology (Berl) 199 (2008) 89–98. [38] M.C. Kelton, H.J. Kahn, C.L. Conrath, P.A. Newhouse, The effects of nicotine on Parkinson’s disease, Brain Cogn. 43 (2000) 274–282. [39] D.J. Kim, H.P. Lee, M.S. Kim, Y.J. Park, H.J. Go, K.S. Kim, S.P. Lee, J.H. Chae, C.T. Lee, The effect of total sleep deprivation on cognitive functions in normal adult male subjects, Int. J. Neurosci. 109 (2001) 127–137. [40] E.Y. Kim, G.S. Mahmoud, L.M. Grover, REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus, Neurosci. Lett. 388 (2005) 163–167. [41] E.D. Levin, M. Castonguay, G.D. Ellison, Effects of the nicotinic receptor blocker mecamylamine on radial-arm maze performance in rats, Behav. Neural Biol. 48 (1987) 206–212. [42] E.D. Levin, S.J. Briggs, N.C. Christopher, J.E. Rose, Chronic nicotinic stimulation and blockade effects on working memory, Behav. Pharmacol. 4 (1993) 179–182. [43] E.D. Levin, N.C. Christopher, S.J. Briggs, Chronic nicotinic agonist and antagonist effects on T-maze alternation, Physiol. Behav. 61 (1997) 863–866. [44] E.D. Levin, C.K. Conners, D. Silva, W. Canu, J. March, Effects of chronic nicotine and methylphenidate in adults with attention deficit/hyperactivity disorder, Exp. Clin. Psychopharmacol. 9 (2001) 83–90. [45] J. Le Houezec, P. Jacob 3rd, N.L. Benowitz, A clinical pharmacological study of subcutaneous nicotine, Eur J Clin Pharmacol. 44 (1993) 225–230. [46] R.B. Machado, D.C. Hipolide, A.A. Benedito-Silva, S. Tufik, Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery, Brain Res. 1004 (2004) 45–51. [47] H.D. Mansvelder, D.S. McGehee, Long-term potentiation of excitatory inputs to brain reward areas by nicotine, Neuron 27 (2000) 349–357. [48] L. Marshall, J. Born, The contribution of sleep to hippocampus-dependent memory consolidation, Trends Cogn. Sci. 11 (2007) 442–450. [49] C.M. McDermott, G.J. LaHoste, C. Chen, A. Musto, N.G. Bazan, J.C. Magee, Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons, J. Neurosci. 23 (2003) 9687–9695. [50] C.M. McDermott, M.N. Hardy, N.G. Bazan, J.C. Magee, Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus, J. Physiol. 570 (2006) 553–565. [51] M.A. Mograss, F. Guillem, V. Brazzini-Poisson, R. Godbout, The effects of total sleep deprivation on recognition memory processes: a study of event-related potential, Neurobiol. Learn. Mem. 91 (2009) 343–352. [52] S. Palchykova, R. Winsky-Sommerer, P. Meerlo, R. Durr, I. Tobler, Sleep deprivation impairs object recognition in mice, Neurobiol. Learn. Mem. 85 (2006) 263–271. [53] S. Park, C. Knopick, S. McGurk, H.Y. Meltzer, Nicotine impairs spatial working memory while leaving spatial attention intact, Neuropsychopharmacology 22 (2000) 200–209. [54] C.R. Park, A.M. Campbell, D.M. Diamond, Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats, Biol. Psychiatry 50 (2001) 994–1004.
31
[55] A.C. Parrott, G. Winder, Nicotine chewing gum (2 mg, 4 mg) and cigarette smoking: comparative effects upon vigilance and heart rate, Psychopharmacology (Berl) 97 (1989) 257–261. [56] P. Philip, J. Taillard, D. Leger, K. Diefenbach, T. Akerstedt, B. Bioulac, C. Guilleminault, Work and rest sleep schedules of 227 European truck drivers, Sleep Med. 3 (2002) 507–511. [57] C. Pierard, P. Liscia, F. Chauveau, M. Coutan, M. Corio, A. Krazem, D. Beracochea, Differential effects of total sleep deprivation on contextual and spatial memory: modulatory effects of modafinil, Pharmacol. Biochem. Behav. 97 (2011) 399–405. [58] D.V. Poltavski, T. Petros, Effects of transdermal nicotine on attention in adult non-smokers with and without attentional deficits, Physiol. Behav. 87 (2006) 614–624. [59] D.J. Polzella, Effects of sleep deprivation on short-term recognition memory, J. Exp. Psychol. Hum. Learn. 104 (1975) 194–200. [60] W.S. Poston, J.E. Taylor, K.M. Hoffman, A.L. Peterson, H.A. Lando, S. Shelton, C.K. Haddock, Smoking and deployment: perspectives of junior-enlisted U.S. Air Force and U.S. Army personnel and their supervisors, Mil. Med. 173 (2008) 441–447. [61] A.S. Potter, P.A. Newhouse, Acute nicotine improves cognitive deficits in young adults with attention-deficit/hyperactivity disorder, Pharmacol. Biochem. Behav. 88 (2008) 407–417. [62] N. Quigley, J.F. Green, D. Morgan, C. Idzikowski, D.J. King, The effect of sleep deprivation on memory and psychomotor function in healthy volunteers, Hum. Psychopharmacol. 15 (2000) 171–177. [63] P. Ravassard, B. Pachoud, J.C. Comte, C. Mejia-Perez, C. Scote-Blachon, N. Gay, B. Claustrat, M. Touret, P.H. Luppi, P.A. Salin, 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 32 (2009) 227–240. [64] D.N. Ruskin, K.E. Dunn, I. Billiot, N.G. Bazan, G.J. LaHoste, Eliminating the adrenal stress response does not affect sleep deprivation-induced acquisition deficits in the water maze, Life Sci. 78 (2006) 2833–2838. [65] S. Sawada, C. Yamamoto, T. Ohno-Shosaku, Long-term potentiation and depression in the dentate gyrus, and effects of nicotine, Neurosci. Res. 20 (1994) 323–329. [66] C.T. Smith, J.M. Conway, G.M. Rose, Brief paradoxical sleep deprivation impairs reference, but not working, memory in the radial arm maze task, Neurobiol. Learn. Mem. 69 (1998) 211–217. [67] R.C. Smith, A. Singh, M. Infante, A. Khandat, A. Kloos, Effects of cigarette smoking and nicotine nasal spray on psychiatric symptoms and cognition in schizophrenia, Neuropsychopharmacology 27 (2002) 479–497. [68] C.A. Sorenson, L.A. Raskin, Y. Suh, The effects of prenatal nicotine on radial-arm maze performance in rats, Pharmacol. Biochem. Behav. 40 (1991) 991–993. [69] M. Srivareerat, T.T. Tran, K.H. Alzoubi, K.A. Alkadhi, Chronic psychosocial stress exacerbates impairment of cognition and long-term potentiation in beta-amyloid rat model of Alzheimer’s disease, Biol. Psychiatry 65 (2009) 918–926. [70] M. Srivareerat, T.T. Tran, S. Salim, A.M. Aleisa, K.A. Alkadhi, Chronic nicotine restores normal Abeta levels and prevents short-term memory and E-LTP impairment in Abeta rat model of Alzheimer’s disease, Neurobiol. Aging 32 (2011) 834–844. [71] G.E. Swan, C.N. Lessov-Schlaggar, The effects of tobacco smoke and nicotine on cognition and the brain, Neuropsychol. Rev. 17 (2007) 259–273. [72] Y.P. Tang, E. Shimizu, G.R. Dube, C. Rampon, G.A. Kerchner, M. Zhuo, G. Liu, J.Z. Tsien, Genetic enhancement of learning and memory in mice, Nature 401 (1999) 63–69. [73] Y.P. Tang, H. Wang, R. Feng, M. Kyin, J.Z. Tsien, Differential effects of enrichment on learning and memory function in NR2B transgenic mice, Neuropharmacology 41 (2001) 779–790. [74] J.L. Tartar, C.P. Ward, J.T. McKenna, M. Thakkar, E. Arrigoni, R.W. McCarley, R.E. Brown, R.E. Strecker, Hippocampal synaptic plasticity and spatial learning are impaired in a rat model of sleep fragmentation, Eur. J. Neurosci. 23 (2006) 2739–2748. [75] P.A. Tiba, M.G. Oliveira, V.C. Rossi, S. Tufik, D. Suchecki, Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments, Sleep 31 (2008) 505–515. [76] A. Toledano, M.I. Alvarez, A. Toledano-Diaz, Diversity and variability of the effects of nicotine on different cortical regions of the brain – therapeutic and toxicological implications, Cent. Nerv. Syst. Agents Med. Chem. 10 (2011) 180–206. [77] T.H. Turner, S.P. Drummond, J.S. Salamat, G.G. Brown, Effects of 42 hr of total sleep deprivation on component processes of verbal working memory, Neuropsychology 21 (2007) 787–795. [78] K. Wesnes, D.M. Warburton, Effects of scopolamine and nicotine on human rapid information processing performance, Psychopharmacology (Berl) 82 (1984) 147–150. [79] H.K. White, E.D. Levin, Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer’s disease, Psychopharmacology (Berl) 143 (1999) 158–165. [80] Y. Yamazaki, Y. Jia, R. Niu, K. Sumikawa, Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus, Eur. J. Neurosci. 23 (2006) 1819–1828. [81] B.D. Youngblood, J. Zhou, G.N. Smagin, D.H. Ryan, R.B. Harris, Sleep deprivation by the “flower pot” technique and spatial reference memory, Physiol. Behav. 61 (1997) 249–256.