Abstract
Nicotinic acetylcholine receptors (nAChRs) modulate the neurobiological processes underlying hippocampal learning and memory. In addition, nicotine’s ability to desensitize and upregulate certain nAChRs may alter hippocampus-dependent memory processes. Numerous studies have examined the effects of nicotine on hippocampus-dependent learning, as well as the roles of low- and high-affinity nAChRs in mediating nicotine’s effects on hippocampus-dependent learning and memory. These studies suggested that while acute nicotine generally acts as a cognitive enhancer for hippocampus-dependent learning, withdrawal from chronic nicotine results in deficits in hippocampus-dependent memory. Furthermore, these studies demonstrated that low- and high-affinity nAChRs functionally differ in their involvement in nicotine’s effects on hippocampus-dependent learning. In the present chapter, we reviewed studies using systemic or local injections of acute or chronic nicotine, nAChR subunit agonists or antagonists; genetically modified mice; and molecular biological techniques to characterize the effects of nicotine on hippocampus-dependent learning.
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References
Abdulla FA, Bradbury E, Calaminici MR et al (1996) Relationship between up-regulation of nicotine binding sites in rat brain and delayed cognitive enhancement observed after chronic or acute nicotinic receptor stimulation. Psychopharmacology 124:323–331
Abel T, Nguyen PV (2008) Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Prog Brain Res 169:97–115
Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615–626
Abreu-Villaca Y, Seidler FJ, Qiao D, Tate CA, Cousins MM, Thillai I, Slotkin TA (2003) Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds. Neuropsychopharmacology 28:1935–1949
Addy N, Levin ED (2002) Nicotine interactions with haloperidol, clozapine and risperidone and working memory function in rats. Neuropsychopharmacology 27:534–541
Akers RF, Lovinger DM, Colley PA, Linden DJ, Routtenberg A (1986) Translocation of protein kinase C activity may mediate hippocampal long-term potentiation. Science 231:587–589
Alkondon M, Pereira EF, Albuquerque EX (1996) Mapping the location of functional nicotinic and gamma-aminobutyric acid A receptors on hippocampal neurons. J Pharmacol Exp Ther 279:1491–1506
Alkondon M, Braga MF, Pereira EF, Maelicke A, Albuquerque EX (2000) Alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus. Eur J Pharmacol 393:59–67
André JM, Gulick D, Portugal GS, Gould TJ (2008) Nicotine withdrawal disrupts both foreground and background contextual fear conditioning but not pre-pulse inhibition of the acoustic startle response in C57BL/6 mice. Behav Brain Res 190:174–181
Andre JM, Leach PT, Gould TJ (2011) Nicotine ameliorates NMDA receptor antagonist-induced deficits in contextual fear conditioning through highaffinity nicotinic acetylcholine receptors in the hippocampus. Neuropharmacology 60:617–625
Araujo DM, Lapchak PA, Collier B, Quirion R (1988) Characterization of N-[3H]methylcarbamylcholine binding sites and effect of Nmethylcarbamylcholine on acetylcholine release in rat brain. J Neurochem 51:292–299
Arthur D, Levin ED (2002) Chronic inhibition of alpha4beta2 nicotinic receptors in the ventral hippocampus of rats: impacts on memory and nicotine response. Psychopharmacology 160:140–145
Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602–609
Attaway CM, Compton DM, Turner MD (1999) The effects of nicotine on learning and memory: a neuropsychological assessment in young and senescent fischer 344 rats. Physiol Behav 67:421–431
Awh E, Jonides J (2001) Overlapping mechanisms of attention and spatial working memory. Trends Cogn Sci 5:119–126
Azzopardi E, Typlt M, Jenkins B, Schmid S (2013) Sensorimotor gating and spatial learning in a7-nicotinic receptor knockout mice. Genes Brain Behav 12:414–423
Bancroft A, Levin ED (2000) Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology 39:2770–2778
Barrantes GE, Westwick J, Wonnacott S (1994) Nicotinic acetylcholine receptors in primary cultures of hippocampal neurons: pharmacology and Ca++ permeability. Biochem Soc Trans 22:294S
Barrantes GE, Murphy CT, Westwick J, Wonnacott S (1995) Nicotine increases intracellular calcium in rat hippocampal neurons via voltage-gated calcium channels. Neurosci Lett 196:101–104
Benwell ME, Balfour DJK, Anderson JM (1988) Evidence that tobacco smoking increases the density of (-)-[3H]nicotine binding sites in human brain. J Neurochem 50:1243–1247
Berg DK, Conroy WG (2002) Nicotinic α7 receptors: synaptic options and downstream signaling in neurons. J Neurobiol 53:512–523
Bernabeu R, Bevilaqua L, Ardenghi P, Bromberg E, Schmitz P, Bianchin M et al (1997) Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc Natl Acad Sci USA 94:7041–7046
Bernal MC, Vicens P, Carrasco MC, Redolat R (1999) Effects of nicotine on spatial learning in C57BL mice. Behav Pharmacol 10:333–336
Bettany JH, Levin ED (2001) Ventral hippocampal alpha7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze. Pharmacol Biochem Behav 70:467–474
Bjorkblom B, Ostman N, Hongisto V et al (2005) Constitutively active cytoplasmic c-jun n-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 25:6350–6361
Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39
Bogoyevitch MA, Kobe B (2006) Uses for JNK: the many and varied substrates of the c-jun n-terminal kinases. Microbiol Mol Biol Rev 70:1061–1095
Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485–494
Bouton ME, Bolles RC (1979) Contextual control of the extinction of conditioned fear. Learn Motiv 10:445–466
Bouton ME, King DA (1983) Contextual control of the extinction of conditioned fear: tests for the associative value of the context. J Exp Psychol Anim Behav Process 9:248–265
Bouton ME, Westbrook RF, Corcoran KA, Maren S (2006) Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 60:352–360
Breese CR, Marks MJ, Logel J, Adams CE, Sullivan B, Collins AC et al (1997) Effect of smoking history on [3H]nicotine binding in human postmortem brain. J Pharmacol Exp Ther 282:7–13
Brody AL, Mukhin AG, Shulenberger S, Mamoun MS, Kozman M, Phuong J, Mandelkern MA (2013) Treatment for tobacco dependence: effect on brain nicotinic acetylcholine receptor density. Neuropsychopharmacology 38:1548–1556
Broide RS, Leslie FM (1999) The α7 nicotinic acetylcholine receptor in neuronal plasticity. Mol Neurobiol 20:1–16
Caldarone BJ, Duman CH, Picciotto MR (2000) Fear conditioning and latent inhibition in mice lacking the high affinity subclass of nicotinic acetylcholine receptors in the brain. Neuropharmacology 39:2779–2784
Castner SA, Smagin GN, Piser TM et al (2011) Immediate and sustained improvements in working memory after selective stimulation of α7 nicotinic acetylcholine receptors. Biol Psychiatry 69:12–18
Clarke PB, Reuben M (1996) Release of [3H]-noradrenaline from rat hippocampal synaptosomes by nicotine: Mediation by different nicotinic receptor subtypes from striatal [3H]-dopamine release. Br J Pharmacol 117:595–606
Collins AC, Romm E, Wehner JM (1990) Dissociation of the apparent relationship between nicotine tolerance and up-regulation of nicotinic receptors. Brain Res Bull 25:373–379
Corcoran KA, Desmond TJ, Frey KA, Maren S (2005) Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J Neurosci 25:8978–8987
Cordero-Erausquin M, Marubio LM, Klink R, Changeux JP (2000) Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol Sci 21:211–217
Dani JA, Heinemann S (1996) Molecular and cellular aspects of nicotine abuse. Neuron 16:905–908
Davis JA, Gould TJ (2006) The effects of DHBE and MLA on nicotine-induced enhancement of contextual fear conditioning in C57BL/6 mice. Psychopharmacology 184:345–352
Davis J, Gould T (2007) Beta2 subunit-containing nicotinic receptors mediate the enhancing effect of nicotine on trace cued fear conditioning in C57BL/6 mice. Psychopharmacology 190:343–352
Davis JA, Gould TJ (2009) Hippocampal nAChRs mediate nicotine withdrawal-related learning deficits. Eur Neuropsychopharmacol 19:551–561
Davis JA, James JR, Siegel SJ, Gould TJ (2005) Withdrawal from chronic nicotine administration impairs contextual fear conditioning in C57BL/6 mice. J Neurosci 25:8708–8713
Davis JA, Porter J, Gould TJ (2006) Nicotine enhances both foreground and background contextual fear conditioning. Neurosci Lett 394:202–205
Davis JA, Kenney JW, Gould TJ (2007) Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci 27:10870–10877
Decker MW, Brioni JD, Bannon AW, Arneric SP (1995) Diversity of neuronal nicotinic acetylcholine receptors: lessons from behavior and implications for CNS therapeutics. Life Sci 56:545–570
Dominguez del Toro E, Juiz JM, Peng X, Lindstrom J, Criado M (1994) Immunocytochemical localization of the alpha 7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J Comp Neurol 349:325–342
Elias GA, Gulick D, Wilkinson DS, Gould TJ (2010) Nicotine and extinction of fearconditioning. Neuroscience 165:1063–1073
English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103–19106
Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG et al (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21:7993–8003
Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19
Fanselow MS, Kim JJ, Yipp J, De Oca B (1994) Differential effects of the Nmethyl- D-aspartate antagonist DL-2-amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues. Behav Neurosci 108:235–240
Feiro O, Gould TJ (2005) The interactive effects of nicotinic and muscarinic cholinergic receptor inhibition on fear conditioning in young and aged C57BL/6 mice. Pharmacol Biochem Behav 80:251–262
Freund RK, Jungschaffer DA, Collins AC, Wehner JM (1988) Evidence for modulation of GABAergic neurotransmission by nicotine. Brain Res 453:215–220
Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57–65
Frey U, Frey S, Schollmeier F, Krug M (1996) Influence of actinomycin D, a RNA synthesis inhibitor, on long-term potentiation in rat hippocampal neurons in vivo and in vitro. J Physiol 490:703–711
Fu Y, Matta SG, James TJ, Sharp BM (1998) Nicotine-induced norepinephrine release in the rat amygdala and hippocampus is mediated through brainstem nicotinic cholinergic receptors. J Pharmacol Exp Ther 284:1188–1196
Gould TJ, McCarthy MM, Keith RA (2002) MK-801 disrupts acquisition of contextual fear conditioning but enhances memory consolidation of cued fear conditioning. Behav Pharmacol 13:287–294
Gould TJ (2003) Nicotine produces a within subject enhancement of contextual fear conditioning in C57BL/6 mice independent of sex. Integr Physiol Behav Sci 38:124–132
Gould TJ, Higgins JS (2003) Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training. Neurobiol Learn Mem 80:147–157
Gould TJ, Leach PT (2014) Cellular, molecular, and genetic substrates underlying the impact of nicotine on learning. Neurobiol Learn Mem 107:108–132
Gould TJ, Lewis MC (2005) Coantagonism of glutamate receptors and nicotinic acetylcholinergic receptors disrupts fear conditioning and latent inhibition of fear conditioning. Learn Mem 12:389–398
Gould TJ, Wehner JM (1999) Nicotine enhancement of contextual fear conditioning. Behav Brain Res 102:31–39
Gould TJ, McCarthy MM, Keith RA (2002) MK-801 disrupts acquisition of contextual fear conditioning but enhances memory consolidation of cued fear conditioning. Behav Pharmacol 13:287–294
Gould TJ, Feiro O, Moore D (2004) Nicotine enhancement of trace cued fear conditioning but not delay cued fear conditioning in C57BL/6J mice. Behav Brain Res 155:167–173
Gould TJ, Portugal GS, Andre JM, Tadman MP, Marks MJ, Kenney JW et al (2012) The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation. Neuropharmacology 62:2118–2125
Gould TJ, Wilkinson DS, Yildirim E, Blendy JA, Adoff MD (2014a) Dissociation of tolerance and nicotine withdrawal-associated deficits in contextual fear. Brain Res 1559:1–10
Gould TJ, Wilkinson DS, Yildirim E, Poole RL, Leach PT, Simmons SJ (2014b) 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 109:151–159
Grady S, Marks MJ, Wonnacott S, Collins AC (1992) Characterization of nicotinic receptor-mediated [H-3] dopamine release from synaptosomes prepared from mouse striatum. J Neurochem 59:848–856
Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713–716
Gupta S, Barrett T, Whitmarsh AJ et al (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15:2760–2770
He J, Deng CY, Chen RZ, Zhu XN, Yu JP (2000) Long-term potentiation induced by nicotine in CA1 region of hippocampal slice is Ca(2+)-dependent. Acta Pharmacol Sin 21:429–432
Hobin JA, Ji J, Maren S (2006) Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 16:174–182
Hogg RC, Raggenbass M, Bertrand D (2003) Nicotinic acetylcholine receptors: from structure to brain function. Reviews of physiology, biochemistry and pharmacology. Springer, Berlin, pp 1–46)
Huang YY, Kandel ER (1994) Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learn Mem 1:74–82
Huerta PT, Sun LD, Wilson MA, Tonegawa S (2000) Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25:473–480
Hughes JR (2007) Effects of abstinence from tobacco: valid symptoms and time course. Nicotine Tob Res 9:315–327
Hulihan-Giblin BA, Lumpkin MD, Kellar KJ (1990) Acute effects of nicotine on prolactin release in the rat: agonist and antagonist effects of a single injection of nicotine. J Pharmacol Exp Ther 252:15–20
Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR (1998a) Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nat Neurosci 1:595–601
Impey S, Obrietan K, Wong ST, Poser S, Yano S, Wayman G et al (1998b) Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB dependent transcription and ERK nuclear translocation. Neuron 21:869–883
Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR (2005) Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57:56–66
Jacobsen LK, Slotkin TA, Westerveld M, Menci WE, Pugh KR (2006) Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31:1550–1561
Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749–758
Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22:555–561
Karadsheh MS, Shah MS, Tang X, Macdonald RL, Stitzel JA (2004) Functional characterization of mouse alpha4beta2 nicotinic acetylcholine receptors stably expressed in HEK293T cells. J Neurochem 91:1138–1150
Kenney JW, Gould TJ (2008a) Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38:101–121
Kenney JW, Gould TJ (2008b) Nicotine enhances context learning but not context-shock associative learning. Behav Neurosci 122:1158–1165
Kenney JW, Florian C, Portugal GS, Abel T, Gould TJ (2010) Involvement of hippocampal jun-N terminal kinase pathway in the enhancement of learning and memory by nicotine. Neuropsychopharmacology 35:483–492
Kenney JW, Adoff MD, Wilkinson DS, Gould TJ (2011) The effects of acute, chronic, and withdrawal from chronic nicotine on novel and spatial object recognition in male C57BL/6J mice. Psychopharmacology 217:353–365
Kenney JW, Raybuck JD, Gould TJ (2012a) Nicotinic receptors in the dorsal and ventral hippocampus differentially modulate contextual fear conditioning. Hippocampus 22:1681–1690
Kenney JW, Poole RL, Adoff MD, Logue SF, Gould TJ (2012b) Learning and nicotine interact to increase CREB phosphorylation at the jnk1 promoter in the hippocampus. PLoS One 7:e39939
Kholdebarin E, Caldwell DP, Blackwelder WP, Kao M, Christopher NC, Levin ED (2007) Interaction of nicotinic and histamine H3 systems in the radial-arm maze repeated acquisition task. Eur J Pharmacol 569:64–69
Klann E, Chen SJ, Sweatt JD (1991) Persistent protein kinase activation in the maintenance phase of long-term potentiation. J Biol Chem 266:24253–24256
Knight DC, Cheng DT, Smith CN, Stein EA, Helmstetter FJ (2004) Neural substrates mediating human delay and trace fear conditioning. J Neurosci 24:218–228
Konorski J (1967) Integrative activity of the brain. University of Chicago Press, Chicago
Kota D, Robinson SE, Imad Damaj M (2009) Enhanced nicotine reward in adulthood after exposure to nicotine during early adolescence in mice. Biochem Pharmacol 78:873–879
Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39–42
Kutlu MG, Gould TJ (2014) Acute nicotine delays extinction of contextual fear in mice. Behav Brain Res 263:133–137
Le Novere N, Grutter T, Changeux JP (2002) Models of the extracellular domain of the nicotinic receptors and of agonist-and Ca2+-binding sites. Proc Natl Acad Sci USA 99:3210–3215
Levin ED, Torry D (1996) Acute and chronic nicotine effects on working memory in aged rats. Psychopharmacology 123:88–97
Levin ED, Lee C, Rose JE et al (1990) Chronic nicotine and withdrawal effects on radial-arm maze performance in rats. Behav Neural Biol 53:269–276
Levin ED, Briggs SJ, Christopher NC, Rose JE (1992) Persistence of chronic nicotine-induced cognitive facilitation. Behav Neural Biol 58:152–158
Levin ED, Briggs SJ, Christopher NC, Rose JE (1993a) Chronic nicotinic stimulation and blockade effects on working memory. Behav Pharmacol 4:179–182
Levin ED, Christopher NC, Briggs SJ, Rose JE (1993b) Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Brain Res Cogn Brain Res. 1:137-43
Levin ED, Kaplan S, Boardman A (1997) Acute nicotine interactions with nicotinic and muscarinic antagonists: working and reference memory effects in the 16-arm radial maze. Behav Pharmacol 8:236–242
Levin ED, Bettegowda C, Weaver T, Christopher NC (1998) Nicotine-dizocilpine interactions and working and reference memory performance of rats in the radial-arm maze. Pharmacol Biochem Behav 61:335–340
Levin ED, Christopher NC, Weaver T, Moore J, Brucato F (1999) Ventral hippocampal ibotenic acid lesions block chronic nicotine-induced spatial working memory improvement in rats. Cogn Brain Res 7:405–410
Levin ED, Bradley A, Addy N, Sigurani N (2002) Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory. Neuroscience 109:757–765
Levin ED, Sledge D, Baruah A, Addy NA (2003) Ventral hippocampal NMDA blockade and nicotinic effects on memory function. Brain Res Bull 61:489–495
Levin E, Icenogle L, Farzad A (2005a) Ketanserin attenuates nicotine-induced working memory improvement in rats. Pharmacol Biochem Behav 82:289–292
Levin ED, Tizabi Y, Rezvani AH, Caldwell DP, Petro A, Getachew B (2005b) Chronic nicotine and dizocilpine effects on regionally specific nicotinic and NMDA glutamate receptor binding. Brain Res 1041:132–142
Li XM, Li CC, Yu SS, Chen JT, Sabapathy K, Ruan DY (2007) JNK1 contributes to metabotropic glutamate receptor-dependent long-term depression and short-term synaptic plasticity in the mice area hippocampal CA1. Eur J Neurosci 25:391–396
Lotfipour S, Byun JS, Leach P et al (2013) Targeted deletion of the mouse alpha2 nicotinic acetylcholine receptor subunit gene (Chrna2) potentiates nicotine-modulated behaviors. J Neurosci 33:7728–7741
Lynch G, Kessler M, Arai A, Larson J (1990) The nature and causes of hippocampal long-term potentiation. Prog Brain Res 83:233–250
Marks MJ (1999) Desensitization and the regulation of neuronal nicotinic receptors. In: Arneric SP, Brioni JD (eds) Neuronal nicotinic receptors: pharmacology and therapeutic opportunities. Wiley-Liss, New York, pp 65–80
Marks MJ, Collins AC (1982) Characterization of nicotine binding in mouse brain and comparison with the binding of alpha-bungarotoxin and quinuclidinyl benzilate. Mol Pharmacol 22:554–564
Marks MJ, Burch JB, Collins AC (1983) Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J Pharmacol Exp Ther 226:817–825
Marks MJ, Stitzel JA, Collins AC (1985) Time course study of the effects of chronic nicotine infusion on drug response and brain receptors. J Pharmacol Exp Ther 235:619–628
Marks MJ, Stitzel JA, Romm E, Wehner JM, Collins AC (1986) Nicotinic binding sites in rat and mouse brain: comparison of acetylcholine, nicotine, and alpha-bungarotoxin. Mol Pharmacol 30:427–436
Marks MJ, Grady SR, Collins AC (1993) Downregulation of nicotinic receptor function after chronic nicotine infusion. J Pharmacol Exp Ther 266:1268–1276
Matsuyama S, Matsumoto A (2003) Epibatidine induces long-term potentiation (LTP) via activation of alpha4beta2 nicotinic acetylcholine receptors (nAChRs) in vivo in the intact mouse dentate gyrus: both alpha7 and alpha4beta2 nAChRs essential to nicotinic LTP. J Pharmacol Sci. 93:180–187
Matsuyama S, Matsumoto A, Enomoto T, Nishizaki T (2000) Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci 12:3741–3747
Matta SG, Balfour DJ, Benowitz NL et al (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology 190:269–319
McCallum SE, Caggiula AR, Booth S, Breese CR, Lee MJ, Donny EC, Sved AF (2000) Mecamylamine prevents tolerance but enhances whole brain [3H] epibatidine binding in response to repeated nicotine administration in rats. Psychopharmacology 150:1–8
McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF (1998) Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8:638–646
McGehee DS (1999) Molecular diversity of neuronal nicotinic acetylcholine receptors. Ann N Y Acad Sci 868:565–577
McKay BE, Placzek AN, & Dani JA (2007) Regulation of synaptic transmission and plasticity by neuronal nicotinic acetylcholine receptors. Biochem Pharmacol, 74:1120–1133
Mendrek A, Monterosso J, Simon SL, Jarvik M, Brody A, Olmstead R, Domier CP, Cohen MS, Ernst M, London ED (2006) Working memory in cigarette smokers: comparison to non-smokers and effects of abstinence. Addict Behav 31:833–844
Morris RG, Anderson E, Lynch GS, Baudry M (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319:774–776
Myers CS, Taylor RC, Moolchan ET, Heishman SJ (2008) Dose-related enhancement of mood and cognition in smokers administered nicotine nasal spray. Neuropsychopharmacology 33:588–598
Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD et al (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297:211–218
Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104–1107
Nicoll RA, Malenka RC (1999) Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 868:515–525
O’Dell LE, Bruijnzeel AW, Smith RT, Parsons LH, Merves ML, Goldberger BA, Richardson HN, Koob GF, Markou A (2006) Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction. Psychopharmacology 186:612–619
Olale F, Gerzanich V, Kuryatov A, Wang F, Lindstrom J (1997) Chronic nicotine exposure differentially affects the function of human alpha3, alpha4, and alpha7 neuronal nicotinic receptor subtypes. J Pharmacol Exp Ther 283:675–683
Orr-Urtreger A, Seldin MF, Baldini A, Beaudet AL (1995) Cloning and mapping of the mouse alpha 7-neuronal nicotinic acetylcholine receptor. Genomics 26:399–402
Orr-Urtreger A, Goldner FM, Saeki M et al (1997) Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents. J Neurosci 17:9165–9171
Otani S, Marshall CJ, Tate WP, Goddard GV, Abraham WC (1989) Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization. Neuroscience 28:519–526
Park S, Knopick C, McGurk S, Meltzer HY (2000) Nicotine impairs spatial working memory while leaving spatial attention intact. Neuropsychopharmacology 22:200–209
Patterson F, Jepson C, Strasser AA, Loughead J, Perkins KA, Gur RC, Lerman C (2009) Varenicline improves mood and cognition during smoking abstinence. Biol Psychiatry 65:144–149
Patterson F, Jepson C, Loughead J, Perkins K, Strasser AA, Siegel S, Lerman C (2010) Working memory deficits predict short-term smoking resumption following brief abstinence. Drug Alcohol Depend 106:61–64
Paylor R, Nguyen M, Crawley JN, Patrick J, Beaudet A, Orr-Urtreger A (1998) Alpha 7 nicotinic receptor subunits are not necessary for hippocampal-dependent learning or sensorimotor gating: a behavioral characterization of acra7-deficient mice. Learn Mem 5:302–316
Perry DC, Xiao Y, Nguyen HN, Musachio JL, Davila-Garcia MI, Kellar KJ (2002) Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J Neurochem 82:468–481
Place R, Lykken C, Beer Z, Suh J, McHugh TJ, Tonegawa S et al (2012) NMDA signaling in CA1 mediates selectively the spatial component of episodic memory. Learn Mem 19:164–169
Platenik J, Kuramoto N, Yoneda Y (2000) Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci 67:335–364
Pocivavsek A, Icenogle L, Levin ED (2006) Ventral hippocampal alpha7 and alpha4beta2 nicotinic receptor blockade and clozapine effects on memory in female rats. Psychopharmacology 188:597–604
Polesskaya OO, Fryxell KJ, Merchant AD, Locklear LL, Ker KF, McDonald CG et al (2007) Nicotine causes age-dependent changes in gene expression in the adolescent female rat brain. Neurotoxicol Teratol 29:126–140
Porter JT, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19:5228–5235
Portugal GS, Gould TJ (2009) Nicotine withdrawal disrupts new contextual learning. Pharmacol Biochem Behav 92:117–123
Portugal GS, Kenney JW, Gould TJ (2008) b2 Containing Acetylcholine Receptors Mediate Nicotine Withdrawal Deficits in Learning. Neurobiol Learn Mem 89:106–113
Portugal G, Wilkinson D, Kenney J, Sullivan C, Gould T (2012a) Strain-dependent effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Behav Genetics 42:1–18
Portugal GS, Wilkinson DS, Turner JR, Blendy JA, Gould TJ (2012b) Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Neurobiol Learn Mem 97:482–494
Poser S, Storm DR (2001) Role of Ca2 + -stimulated adenylyl cyclases in LTP and memory formation. Int J Dev Neurosci 19:387–394
Radcliffe KA, Fisher JL, Gray R, Dani JA (1999) Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 868:591–610
Rapier C, Lunt GG, Wonnacott S (1990) Nicotinic modulation of [3H]dopamine release from striatal synaptosomes: pharmacological characterisation. J Neurochem 54:937–945
Raybuck JD, Gould TJ (2007) Extracellular signal-regulated kinase 1/2 involvement in the enhancement of contextual fear conditioning by nicotine. Behav Neurosci 121:1119–1124
Raybuck JD, Gould TJ (2009) Nicotine withdrawal-induced deficits in trace fear conditioning in C57BL/6 mice–a role for high-affinity b2 subunit-containing nicotinic acetylcholine receptors. Eur J Neurosci 29:377–387
Raybuck JD, Gould TJ (2010) The role of nicotinic acetylcholine receptors in the medial prefrontal cortex and hippocampus in trace fear conditioning. Neurobiol Learn Mem 94:353–363
Ribeiro EB, Bettiker RL, Bogdanov M, Wurtman RJ (1993) Effects of systemic nicotine on serotonin release in rat brain. Brain Res 621:311–318
Robinson SE, James JR, Lapp LN, Vann RE, Gross DF, Philibin SD, Rosecrans JA (2006) Evidence of cellular nicotinic receptor desensitization in rats exhibiting nicotine-induced acute tolerance. Psychopharmacology 184:306–313
Robinson SE, Vann RE, Britton AF, O’Connell MM, James JR, Rosecrans JA (2007) Cellular nicotinic receptor desensitization correlates with nicotine-induced acute behavioral tolerance in rats. Psychopharmacology 192:71–78
Rowell PP, Winkler DL (1984) Nicotinic stimulation of [3H]acetylcholine release from mouse cerebral cortical synaptosomes. J Neurochem 43:1593–1598
Runyan JD, Moore AN, Dash PK (2004) A role for prefrontal cortex in memory storage for trace fear conditioning. J Neurosci 24:1288–1295
Rush R, Kuryatov A, Nelson ME, Lindstrom J (2002) First and second transmembrane segments of α3, α4, β2, and β4 nicotinic acetylcholine receptor subunits influence the efficacy and potency of nicotine. Mol Pharmacol 61:1416–1422
Rushforth SL, Steckler T, Shoaib M (2011) Nicotine improves working memory span capacity in rats following sub-chronic ketamine exposure. Neuropsychopharmacology 36:2774–2781
Sananbenesi F, Fischer A, Schrick C, Spiess J, Radulovic J (2002) Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1. Mol Cell Neurosci 21:463–476
Scerri C, Stewart C, Breen K, Balfour D (2006) The effects of chronic nicotine on spatial learning and bromodeoxyuridine incorporation into the dentate gyrus of the rat. Psychopharmacology 184:540–546
Schwartz RD, Kellar KJ (1983) Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science 220:214–216
Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596–604
Semenova S, Contet C, Roberts AJ, Markou A (2012) Mice Llcking the b4 subunit of the nicotinic acetylcholine receptor show memory deficits, altered anxiety- and depression-like behavior, and diminished nicotine-induced analgesia. Nicotine Tob Res 14:1346–1355
Sharifzadeh M, Tavasoli M, Naghdi N, Ghanbari A, Amini M, Roghani A (2005) Post-training intrahippocampal infusion of nicotine prevents spatial memory retention deficits induced by the cyclo-oxygenase-2-specific inhibitor celecoxib in rats. J Neurochem 95:1078–1090
Sharp BM, Beyer HS (1986) Rapid desensitization of the acute stimulatory effects of nicotine on rat plasma adrenocorticotropin and prolactin. J Pharmacol Exp Ther 238:486–491
Shram MJ, Le AD (2010) Adolescent male Wistar rats are more responsive than adult rats to the conditioned rewarding effects of intravenously administered nicotine in the place conditioning procedure. Behav Brain Res 206:240–244
Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127–148
Socci DJ, Sanberg PR, Arendash GW (1995) Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol Aging 16:857–860
Sorenson EM, Shiroyama T, Kitai ST (1998) Postsynaptic nicotinic receptors on dopaminergic neurons in the substantia nigra pars compacta of the rat. Neuroscience 87:659–673
Spaeth AM, Barnet RC, Hunt PS, Burk JA (2010) Adolescent nicotine exposure disrupts context conditioning in adulthood in rats. Pharmacol Biochem Behav 96:501–506
Staley JK, Krishnan-Sarin S, Cosgrove KP, Krantzler E, Frohlich E, Perry E, van Dyck CH (2006) Human tobacco smokers in early abstinence have higher levels of β2* nicotinic acetylcholine receptors than nonsmokers. J Neurosci 26:8707–8714
Strekalova T, Zorner B, Zacher C, Sadovska G, Herdegen T, Gass P (2003) Memory retrieval after contextual fear conditioning induces c-Fos and JunB expression in CA1 hippocampus. Genes Brain Behav 2:3–10
Szyndler J, Sienkiewicz-Jarosz H, Maciejak P et al (2001) The anxiolytic-like effect of nicotine undergoes rapid tolerance in a model of contextual fear conditioning in rats. Pharmacol Biochem Behav 69:511–518
Tian S, Gao J, Han L, Fu J, Li C, Li Z (2008) Prior chronic nicotine impairs cued fear extinction but enhances contextual fear conditioning in rats. Neuroscience 153:935–943
Tonegawa S, Tsien JZ, McHugh TJ, Huerta P, Blum KI, Wilson MA (1996) Hippocampal CA1-region-restricted knockout of NMDAR1 gene disrupts synaptic plasticity, place fields, and spatial learning. Cold Spring Harb Symp Quant Biol 61:225–238
Torres OV, Tejeda HA, Natividad LA, O’Dell LE (2008) Enhanced vulnerability to the rewarding effects of nicotine during the adolescent period of development. Pharmacol Biochem Behav 90:658–663
Trauth JA, Seidler FJ, McCook EC, Slotkin TA (1999) Adolescent nicotine exposure causes persistent upregulation of nicotinic cholinergic receptors in rat brain regions. Brain Res 851:9–19
Trauth JA, Seidler FJ, Slotkin TA (2000) An animal model of adolescent nicotine exposure: effects on gene expression and macromolecular constituents in rat brain regions. Brain Res 867:29–39
Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327–1338
Walters CL, Cleck JN, Kuo YC, Blendy JA (2005) Mu-opioid receptor and CREB activation are required for nicotine reward. Neuron, 46:933–943
Wehner JM, Keller JJ, Keller AB et al (2004) Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning. Neuroscience 129:11–24
Wenk GL, Walker LC, Price DL, Cork LC (1991) Loss of NMDA, but not GABA-A, binding in the brains of aged rats and monkeys. Neurobiol Aging 12:93–98
Westfall TC, Grant H, Perry H (1983) Release of dopamine and 5-hydroxytryptamine from rat striatal slices following activation of nicotinic cholinergic receptors. Gen Pharmacol 14:321–325
Wilkie GI, Hutson P, Sullivan JP, Wonnacott S (1996) Pharmacological characterization of a nicotinic autoreceptor in rat hippocampal synaptosomes. Neurochem Res 21:1141–1148
Wilkinson DS, Gould TJ (2013) Withdrawal from chronic nicotine and subsequent sensitivity to nicotine challenge on contextual learning. Behav Brain Res 250:58–61
Wonnacott S (1986) A bungarotoxin binds to low-affinity nicotine binding sites in rat brain. J Neurochem 47:1706–1712
Wonnacott S (1997) Presynaptic nicotinic ACh receptors. Trends Neurosci 20:92–98
Zarei MM, Radcliffe KA, Chen D, Patrick JW, Dani JA (1999) Distributions of nicotinic acetylcholine receptor alpha7 and beta2 subunits on cultured hippocampal neurons. Neuroscience 88:755–764
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This work was funded with grant support from the National Institute on Drug Abuse (T.J.G., DA017949).
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Kutlu, M.G., Gould, T.J. (2015). Nicotinic Receptors, Memory, and Hippocampus. In: Balfour, D., Munafò, M. (eds) The Neurobiology and Genetics of Nicotine and Tobacco. Current Topics in Behavioral Neurosciences, vol 23. Springer, Cham. https://doi.org/10.1007/978-3-319-13665-3_6
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