The aim of the present study was to investigate whether cognitive behavioral impairment, induced by nicotine in offspring rats, was associated with the alteration of hippocampal short-term potentiation (STP) and long-term potentiation (LTP) and to discuss the potential underlying mechanism. Young adult offspring rats were randomly divided into three groups. The groups include: control group (CC), nicotine group 1 (NC), in which their mothers received nicotine from gestational day 3 (GD3) to GD18, and nicotine group 2 (CN), in which young adult offspring rats received nicotine from postnatal day 42 (PD42) to PD56. Morris water maze (MWM) test was performed and then field excitatory postsynaptic potentials elicited by the stimulation of perforant pathway were recorded in the hippocampal dentate gyrus region. The results of the MWM test showed that learning and memory were impaired by either prenatal or postnatal nicotine exposure. In addition, it was found that there was no statistical difference of the MWM data between both nicotine treatments. In the electrophysiological test, LTP and STP were significantly inhibited in both NC and CN groups in comparison with the CC group. Notably, STP in CN group was also lower than that in the NC group. These findings suggested that both prenatal and postnatal exposure to nicotine induced learning and memory deficits, while the potential mechanism might be different from each other due to their dissimilar impairments of synaptic plasticity.

References

1. Benowitz, NL . Nicotine addiction . N Engl J Med 2010 ; 362: 2295 – 2303 .

Google Scholar Crossref | Medline | ISI

2. Wang, J, Li, MD. Common and unique biological pathways associated with smoking initiation/progression, nicotine dependence, and smoking cessation . Neuropsychopharmacology 2010 ; 35: 702 – 719 .

Google Scholar Crossref | Medline | ISI

3. Slikker, W, , Xu, ZA, Levin, ED, Slotkin, TA. Mode of action: disruption of brain cell replication, second messenger, and neurotransmitter systems during development leading to cognitive dysfunction—developmental neurotoxicity of nicotine . Crit Rev Toxicol 2005 ; 35: 703 – 711 .

Google Scholar Crossref | Medline | ISI

4. Slotkin, TA . Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates . Toxicol Appl Pharmacol 2004 ; 198: 132 – 151 .

Google Scholar Crossref | Medline | ISI

5. Wakschlag, LS, Hans, SL. Maternal smoking during pregnancy and conduct problems in high-risk youth: a developmental framework . Dev Psychopathol 2002 ; 14: 351 – 369 .

Google Scholar Crossref | Medline | ISI

6. Weitzman, M, Byrd, RS, Aligne, CA, Moss, M. The effects of tobacco exposure on children’s behavioral and cognitive functioning: implications for clinical and public health policy and future research . Neurotoxicol Teratol 2002 ; 24: 397 – 406 .

Google Scholar Crossref | Medline | ISI

7. Bergmann, KE, Bergmann, RL, Von Kries, R, Böhm, O, Richter, R, Dudenhausen, JW Early determinants of childhood overweight and adiposity in a birth cohort study: role of breast-feeding . Int J Obes Relat Metab Disord 2003 ; 27: 162 – 172 .

Google Scholar Crossref | Medline | ISI

8. Andres, RL, Day, MC. Perinatal complications associated with maternal tobacco use . Sem Neonatol 2000 ; 5: 231 – 241 .

Google Scholar Crossref | Medline

9. Santiago, SE, Huffman, KJ. Postnatal effects of prenatal nicotine exposure on body weight, brain size and cortical connectivity in mice . Neurosci Res 2012 ; 73: 282 – 291 .

Google Scholar Crossref | Medline | ISI

10. Bruin, JE, Gerstein, HC, Holloway, AC. Long-term consequences of fetal and neonatal nicotine exposure: a critical review . Toxicol Sci 2010 ; 116: 364 – 374 .

Google Scholar Crossref | Medline | ISI

11. Lambers, DS, Clark, KE. The maternal and fetal physiologic effects of nicotine . Sem Perinatol 1996 ; 20: 115 – 126 .

Google Scholar Crossref | Medline | ISI

12. Jordanov, JS . Cotinine concentrations in amniotic fluid and urine of smoking, passive smoking and non-smoking pregnant women at term and in the urine of their neonates on 1st day of life . Eur J Pediat 1990 ; 149: 734 – 737 .

Google Scholar Crossref | Medline | ISI

13. Pauly, JR, Slotkin, TA. Maternal tobacco smoking, nicotine replacement and neurobehavioural development . Acta Paediat 2008 ; 97: 1331 – 1337 .

Google Scholar Crossref | Medline | ISI

14. Dwyer, JB, McQuown, SC, Leslie, FM. The dynamic effects of nicotine on the developing brain . Pharmacol Therap 2009 ; 122: 125 – 139 .

Google Scholar Crossref | Medline | ISI

15. Rogers, JM . Tobacco and pregnancy . Reprod Toxicol 2009 ; 28: 152 – 160 .

Google Scholar Crossref | Medline | ISI

16. Blood-Siegfried, J, Rende, EK. The long-term effects of prenatal nicotine exposure on neurologic development . J Midwifery Wom Health 2010 ; 55: 143 – 152 .

Google Scholar Crossref | Medline | ISI

17. Abreu-Villaca, Y, Seidler, FJ, Qiao, D, Tate, CA, Cousins, MM, Thillai, I Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds . Neuropsychopharmacol 2003 ; 28: 1935 – 1949 .

Google Scholar Crossref | Medline | ISI

18. Collins, SL, Wade, D, Ledon, J, Izenwasser, S. Neurochemical alterations produced by daily nicotine exposure in periadolescent vs. adult male rats . Eur J Pharmacol 2004 ; 502: 75 – 85 .

Google Scholar Crossref | Medline | ISI

19. Elliott, BM, Faraday, MM, Phillips, JM, Grunberg, NE. Adolescent and adult female rats differ in sensitivity to nicotine's activity effects . Pharmacol Biochem Behav 2005 ; 80: 567 – 575 .

Google Scholar Crossref | Medline | ISI

20. Roy, TS, Sabherwal, U. Effects of gestational nicotine exposure on hippocampal morphology . Neurotoxicol Teratol 1998 ; 20: 465 – 473 .

Google Scholar Crossref | Medline | ISI

21. Shram, MJ, Li, Z, Le, AD. Age differences in the spontaneous acquisition of nicotine self-administration in male Wistar and Long-Evans rats . Psychopharmacology (Berl) 2008 ; 197: 45 – 58 .

Google Scholar Crossref | Medline | ISI

22. Matta, SG, Balfour, DJ, Benowitz, NL, Boyd, RT, Buccafusco, JJ, Caggiula, AR Guidelines on nicotine dose selection for in vivo research . Psychopharmacology (Berl) 2007 ; 190: 269 – 319 .

Google Scholar Crossref | Medline | ISI

23. DiFranza, JR, Lew, RA. Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome . J Fam Pract 1995 ; 40: 385 – 394 .

Google Scholar Medline | ISI

24. Socci, DJ, Sanberg, PR, Arendash, GW. Nicotine enhances Morris water maze performance of young and aged rats . Neurobiol Aging 1995 ; 16: 857 – 860 .

Google Scholar Crossref | Medline | ISI

25. Abdulla, FA, Bradbury, E, Calaminici, MR, Lippiello, PM, Wonnacott, S, Gray, JA Relationship between up-regulation of nicotine binding sites in rat brain and delayed cognitive enhancement observed after chronic or acute nicotinic receptor stimulation . Psychopharmacology (Berl) 1996 ; 124: 323 – 331 .

Google Scholar Crossref | Medline | ISI

26. Tian, S, Gao, J, Han, L, Fu, J, Li, C, Li, Z. Prior chronic nicotine impairs cued fear extinction but enhances contextual fear conditioning in rats . Neuroscience 2008 ; 153: 935 – 943 .

Google Scholar Crossref | Medline | ISI

27. Le Houezec, J, Jacob, P, Benowitz, NL. A clinical pharmacological study of subcutaneous nicotine . Eur J Clin Pharmacol 1993 ; 44: 225 – 230 .

Google Scholar Crossref | Medline | ISI

28. Ajarem, JS, Ahmad, M. Prenatal nicotine exposure modifies behavior of mice through early development . Pharmacol Biochem Behav 1998 ; 59: 313 – 318 .

Google Scholar Crossref | Medline | ISI

29. Morris, R . Developments of a water-maze procedure for studying spatial learning in the rat . J Neurosci Meth 1984 ; 11: 47 – 60 .

Google Scholar Crossref | Medline | ISI

30. An, L, Li, Z, Yang, Z, Zhang, T. Melamine induced cognitive impairment associated with oxidative damage in rat's hippocampus . Pharmacol Biochem Behav 2012 ; 102: 196 – 202 .

Google Scholar Crossref | Medline | ISI

31. An, L, Yang, Z, Zhang, T. Imbalanced synaptic plasticity induced spatial cognition impairment in male offspring rats treated with chronic prenatal ethanol exposure . Alcoholism Clin Exp Res 2012 ; 37: 763 – 770 .

Google Scholar Crossref | Medline | ISI

32. An, L, Liu, S, Yang, Z, Zhang, T. Cognitive impairment in rats induced by nano-CuO and its possible mechanisms . Toxicol Lett 2012 ; 213: 220 – 227 .

Google Scholar Crossref | Medline | ISI

33. An, L, Yang, Z, Zhang, T. Melamine induced spatial cognitive deficits associated with impairments of hippocampal long-term depression and cholinergic system in Wistar rats . Neurobiol Learn Mem 2013 ; 100: 18 – 24 .

Google Scholar Crossref | Medline | ISI

34. Paxinos, G, Watson, CR, Emson, PC. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates . J Neurosci Meth 1980 ; 3: 129 – 149 .

Google Scholar Crossref | Medline | ISI

35. Boric, K, Munoz, P, Gallagher, M, Kirkwood, A. Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus . J Neurosci 2008 ; 28: 8034 – 8039 .

Google Scholar Crossref | Medline | ISI

36. Quan, MN, Tian, YT, Xu, KH, Zhang, T, Yang, Z. Post weaning social isolation influences spatial cognition, prefrontal cortical synaptic plasticity and hippocampal potassium ion channels in Wistar rats . Neuroscience 2010 ; 169: 214 – 222 .

Google Scholar Crossref | Medline | ISI

37. An, L, Li, Z, Yang, Z, Zhang, T. Cognitive deficits induced by melamine in rats . Toxicol Lett 2011 ; 206: 276 – 280 .

Google Scholar Crossref | Medline | ISI

38. MacIver, MB, Roth, SH. Barbiturate effects on hippocampal excitatory synaptic responses are selective and pathway specific . Can J Physiol Pharmacol 1987 ; 65: 385 – 394 .

Google Scholar Crossref | Medline | ISI

39. Wu, K, Li, S, Bodhinathan, K, Meyers, C, Chen, W, Campbell-Thompson, M Enhanced expression of Pctk1, Tcf12 and Ccnd1 in hippocampus of rats: impact on cognitive function, synaptic plasticity and pathology . Neurobiol Learn Mem 2012 ; 97: 69 – 80 .

Google Scholar Crossref | Medline | ISI

40. Kang, H, Welcher, AA, Shelton, D, Schuman, EM. Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation . Neuron 1997 ; 19: 653 – 664 .

Google Scholar Crossref | Medline | ISI

41. Erickson, MA, Maramara, LA, Lisman, J. A single brief burst induces GluR1-dependent associative short-term potentiation: a potential mechanism for short-term memory . J Cognitive Neurosci 2010 ; 22: 2530 – 2540 .

Google Scholar Crossref | Medline | ISI

42. Cowan, N, AuBuchon, AM. Short-term memory loss over time without retroactive stimulus interference . Psychon Bull Rev 2008 ; 15: 230 – 235 .

Google Scholar Crossref | Medline | ISI

43. Placzek, AN, Zhang, TA, Dani, JA. Nicotinic mechanisms influencing synaptic plasticity in the hippocampus . Acta Pharmacol Sin 2009 ; 30: 752 – 760 .

Google Scholar Crossref | Medline | ISI

44. Winzer-Serhan, UH . Long-term consequences of maternal smoking and developmental chronic nicotine exposure . Front Biosci 2008 ; 13: 636 – 649 .

Google Scholar Crossref | Medline | ISI

45. Bernal, MC, Vicens, P, Carrasco, MC, Redolat, R. Effects of nicotine on spatial learning in C57BL mice . Behav Pharmacol 1999 ; 10: 333 – 336 .

Google Scholar Crossref | Medline | ISI

46. Scerri, C, Stewart, CA, Breen, KC, Balfour, DJ. The effects of chronic nicotine on spatial learning and bromodeoxyuridine incorporation into the dentate gyrus of the rat . Psychopharmacology (Berl). 2006 ; 184: 540 – 546 .

Google Scholar Crossref | Medline | ISI

47. Kenney, JW, Gould, TJ. Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine . Mol Neurobiol 2008 ; 38: 101 – 121 .

Google Scholar Crossref | Medline | ISI

48. Eppolito, AK, Bachus, SE, McDonald, CG, Meador-Woodruff, JH, Smith, RF. Late emerging effects of prenatal and early postnatal nicotine exposure on the cholinergic system and anxiety-like behavior . Neurotoxicol Teratol 2010 ; 32: 336 – 345 .

Google Scholar Crossref | Medline | ISI

49. Eugenin, J, Otarola, M, Bravo, E, Coddou, C, Cerpa, V, Reyes-Parada, M Prenatal to early postnatal nicotine exposure impairs central chemoreception and modifies breathing pattern in mouse neonates: a probable link to sudden infant death syndrome . J Neurosci 2008 ; 28: 13907 – 13917 .

Google Scholar Crossref | Medline | ISI

50. Levin, ED, Christopher, NC, Weaver, T, Moore, J, Brucato, F. Ventral hippocampal ibotenic acid lesions block chronic nicotine-induced spatial working memory improvement in rats . Brain Res Cogn Brain Res 1999 ; 7: 405 – 410 .

Google Scholar Crossref | Medline

51. Szyndler, J, Sienkiewicz-Jarosz, H, Maciejak, P, Siemiatkowski, M, Rokicki, D, Członkowska, AI The anxiolytic-like effect of nicotine undergoes rapid tolerance in a model of contextual fear conditioning in rats . Pharmacol Biochem Behav 2001 ; 69: 511 – 518 .

Google Scholar Crossref | Medline | ISI

52. Morris, RG . Long-term potentiation and memory . Philos Trans R Soc Lond B, Biol Sci 2003 ; 358: 643 – 647 .

Google Scholar Crossref | Medline | ISI

53. Bliss, TV, Collingridge, GL. A synaptic model of memory: long-term potentiation in the hippocampus . Nature 1993 ; 361: 31 – 39 .

Google Scholar Crossref | Medline | ISI

54. Xu, Z, Seidler, FJ, Ali, SF, Slikker, W, Slotkin, TA. Fetal and adolescent nicotine administration: effects on CNS serotonergic systems . Brain Res 2001 ; 914: 166 – 178 .

Google Scholar Crossref | Medline | ISI

55. Brazell, MP, Mitchell, SN, Gray, JA. Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats: a dose-response and antagonist study . Neuropharmacology 1991 ; 30: 823 – 833 .

Google Scholar Crossref | Medline | ISI

56. Abreu-Villaca, Y, Seidler, FJ, Tate, CA, Slotkin, TA. Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations . Brain Res 2003 ; 979: 114 – 128 .

Google Scholar Crossref | Medline | ISI

57. Lindner, MD . Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze . Neurobiol Learn Mem 1997 ; 68: 203 – 220 .

Google Scholar Crossref | Medline | ISI

58. Palencia, CA, Ragozzino, ME. The effect of N-methyl- d -aspartate receptor blockade on acetylcholine efflux in the dorsomedial striatum during response reversal learning . Neuroscience 2006 ; 143: 671 – 678 .

Google Scholar Crossref | Medline | ISI

59. Sarter, M, Bruno, JP, Givens, B. Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learn Mem 2003 ; 80: 245 – 256 .

Google Scholar Crossref | Medline | ISI

60. Alkondon, M, Braga, MF, Pereira, EF, Maelicke, A, Albuquerque, EX. Alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus . Eur J Pharmacol 2000 ; 393: 59 – 67 .

Google Scholar Crossref | Medline | ISI

61. Buhler, AV, Dunwiddie, TV. Regulation of the activity of hippocampal stratum oriens interneurons by alpha7 nicotinic acetylcholine receptors . Neuroscience 2001 ; 106: 55 – 67 .

Google Scholar Crossref | Medline | ISI

62. Welsby, P, Rowan, M, Anwyl, R. Nicotinic receptor-mediated enhancement of long-term potentiation in-volves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus . Eur J Neurosci 2006 ; 24: 3109 – 3118 .

Google Scholar Crossref | Medline | ISI

63. Winder, DG, Mansuy, IM, Osman, M, Moallem, TM, Kandel, ER. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin . Cell 1998 ; 92: 25 – 37 .

Google Scholar Crossref | Medline | ISI

64. Sandberg, A, Tegner, J, Lansner, A. A working memory model based on fast Hebbian learning . Network 2003 ; 14: 789 – 802 .

Google Scholar Crossref | Medline | ISI

65. Hartley, T, Bird, CM, Chan, D, Cipolotti, L, Husain, M, Vargha-Khadem, F The hippocampus is required for short-term topographical memory in humans . Hippocampus 2007 ; 17: 34 – 48 .

Google Scholar Crossref | Medline | ISI

66. Ranganath, C, Blumenfeld, RS. Doubts about double dissociations between short- and long-term memory . Tren Cogn Sci 2005 ; 9: 374 – 380 .

Google Scholar Crossref | Medline | ISI

67. Mann, EO, Greenfield, SA. Novel modulatory mechanisms revealed by the sustained application of nicotine in the guinea-pig hippocampus in vitro . J Physiol 2003 ; 551: 539 – 550 .

Google Scholar Crossref | Medline | ISI

68. Fujii, S, Ji, Z, Sumikawa, K. Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region . Neurosci Lett 2000 ; 286: 134 – 138 .

Google Scholar Crossref | Medline | ISI

69. Ji, D, Lape, R, Dani, JA. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity . Neuron 2001 ; 31: 131 – 141 .

Google Scholar Crossref | Medline | ISI