Early postnatal nicotine exposure causes hippocampus-dependent memory impairments in adolescent mice: Association with altered nicotinic cholinergic modulation of LTP, but not impaired LTP

Neurobiology of Learning and Memory

Volumn 118, Issue , 2015, Pages 178-188

  Nakauchi, Sakura ^a   Malvaez, Melissa ^a,b   Su, Hailing ^a   Kleeman, Elise ^a   Dang, Richard ^a   Wood, Marcelo A ^a   Sumikawa, Katumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CA1 region; Object location memory; Object recognition memory; Schaffer collateral pathway; Temporoammonic pathway

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; BREAST MILK; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PERINATAL DRUG EXPOSURE; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; AGE; ANIMAL; ANXIETY; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; HIPPOCAMPUS; NERVE CELL; RECOGNITION; SPATIAL MEMORY;

AGE FACTORS; ANIMALS; ANXIETY; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; NEURONS; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RECOGNITION (PSYCHOLOGY); SPATIAL MEMORY;

EID: 84920973642     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.12.007     Document Type: Article

References (64)

1. Adams C.E., Broide R.S., Chen Y., Winzer-Serhan U.H., Henderson T.A., Leslie F.M., et al. Development of the alpha7 nicotinic cholinergic receptor in rat hippocampal formation. Brain Research Developmental Brain Research 2002, 139(2):175-187.
2. Ankarberg E., Fredriksson A., Eriksson P. Neurobehavioural defects in adult mice neonatally exposed to nicotine: Changes in nicotine-induced behaviour and maze learning performance. Behavioural Brain Research 2001, 123(2):185-192.
3. Assini F.L., Duzzioni M., Takahashi R.N. Object location memory in mice: Pharmacological validation and further evidence of hippocampal CA1 participation. Behavioural Brain Research 2009, 204(1):206-211.
4. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., et al. Regional dissociations within the hippocampus-memory and anxiety. Neuroscience and Biobehavioral Reviews 2004, 28(3):273-283.
5. Barrett R.M., Malvaez M., Kramar E., Matheos D.P., Arrizon A., Cabrera S.M., et al. Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory. Neuropsychopharmacology 2011, 36(8):1545-1556.
6. Batstra L., Hadders-Algra M., Neeleman J. Effect of antenatal exposure to maternal smoking on behavioural problems and academic achievement in childhood: Prospective evidence from a Dutch birth cohort. Early Human Development 2003, 75(1-2):21-33.
7. Britton A.F., Vann R.E., Robinson S.E. Perinatal nicotine exposure eliminates peak in nicotinic acetylcholine receptor response in adolescent rats. The Journal of Pharmacology and Experimental Therapeutics 2007, 320(2):871-876.
8. Bruin J.E., Gerstein H.C., Holloway A.C. Long-term consequences of fetal and neonatal nicotine exposure: A critical review. Toxicological Sciences 2010, 116(2):364-374.
9. Cutler A.R., Wilkerson A.E., Gingras J.L., Levin E.D. Prenatal cocaine and/or nicotine exposure in rats: Preliminary findings on long-term cognitive outcome and genital development at birth. Neurotoxicology and Teratology 1996, 18(6):635-643.
10. Damborsky J.C., Griffith W.H., Winzer-Serhan U.H. Chronic neonatal nicotine exposure increases excitation in the young adult rat hippocampus in a sex-dependent manner. Brain Research 2012, 1430:8-17.
11. Danglot L., Triller A., Marty S. The development of hippocampal interneurons in rodents. Hippocampus 2006, 16(12):1032-1060.
12. de Graaf-Peters V.B., Hadders-Algra M. Ontogeny of the human central nervous system: What is happening when?. Early Human Development 2006, 82(4):257-266.
13. Dwyer J.B., McQuown S.C., Leslie F.M. The dynamic effects of nicotine on the developing brain. Pharmacology & Therapeutics 2009, 122(2):125-139.
14. Eppolito A.K., Smith R.F. Long-term behavioral and developmental consequences of pre- and perinatal nicotine. Pharmacology, Biochemistry, and Behavior 2006, 85(4):835-841.
15. Eriksson P., Ankarberg E., Fredriksson A. Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotinic receptors and in behaviour of adult mice. Brain Research 2000, 853(1):41-48.
16. Fried P.A., Watkinson B., Gray R. Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicology and Teratology 2003, 25(4):427-436.
17. Gu Z., Lamb P.W., Yakel J.L. Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. The Journal of Neuroscience 2012, 32(36):12337-12348.
18. Gu Z., Yakel J.L. Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 2011, 71(1):155-165.
19. Haettig J., Sun Y., Wood M.A., Xu X. Cell-type specific inactivation of hippocampal CA1 disrupts location-dependent object recognition in the mouse. Learning & Memory 2013, 20(3):139-146.
20. Halff A.W., Gomez-Varela D., John D., Berg D.K. A novel mechanism for nicotinic potentiation of glutamatergic synapses. The Journal of Neuroscience 2014, 34(6):2051-2064.
21. Huang L.Z., Liu X., Griffith W.H., Winzer-Serhan U.H. Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats. Behavioral Neuroscience 2007, 121(6):1342-1352.
22. Huang L.Z., Winzer-Serhan U.H. Chronic neonatal nicotine upregulates heteromeric nicotinic acetylcholine receptor binding without change in subunit mRNA expression. Brain Research 2006, 1113(1):94-109.
23. Ishibashi M., Yamazaki Y., Miledi R., Sumikawa K. Nicotinic and muscarinic agonists and acetylcholinesterase inhibitors stimulate a common pathway to enhance GluN2B-NMDAR responses. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(34):12538-12543.
24. Ishii K., Wong J.K., Sumikawa K. Comparison of alpha2 nicotinic acetylcholine receptor subunit mRNA expression in the central nervous system of rats and mice. The Journal of Comparative Neurology 2005, 493(2):241-260.
25. Ji D., Lape R., Dani J.A. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 2001, 31(1):131-141.
26. Kenney J.W., Gould T.J. Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Molecular Neurobiology 2008, 38(1):101-121.
27. Kjelstrup K.G., Tuvnes F.A., Steffenach H.A., Murison R., Moser E.I., Moser M.B. Reduced fear expression after lesions of the ventral hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(16):10825-10830.
28. Levin E.D., Briggs S.J., Christopher N.C., Rose J.E. Chronic nicotinic stimulation and blockade effects on working memory. Behavioural Pharmacology 1993, 4(2):179-182.
29. Liu Z., Neff R.A., Berg D.K. Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 2006, 314(5805):1610-1613.
30. Liu Z., Zhang J., Berg D.K. Role of endogenous nicotinic signaling in guiding neuronal development. Biochemical Pharmacology 2007, 74(8):1112-1119.
31. Maggi L., Le Magueresse C., Changeux J.P., Cherubini E. Nicotine activates immature "silent" connections in the developing hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(4):2059-2064.
32. Maggi L., Sola E., Minneci F., Le Magueresse C., Changeux J.P., Cherubini E. Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus. The Journal of Physiology 2004, 559(Pt 3):863-874.
33. Mahar I., Bagot R.C., Davoli M.A., Miksys S., Tyndale R.F., Walker C.D., Maheu M., Huang S.H., Wong T.P., Mechawar N. Developmental hippocampal neuroplasticity in a model of nicotine replacement therapy during pregnancy and breastfeeding. PLos One 2012, 7:e37219.
34. McNew J.J., Thompson R. Role of the limbic system in active and passive avoidance conditioning in the rat. Journal of Comparative and Physiological Psychology 1966, 61(2):173-180.
35. McQuown S.C., Barrett R.M., Matheos D.P., Post R.J., Rogge G.A., Alenghat T., et al. HDAC3 is a critical negative regulator of long-term memory formation. The Journal of Neuroscience 2011, 31(2):764-774.
36. Miao H., Liu C., Bishop K., Gong Z.H., Nordberg A., Zhang X. Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain. Journal of Neurochemistry 1998, 70(2):752-762.
37. Moscarello J.M., LeDoux J.E. Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. The Journal of Neuroscience 2013, 33(9):3815-3823.
38. Moses S.N., Cole C., Driscoll I., Ryan J.D. Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships. Brain Research Bulletin 2005, 67(1-2):62-76.
39. Naeff B., Schlumpf M., Lichtensteiger W. Pre- and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: An autoradiographic study. Brain Research Developmental Brain Research 1992, 68(2):163-174.
40. Nakauchi S., Brennan R.J., Boulter J., Sumikawa K. Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2* nicotinic ACh receptors. The European Journal of Neuroscience 2007, 25(9):2666-2681.
41. Nakauchi S., Sumikawa K. Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice. The European Journal of Neuroscience 2012, 35(9):1381-1395.
42. Narayanan U., Birru S., Vaglenova J., Breese C.R. Nicotinic receptor expression following nicotine exposure via maternal milk. Neuroreport 2002, 13(7):961-963.
43. Norman G., Eacott M.J. Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behavioural Brain Research 2004, 148(1-2):79-91.
44. Pauly J.R., Slotkin T.A. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatrica 2008, 97(10):1331-1337.
45. Portugal G.S., Wilkinson D.S., Turner J.R., Blendy J.A., Gould T.J. Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Neurobiology of Learning and Memory 2012, 97(4):482-494.
46. Posadas I., Lopez-Hernandez B., Cena V. Nicotinic receptors in neurodegeneration. Current Neuropharmacology 2013, 11(3):298-314.
47. Roozendaal B., Hernandez A., Cabrera S.M., Hagewoud R., Malvaez M., Stefanko D.P., et al. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. The Journal of Neuroscience 2010, 30(14):5037-5046.
48. Seress L. Comparative anatomy of the hippocampal dentate gyrus in adult and developing rodents, non-human primates and humans. Progress in Brain Research 2007, 163:23-41.
49. Seress L., Abraham H., Tornoczky T., Kosztolanyi G. Cell formation in the human hippocampal formation from mid-gestation to the late postnatal period. Neuroscience 2001, 105(4):831-843.
50. Shacka J.J., Robinson S.E. Exposure to prenatal nicotine transiently increases neuronal nicotinic receptor subunit alpha7, alpha4 and beta2 messenger RNAs in the postnatal rat brain. Neuroscience 1998, 84(4):1151-1161.
51. Son J.H., Winzer-Serhan U.H. Postnatal expression of alpha2 nicotinic acetylcholine receptor subunit mRNA in developing cortex and hippocampus. Journal of Chemical Neuroanatomy 2006, 32(2-4):179-190.
52. Sorenson C.A., Raskin L.A., Suh Y. The effects of prenatal nicotine on radial-arm maze performance in rats. Pharmacology, Biochemistry, and Behavior 1991, 40(4):991-993.
53. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(23):9447-9452.
54. Tominaga T., Tominaga Y., Yamada H., Matsumoto G., Ichikawa M. Quantification of optical signals with electrophysiological signals in neural activities of Di-4-ANEPPS stained rat hippocampal slices. Journal of Neuroscience Methods 2000, 102(1):11-23.
55. Tong V.T., Dietz P.M., Morrow B., D'Angelo D.V., Farr S.L., Rockhill K.M., et al. Trends in smoking before, during, and after pregnancy-pregnancy risk assessment monitoring system, United States, 40 sites, 2000-2010. Morbidity and Mortality Weekly Report Surveillance Summaries 2013, 62(6):1-19.
56. Tribollet E., Bertrand D., Marguerat A., Raggenbass M. Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: An autoradiographic study in the rat brain. Neuroscience 2004, 124(2):405-420.
57. Vaglenova J., Birru S., Pandiella N.M., Breese C.R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behavioural Brain Research 2004, 150(1-2):159-170.
58. Vogel-Ciernia A., Matheos D.P., Barrett R.M., Kramar E.A., Azzawi S., Chen Y., et al. The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory. Nature Neuroscience 2013, 16(5):552-561.
59. Wada E., Wada K., Boulter J., Deneris E., Heinemann S., Patrick J., et al. Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: A hybridization histochemical study in the rat. The Journal of Comparative Neurology 1989, 284(2):314-335.
60. Winzer-Serhan U.H., Leslie F.M. Expression of alpha5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development. The Journal of Comparative Neurology 2005, 481(1):19-30.
61. Yamazaki Y., Jia Y., Hamaue N., Sumikawa K. Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. The European Journal of Neuroscience 2005, 22(4):845-860.
62. Yamazaki Y., Jia Y., Niu R., Sumikawa K. Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. The European Journal of Neuroscience 2006, 23(7):1819-1828.
63. Yanai J., Pick C.G., Rogel-Fuchs Y., Zahalka E.A. Alterations in hippocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine. Brain Research Bulletin 1992, 29(3-4):363-368.
64. Zoli M., Le Novere N., Hill J.A., Changeux J.P. Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. The Journal of Neuroscience 1995, 15(3 Pt 1):1912-1939.