Effects of pre-and neonatal nicotine exposure in rodents: Inconsistent evidence

ILAR Journal

Volumn 52, Issue 3, 2011, Pages 251-294

  Sobrian, Sonya K ^a   Robert Holson, R ^b  

^a HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b NEW MEXICO INSTITUTE OF MINING AND TECHNOLOGY   (United States)

Author keywords

Behavioral effect; Cognitive effect; Confound; Developmental exposure; Maternal smoking; Mechanistic consideration; Nicotine; Rodent model

Indexed keywords

NICOTINE;

ANIMAL; HUMAN; LEARNING; MEMORY; PRENATAL EXPOSURE;

ANIMALS; HUMANS; LEARNING; MEMORY; NICOTINE; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84873431669     PISSN: 10842020     EISSN: 19306180     Source Type: Journal    
DOI: 10.1093/ilar.52.3.251     Document Type: Article

References (276)

1. Abdel-Rahman A, Dechkovskaia AM, Sutton JM, Chen W-C, Guan X, Khan WA, Abou-Donia MB. 2005. Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and el-evated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty. Toxicol 209:245-261.
2. Abou-Donia MB, Khan WA, Dechkovskaia AM, Goldstein LB, Bullman SL, Abdel-Rahman A. 2006. In utero exposure to nicotine and chlorpy-rifos alone, and in combination produces persistent sensorimotor defi-cits and Purkinje neuron loss in the cerebellum of adult offspring rats. Arch Toxicol 80:620-631.
3. Abreu-Villaça Y, Seidler FJ, Tate CA, Cousins MM, Slotkin TA. 2004a. Prenatal nicotine exposure alters the response to nicotine administration in adolescence: Effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology 29:879-890.
4. Abreu-Villaça Y, Seidler FJ, Slotkin TA. 2004b. Does prenatal nicotine ex-posure sensitize the brain to nicotine-induced neurotoxicity in adoles-cence? Neuropsychopharmacology 29:1440-1450.
5. Adams AK, Harvey HE, Heather E, Prince RJ. 2005. Association of mater-nal smoking with overweight at age 3 in American Indian children. Am J Clin Nutr 82:393-398.
6. Ajarem JS, Ahmad M. 1998. Prenatal nicotine exposure modifies behavior of mice through early development. Pharmacol Biochem Behav 59:313-318.
7. Alati R, Macleod J, Hickman M, Sayal K, May M, Smith GD, Lawlor DA. 2008. Intrauterine exposure to alcohol and tobacco use and childhood IQ: Findings from a parental-offspring comparison within the Avon Longitudinal Study of Parents and Children. Pediatr Res 64:659-666.
8. Al Mamun A, Lawlor DA, Alati R, O'Callaghan AJ, Michael J, Williams GM, Najman JM. 2006. Does maternal smoking during pregnancy have a di-rect effect on future offspring obesity? Am J Epidemiol 164:317-325.
9. Altman J, Anderson W, Strop M. 1971. Retardation of cerebellar and motor development by focal x-irradiation during infancy. Physiol Behav 7: 143-150.
10. Ankarberg E, Fredriksson A, Eriksson P. 2001. Neurobehavioural defects in adult mice neonatally exposed to nicotine: Changes in nicotine-induced behaviour and maze learning performance. Behav Brain Res 1231: 85-92.
11. Ankarberg E, Fredriksson A, Eriksson P. 2004. Increased susceptibility to adult paraoxon exposure in mice neonatally exposed to nicotine. Toxicol Sci 82:555-561.
12. Baghurst PA, Tong SL, Woodward A, McMichael AJ. 1992. Effects of ma-ternal smoking upon neuropsychological development in early childhood:Importance of taking account of social and environmental factors. Pae-diatr Perinat Epidemiol 6:403-415.
13. Barr GA, McPhie-Lalmansingh A, Perez J, Riley M. 2011. Changing mech-anisms of opiate tolerance and withdrawal during early development: Animal models of the human experience. ILAR J 52:329-341.
14. Batstra L, Hadders-Algra M, Neeleman J. 2003. Effect of antenatal expo-sure to maternal smoking on behavioural problems and academic achievement in childhood: Prospective evidence from a Dutch birth cohort. Early Hum Dev 75:21-33.
15. Batty GD, Der G, Deary IJ. 2006. Effect of maternal smoking during preg-nancy on offspring's cognitive ability: Empirical evidence for complete confounding in the US national longitudinal survey of youth. Pediatrics 118:943-959.
16. Bayer SA, Altman J, Russo RJ, Zhang X. 1993. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicol 14:83-144.
17. Becker RF, King JE, Little CR. 1968. Experimental studies on nicotine ab-sorption during pregnancy. IV. The postmature neonate. Am J Obstet Gynecol 101:109-119.
18. Berger DF, Lombardo JP, Peck JA, Joshua A, Faraone SV, Middleton FA, Youngetob SL. 2010. The effects of strain and prenatal nicotine expo-sure on ethanol consumption by adolescent male and female rats. Behav Brain Res 210:147-154.
19. Bertolini A, Bernardi M, Genedani S. 1982. Effects of prenatal exposure to cigarette smoke and nicotine on pregnancy, offspring development and avoidance behavior in rats. Neurobehav Toxicol Teratol 4:545-548.
20. Bhat RV, Turner SL, Selvaag SR, Marks MJ, Collins MC. 1991. Regulation of brain nicotinic receptors by chronic agonist infusion. J Neurochem 56:1932-1939.
21. Biederman J, Monuteaux MC, Faraone SV, Mick E. 2009. Parsing the associations between prenatal exposure to nicotine and offspring psychopathology in a nonreferred sample. J Adolesc Health 45: 142-148.
22. Blake KV, Gurrin LC, Evans SF, Beilin LJ, Landau LI, Stanley FJ, Newn-ham JP. 2000. Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev 57:137-147.
23. Bloch M, Althabe F, Onyamboko M, Kaseba-Sata C, Castilla EE, Freire S, Garces AL, Parida S, Shivaprasad S, Goudar SS, Kadir MM, Goco N, Thornberry J, Daniels M, Bartz J, Hartwell T, Moss N, Goldenberg R. 2008. Tobacco use and secondhand smoke exposure during pregnancy: An investigative survey of women in 9 developing nations. Am J Public Health 98:1833-1840.
24. Boutwell BB, Beaver KM. 2010. Maternal cigarette smoking during pregnancy and offspring externalizing behavioral problems: A pro-pensity score matching analysis. Int J Environ Res Public Health 7:146-163.
25. Boyd ND. 1987. Two distinct kinetic phases of desensitization of acetylcho-line receptors of clonal rat PC12 cells. J Physiol 389:45-67.
26. Braun JM, Kahn RS, Froehlich T, Auinger P, Lanphear BP. 2006. Exposures to environmental toxicants and attention deficit hyperactivity disorder in US children. Environ Health Perspect 114:1904-1909.
27. Braun JM, Froehlich TE, Daniels JL, Dietrich KN, Hornung R, Auinger P, Lanphear BP. 2008. Association of environmental toxicants and conduct disorder in US children: NHANES 2001-2004. Environ Health Perspect 116:956-962.
28. Brennan PA, Grekin ER, Mednick SA. 1999. Maternal smoking during pregnancy and adult male criminal outcomes. Arch Gen Psychiatry 56:215-219.
29. Breslau N, Paneth N, Lucian VC, Paneth-Pollak R. 2005. Maternal smoking during pregnancy and offspring IQ. Int J Epidemiol 34:1047-1053.
30. Britton GR, Brinthaupt J, Stehle JM, James GD. 2004. Comparison of self-reported smoking and urinary cotinine levels in a rural pregnant popula-tion. J Obstet Gynecol Neonatal Nurs 33:306-311.
31. Bruin JE, Gerstein HC, Holloway AC. 2010. Long-term consequences of fetal and neonatal nicotine exposure: A critical review. Toxicol Sci 116:364-374.
32. Buka SL, Shenassa ED, Niaura R. 2003. Elevated risk of tobacco depen-dence among offspring of mothers who smoked during pregnancy: A 30-year prospective study. Am J Psychiatry 160:1978-1984.
33. Butler NR, Goldstein H. 1973. Smoking in pregnancy and subsequent child development. Br Med J 4:573-575.
34. Campbell BA, Lynch GS. 1969. Cortical modulation of spontaneous activ-ity during hunger and thirst. J Comp Physiol Psychol 67:15-22.
35. Carmines EL, Gaworski CL, Faqi AS, Rajendran N. 2003. In utero exposure to 1R4F reference cigarette smoke: Evaluation of developmental toxic-ity. Toxicol Sci 75:134-147.
36. CDC [Centers for Disease Control and Prevention]. 2004. Smoking during pregnancy: United States, 1990-2002. MMWR Morb Mortal Wkly Rep 53:911-915.
37. CDC. 2009a. Births: Final Data for 2007. National Vital Statistics Reports 58 #24.
38. CDC. 2009b. Trends in Smoking Before, During and After Pregnancy: Pregnancy Risk Assessment Monitoring System (PRAMS), United States, 31 Sites, 2000-2005. MMWR CDC Surveill Summ 58:1-31.
39. Chen H, Parker SL, Matta SG, Sharp BM. 2005. Gestational nicotine expo-sure reduces nicotinic cholinergic receptor (nAChR) expression in dop-aminergic brain regions of adolescent rats. Eur J Neurosci 22:380-388.
40. Chen A, Pennell ML, Klebanoff MA, Rogan WJ, Longnecker MP. 2006. Maternal smoking during pregnancy in relation to child overweight: Follow-up to age 8 years. Int J Epidemiol 35:121-130.
41. Chistyakov V, Patkina N, Tammimaki A, Talka R, Salminen O, Belozert-seva I, Galankin T, Tuominen R, Zvartau E. 2010. Nicotine exposure throughout early development promotes nicotine self-administration in adolescent mice and induces long-lasting behavioural changes. Eur J Pharmacol 640:87-93.
42. Clancy B, Finlay BL, Darlington RB, Anand KJ. 2007. Extrapolating brain development from experimental species to humans. Neurotoxicol 28:931-937.
43. Cnattingius S. 2004. The epidemiology of smoking during pregnancy: Smoking prevalence, maternal characteristics and pregnancy outcome. Nic Tobacco Res 6 suppl 2:S125-S140.
44. Cornelius MD, Leech SL, Goldschmidt L, Day N. 2005. Is prenatal tobacco exposure a risk factor for early adolescent smoking? A follow-up study. Neurotoxicol Teratol 27:667-676.
45. Cutler AR, Wilkerson AE, Gingras JL, Levin ED. 1996. Prenatal cocaine and/or nicotine exposure in rats: preliminary findings on long-term cog-nitive outcome and genital development at birth. Neurotoxicol Teratol 18:635-643.
46. Denenberg VH. 1969. Open-field behavior in the rat: What does it mean? Ann N Y Acad Sci 159:852-859.
47. Denson R, Nanson JL, McWatters MA. 1975. Hyperkinesis and maternal smoking. Can Psychiatr Assoc J 20:183-187.
48. De Sarno P, Giacobini E. 1989. Modulation of acetylcholine release by nicotinic receptors in the rat brain. J Neurosci Res 22:194-200.
49. DHHS [US Department of Health and Human Services]. 2001. Patterns of tobacco use among women and girls. In: Women and Smoking: A Re-port of the Surgeon General. Rockville MD.
50. Dobbing J. 1971. Undernutrition and the developing brain: The use of ani-mal models to elucidate the human problem. Psychiatr Neurol Neuro-chir 74:433-442.
51. Dobbing J, Sands J. 1979. Comparative aspects of the brain growth spurt. Early Hum Dev 3:79-83.
52. Dombrowski SC, Martin RP, Huttunen MO. 2005. Gestational exposure to cigarette smoke imperils the long-term physical and mental health of offspring. Birth Defects Res A Clin Mol Teratol 73:170-176.
53. D'Onofrio BM, Van Hulle CA, Waldman ID, Rodgers JLK, Paige RZ, Paul JL, Benjamin B. 2008. Smoking during pregnancy and offspring exter-nalizing problems: An exploration of genetic and environmental con-founds. Dev Psychopathol 20:139-164.
54. Dörner G, Geier T, Ahrens L, Krell L, Münx G, Sieler H, Kittner E, Müller H. 1980. Prenatal stress as possible aetiogenetic factor of homosexuality in human males. Endokrinologie 75:365-368.
55. Dubois L, Girard M. 2006. Early determinants of overweight at 4.5 years in a population-based longitudinal study. Int J Obes 30:610-617.
56. Duncan JR, Garland M, Myers MM, Fifer WP, Yang M, Kinney HC, Stark RI. 2009. Prenatal nicotine-exposure alters fetal autonomic activity and medullary neurotransmitter receptors: Implications for sudden infant death syndrome. J Appl Physiol 107:1579-1590.
57. Dunn HG, McBurney AK, Ingram S, Hunter CM. 1976. Maternal cigarette smoking during pregnancy and the child's subsequent development. I. Physical growth to the age of 61/2 years. Can J Public Health 67:499-505.
58. Dwyer JB, McQuown SC, Leslie FM. 2009. The dynamic effects of nico-tine on the developing brain. Pharmacol Ther 122:125-139.
59. Ekblad M, Gissler M, Lehtonen L, Korkeila J. 2010. Prenatal smoking ex-posure and the risk of psychiatric morbidity into young adulthood. Arch Gen Psychiatry 67:841-849.
60. Ellis L, Cole-Harding S. 2001. The effects of prenatal stress, and of prenatal alcohol and nicotine exposure, on human sexual orientation. Physiol Behav 74:213-226.
61. Eppolito AK, Smith RF. 2006. Long-term behavioral and developmental consequences of pre-and perinatal nicotine. Pharmacol Biochem Behav 85:835-841.
62. Eppolito AK, Bachus SE, McDonald CG, Meador-Woodruff JH, Smith RF. 2010. Late emerging effects of prenatal and early postnatal nicotine ex-posure on the cholinergic system and anxiety-like behavior. Neurotoxi-col Teratol 32:336-345.
63. Eriksson P, Ankarberg E, Fredriksson A. 2000. Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nico-tinic receptors and in behaviour of adult mice. Brain Res 853:41-48.
64. Ernst M, Moolchan ET, Robinson ML. 2001. Behavioral and neural conse-quences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psy-chiatry 40:630-641.
65. Eskenazi B, Castorina R. 1999. Association of prenatal maternal or postna-tal child environmental tobacco smoke exposure and neurodevelopmen-tal and behavioral problems in children. Environ Health Perspect 10:991-1000.
66. Fenster CP, Rains MF, Noerager B. 1997. Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentra-tions of nicotine. J Neurosci 17:5747-5759.
67. Fergusson DM, Lloyd M. 1991. Smoking during pregnancy and its effects on child cognitive ability from the ages of 8 to 12 years. Paediatr Perinat Epidemiol 5:189-200.
68. Fergusson DM, Horwood LJ, Shannon FT. 1979. Smoking during preg-nancy. N Z Med J 89:41-43.
69. Fergusson DM, Woodward LJ, Horwood LJ. 1998. Maternal smoking dur-ing pregnancy and psychiatric adjustment in late adolescence. Arch Gen Psychiatry 55:721-727.
70. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ. 1992. A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41:31-37.
71. Fogelman K. 1980. Smoking in pregnancy and subsequent development of the child. Child Care Health Dev 6:233-249.
72. Fogelman KR, Manor O. 1988. Smoking in pregnancy and development into early adulthood. BMJ 297:1233-1236.
73. Ford RPK, Tappin DM, Schluter PJ, Wild CJ. 1996. Smoking during preg-nancy: How reliable are maternal self-reports in New Zealand? J Epide-miol Community Health 57:246-251.
74. Franke RM, Belluzzi JD, Leslie FM. 2007. Gestational exposure to nico-tine and monoamine oxidase inhibitors influences cocaine-induced locomotion in adolescent rats. Psychopharmacology (Berl) 195:117-124.
75. Franke RM, Park M, Belluzzi JD, Leslie FM. 2008. Prenatal nicotine expo-sure changes natural and drug-induced reinforcement in adolescent male rats. Eur J Neurosci 27:2952-2961.
76. Fredriksson A, Eriksson P, Ankarberg E, Palomo T, Archer T. 2000. Neona-tal nicotine administration influences ethanol-induced behaviors. Alco-hol 21:107-115.
77. Fried PA, Watkinson B. 1990. 36-and 48-month neurobehavioral follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol. J Dev Behav Pediatr 11:49-58.
78. Fried PA, Watkinson B. 2000. Visuoperceptual functioning differs in 9-to 12-year olds prenatally exposed to cigarettes and marihuana. Neuro-toxicol Teratol 22:11-20.
79. Fried PA, O'Connell CM, Watkinson B. 1992. 60-and 72-month follow-up of children prenatally exposed to marijuana, cigarettes, and alcohol: Cognitive and language assessment. J Dev Behav Pediatr 13:383-391.
80. Fried PA, Watkinson B, Siegel LS. 1997. Reading and language in 9-to 12-year olds prenatally exposed to cigarettes and marijuana. Neurotoxi-col Teratol 19:171-183.
81. Fried PA, Watkinson B, Gray R. 1998. Differential effects on cognitive functioning in 9-to 12-year olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 20:293-306.
82. Fried PA, James DS, Watkinson B. 1999. Growth from birth to early adoles-cence in offspring prenatally exposed to cigarettes and marijuana. Neu-rotoxicol Teratol 21:513-525.
83. Fried PA, James DS, Watkinson B. 2001. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 23:431-436.
84. Fried PA, Watkinson B, Gray R. 2003. Differential effects on cognitive functioning in 13-to 16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 25:427-436.
85. Frischer RE, King JA, Rose KJ, Strand FL. 1988. Maturational changes in neonatal rat motor system with early postnatal administration of nico-tine. Int J Dev Neurosci 6:149-154.
86. Fung YK. 1988. Postnatal behavioural effects of maternal nicotine exposure in rats. J Pharm Pharmacol 40:870-872.
87. Fung YK. 1989. Postnatal effects of maternal nicotine exposure on the stri-atal dopaminergic system in rats. J Pharm Pharmacol 41:576-578.
88. Gatzke-Kopp LM, Beauchaine TP. 2007. Direct and passive prenatal nico-tine exposure and the development of externalizing psychopathology. Child Psychiatry Hum Dev 38:255-269.
89. Gaworski CL, Carmines EL, Faqi AS, Rajendran N. 2004. In utero and lactation exposure of rats to 1R4F reference cigarette mainstream smoke: Effect on prenatal and postnatal development. Toxicol Sci 79:157-169.
90. Genedani S, Bernardi M, Bertolini A. 1983. Sex-linked differences in avoid-ance learning in the offspring of rats treated with nicotine during preg-nancy. Psychopharmacology (Berl) 80:93-95.
91. Gilbertson RJ, Barron S. 2005. Neonatal ethanol and nicotine exposure causes locomotor activity changes in preweanling animals. Pharmacol Biochem Behav 81:54-64.
92. Gilman SE, Gardener H, Buka SL. 2008. Maternal smoking during preg-nancy and children's cognitive and physical development: A causal risk factor? Amer J Epidemiol 168:522-531.
93. Girard TA, Xing HC, Ward GR, Nguyen H, Wainwright PE. 2001. Exposure to ethanol and nicotine during the brain growth spurt: Spatial DMP per-formance in male rats. Pharmacol Biochem Behav 68:515-523.
94. Gold AB, Keller AB, Perry DC. 2009. Prenatal exposure of rats to nicotine causes persistent alterations of nicotinic cholinergic receptors. Brain Res 1250:88-100.
95. Gospe SM, Zhou SS, Pinkerton KE. 1996. Effects of environmental tobacco smoke exposure in utero and/or postnatally on brain development. Pedi-atric Res 39:494-498.
96. Govind AP, Vezina P, Green WN. 2009. Nicotine-induced upregulation of nicotinic receptors: Underlying mechanisms and relevance to nicotine addiction. Biochem Pharmacol 78:756-765.
97. Gyekis J, Forman JE, Anthony K, Klein LC, Vandenbergh DJ. 2010a. Activity-related behaviors in the hole-board predict nicotine consump-tion in C57B6 mice perinatally exposed to nicotine. Behav Brain Res 206:139-142.
98. Gyekis J, Anthony K, Foreman JE, Klein LC, Vandenbergh DJ. 2010b. Perinatal nicotine exposure delays genital development in mice. Reprod Toxicol 29:378-380.
99. Haddow JE, Knight GJ, Palomaki GE, Kloza EM, Wald NJ. 1987. Cigarette consumption and serum cotinine in relation to birthweight. Br J Obstet Gynaecol 94:678-681.
100. Hamosh M, Simon MR, Hamosh P. 1979. Effects of nicotine on the devel-opment of fetal and suckling rats. Biol Neonate 35:290-297.
101. Haug K, Irgens LM, Skjaerve, R, Markestad T, Baste V, Schreuder P. 2000. Maternal smoking and birthweight: Effect modification of period, ma-ternal age and paternal smoking. Acta Obstet Gynecol Scand 79:485-489.
102. Hill SY, Lowers L, Locke-Wellman J, Shen SA. 2000. Maternal smoking and drinking during pregnancy and the risk for child and adolescent psychiatric disorders. J Stud Alcohol 61:661-668.
103. Hill SY, Shen S, Locke Wellman J, Rickin E, Lowers L. 2005. Offspring from families at high risk for alcohol dependence: Increased body mass index in association with prenatal exposure to cigarettes but not alcohol. Psychiatry Res 135:203-216.
104. Holloway AC, Lim GE, Petrik JJ, Foster WG, Morrison KM, Gerstein HC. 2005. Fetal and neonatal exposure to nicotine in Wistar rats results in in-creased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes. Diabetologia 48:2661-2666.
105. Holmes A, le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C. 2005. Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci Biobehav Rev 29:1335-1346.
106. Holson RR, Freshwater L, Maurissen JP, Moser VC, Phang W. 2008. Statis-tical issues and techniques appropriate for developmental neurotoxicity testing: A report from the ILSI Research Foundation/Risk Science Insti-tute expert working group on neurodevelopmental endpoints. Neuro-toxicol Teratol 30:326-348.
107. Holson RR, Pearce B. 1992. Principles and pitfalls in the analysis of prena-tal treatment effects in multiparous species. Neurotoxicol Teratol 14:221-228.
108. Huang LZ, Hsiao SH, Trzeciakowski J, Frye GD, Winzer-Serham UH. 2006. Chronic nicotine induces growth retardation in neonatal rat pups. Life Sci 78:1483-1493.
109. Huang LPZ, Liu XH, Griffith WH, Winzer-Serhan UH. 2007. Chronic neo-natal nicotine increases anxiety but does not impair cognition in adult rats. Beh Neurosci 121:1342-1352.
110. Huijbregts SCJ, Seguin JR, Zoccolillo M, Boivin M, Tremblay RE. 2007. Associations of maternal prenatal smoking with early childhood physi-cal aggression, hyperactivity-impulsivity, and their co-occurrence. J Abnorm Child Psychol 35:203-215.
111. Indredavik MS, Brubakk A-M, Romundstad P, Vik T. 2007. Prenatal smok-ing exposure and psychiatric symptoms in adolescence. Acta Paediatr 96:377-382.
112. Jaddoe VWV, Verburg BO, de Ridder MAJ, Hofman A, Mackenbach JP, Moll HA, Steegers EAP, Witteman JCM. 2007. Maternal smoking and fetal growth characteristics in different periods of pregnancy: The Gen-eration R Study. Am J Epidemiol 165:1207-1215.
113. Johns JM, Louis TM, Becker RF, Means LW. 1982. Behavioral effects of prenatal exposure to nicotine in guinea pigs. Neurobehav Toxicol Tera-tol 4:365-369.
114. Johns JM, Walters PA, Zimmerman LI. 1993. The effects of chronic prena-tal exposure to nicotine on the behavior of guinea pigs (Cavia porcel-lus). J Gen Psychol 120:49-63.
115. Jones KL, Hoyme HE, Robinson LK, Del Campo M, Manning MA, Prewitt LM, Chambers CD. 2010 Fetal alcohol spectrum disorders: Extending the range of structural defects. Am J Med Genet A 152A:2731-2735.
116. Kallen K. 2000. Maternal smoking during pregnancy and infant head cir-cumference at birth. Early Hum Dev 58:197-204.
117. Kandel DB, Udry JR. 1999. Prenatal effects of maternal smoking on daugh-ters' smoking: Nicotine or testosterone exposure? Am J Public Health 89:1377-1383.
118. Kandel DB, Wu P, Davies M. 1994. Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health 84:1407-1413.
119. Kardia SLR, Pomerleau CS, Rozek LS, Marks JL. 2003. Association of parental smoking history with nicotine dependence, smoking rate, and psychological cofactors in adult smokers. Addict Behav 28:1447-1452.
120. King JA, Strand FL. 1988. Is nicotine depression of neonatal motor behav-ior exerted through ACTH release? Peptides 9 Suppl 1:39-44.
121. Klein LC, Stine MM, Pfaff DW, Vandenbergh DJ. 2003. Maternal nicotine exposure increases nicotine preference in periadolescent male but not female C57B1/6J mice. Nicotine Tob Res 5:117-124.
122. Knopik VS, Sparrow EP, Madden PAF, Bucholz KK, Hudziak JJ, Reich W, Slutske WS, Grant JD, McLaughlin TL, Todorov A, Todd RD, Heath AC. 2005. Contributions of parental alcoholism, prenatal substance ex-posure, and genetic transmission to child ADHD risk: A female twin study. Psychol Med 35:625-635.
123. Koren G. 1999. The association between maternal cigarette smoking and psy-chiatric diseases or criminal outcome in the offspring: A precautionary note about the assumption of causation. Reprod Toxicol 13:345-346.
124. Kotimaa AJ, Moilanen I, Taanila A, Ebeling F, Smalley SL, McGough JJ, Hartikainen AL, Jarvelin MR. 2003. Maternal smoking and hyperactiv-ity in 8-year-old children. J Amer Acad Child Adolescent Psychiat 42:826-833.
125. Kramer MS. 1987. Determinants of low birth weight: Methodological as-sessment and meta-analysis. Bull WHO 65:663-737.
126. Lambe M, Hultman C, Torranga A, Maccabe J, Cnattingius S. 2006. Mater-nal smoking during pregnancy and school performance at age 15. Epi-demiol 17:524-530.
127. Lample M, Kuzawa CM, Jeanty P. 2003. Prenatal smoke exposure alters growth in limb proportions and head shape in the midgestational human fetus. Am J Hum Biol 15:533-546.
128. Langley K, Holmans PA, van den Bree MBM, Thapar A. 2007. Effects of low birth weight, maternal smoking in pregnancy and social class on the phenotypic manifestation of Attention Deficit Hyperactivity Disorder and associated antisocial behaviour: Investigation in a clinical sample. BMC Psychiatry 7 Article No. 26.
129. Leary SD, Smith GD, Rogers IS, Reilly JJ, Wells JC, Ness AR. 2006. Smok-ing during pregnancy and offspring fat and lean mass in childhood. Obe-sity 14:2284-2293.
130. LeSage MG, Gustaf E, Dufek MB, Pentel PR. 2006. Effects of maternal intravenous nicotine administration on locomotor behavior in pre-weanling rats. Pharmacol Biochem Behav 85:575-583.
131. Lester RA, Dani JA. 1995. Acetylcholine receptor desensitization induced by nicotine in rat medial habenula neurons. J Neurophysiol 74:195-206.
132. Levin ED. 2005. Fetal nicotinic overload, blunted sympathetic responsivity and obesity. Birth Defects Res A Clin Mol Teratol 73:481-484.
133. Levin ED, Briggs SJ, Christopher NC, Rose JE. 1993. Prenatal nicotine exposure and cognitive performance in rats. Neurotoxicol Teratol 15:251-260.
134. Levin ED, Wilkerson A, Jones JP, Christopher NC, Briggs SJ. 1996. Prena-tal nicotine effects on memory in rats: Pharmacological and behavioral challenges. Brain Res Dev Brain Res 97:207-215.
135. Levin ED, Lawrence S, Petro A, Horton K, Seidler FJ, Slotkin TA. 2006. Increased nicotine self-administration following prenatal exposure in female rats. Pharmacol Biochem Behav 85:669-674.
136. Liang K, Poytress BS, Chen Y, Leslie FM, Weinberger NM, Metherate R. 2006. Neonatal nicotine exposure impairs nicotinic enhancement of central auditory processing and auditory learning in adult rats. Eur J Neurosci 24:857-866.
137. Lichtensteiger W, Schlumpf M. 1985. Prenatal nicotine affects fetal testos-terone and sexual dimorphism of saccharin preference. Pharmacol Bio-chem Behav 23:439-444.
138. Lichtensteiger W, Ribary U, Schlumpf M, Odermatt B, Widmer HR. 1988. Prenatal adverse effects of nicotine on the developing brain. Prog Brain Res 73:137-157.
139. Lindblad F, Hjern A. 2010. ADHD after fetal exposure to maternal smoking. Nicotine Tob Res 12:408-415.
140. Luck W, Nau H, Hansen R, Steldinger R. 1985. Extent of nicotine and coti-nine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol 8:384-395.
141. MacArthur C, Knox EG, Lancashire RJ. 2001. Effects at age nine of mater-nal smoking in pregnancy: Experimental and observational findings. BJOG 108:67-73.
142. Macphail RC, Farmer JD, Jarema KA, Chernoff N. 2005. Nicotine effects on the activity of mice exposed prenatally to the nicotinic agonist anatoxin-a. Neurotoxicol Teratol 27:593-598.
143. Makin J, Fried PA, Watkinson B. 1991. A comparison of active and passive smoking during pregnancy: Long-term effects. Neurotoxicol Teratol 13:5-12.
144. Marks MJ, Grady SR, Collins AC. 1993. Downregulation of nicotinic re-ceptor function after chronic nicotine infusion. J Pharmacol Exp Ther 266:1268-1276.
145. Marks MJ, Meinerz NM, Brown RW, Collins AC. 2010. 86Rb+ efflux medi-ated by alpha4beta2*-nicotinic acetylcholine receptors with high and low-sensitivity to stimulation by acetylcholine display similar agonist-induced desensitization. Biochem Pharmacol 80:1238-1251.
146. Martin JC, Becker RF. 1971. The effects of maternal nicotine absorption or hypoxic episodes upon appetitive behavior of rat offspring. Dev Psycho-biol 4:133-147.
147. Martin JC, Martin DC. 1981. Voluntary activity in the aging rat as a function of maternal drug exposure. Neurobehav Toxicol Teratol 3:261-264.
148. Martin JC, Martin DC, Radow B, Radow G. 1976. Growth, development and activity in rat offspring following maternal drug exposure. Exper Aging Res 2:235-251.
149. Martin JC, Martin DC, Lund CA, Streissguth AP. 1977. Maternal alcohol ingestion and cigarette smoking and their effects on newborn condition-ing. Alcohol Clin Exp Res 1:243-247.
150. Matsubara F, Kida M, Tamakoshi A, Wakai K, Kawamura T, Ohno Y. 2000. Maternal active and passive smoking and fetal growth: A prospective study in Nagoya, Japan. J Epidemiol 10:335-343.
151. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM. 2007. Guidelines on nicotine dose selection for in vivo research. Psychopharmocology 190:269-319.
152. Maughan B, Taylor C, Taylor A, Butler N, Bynner J. 2001. Pregnancy smoking and childhood conduct problems: A causal association? J Child Psychol Psychiatry 42:1021-1028.
153. McCartney JS, Fried PA, Watkinson B. 1994. Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxi-col Teratol 16:269-276.
154. McFarland BJ, Seidler FJ, Slotkin TA. 1991. Inhibition of DNA synthesis in neonatal rat brain regions caused by acute nicotine administration. Brain Res Dev Brain Res 58:223-229.
155. McGee R, Stanton WR. 1994. Smoking in pregnancy and child develop-ment to age 9 years. J Paediatr Child Health 30:263-268.
156. Meyer DC, Carr LA. 1987. The effects of perinatal exposure to nicotine on plasma LH levels in prepubertal rats. Neurotoxicol Teratol 9:95-98.
157. Miao H, Liu C, Bishop K, Gong ZH, Nordberg A, Zhang X. 1998. Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain. J Neuro-chem 70:752-762.
158. Mick E, Biederman J, Faraone SV, Sayer J, Kleinman S. 2002. Case-control study of attention-deficit hyperactivity disorder and maternal smoking, alcohol use, and drug use during pregnancy. J Am Acad Child Adolesc Psychiatry 41:378-385.
159. Milberger S, Biederman J, Faraone SV, Chen L, Jones J. 1996. Is maternal smoking during pregnancy a risk factor for attention deficit hyperactiv-ity disorder in children? Am J Psychiatry 153:1138-1142.
160. Milberger S, Biederman J, Faraone SV, Jones J. 1998. Further evidence of an association between maternal smoking during pregnancy and atten-tion deficit hyperactivity disorder: Findings from a high-risk sample of siblings. J Clin Child Psychol 27:352-358.
161. Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ. 2007. Maternal separation alters drug intake patterns in adulthood in rats. Bio-chem Pharmacol 73:321-330.
162. Moretti M, Mugnaini M, Tessari M, Zoli M, Gaimarri A, Manfredi I, Pistillo F, Clementi F, Gotti C. 2010. A comparative study of the effects of the intravenous self-administration or subcutaneous minipump infusion of nicotine on the expression of brain neuronal nicotinic receptor subtypes. Mol Pharmacol 78:287-296.
163. Mortensen EL, Michaelsen KF, Sanders SA, Reinisch JM. 2005. A dose-response relationship between maternal smoking during late pregnancy and adult intelligence in male offspring. Paediatric Perinatal Epidemiol 19:4-11.
164. Murrin LC, Ferrer JR, Wanyun Z, Haley NJ. 1987. Nicotine administration to rats: Methodological considerations. Life Sci 40:1699-1708.
165. Naeye RL, Peters EC. 1984. Mental development of children whose moth-ers smoked during pregnancy. Obstet Gynecol 64:601-607.
166. Nasrat HA, Al-Hachim GM, Mahmood FA. 1986. Perinatal effects of nico-tine. Biol Neonate 49:8-14.
167. Navarro HA, Seidler FJ, Whitmore WL, Slotkin TA. 1988. Prenatal expo-sure to nicotine via maternal infusions: Effects on development of cat-echolamine systems. J Pharmacol Exp Ther 244:940-944.
168. Navarro HA, Seidler, FJ, Eylers JP, Baker, FE, Dobbins, SS, Lappi, SE, Slotkin TA. 1989a. Effects of prenatal nicotine exposure on develop-ment of central and peripheral cholinergic neurotransmitter systems: Evidence for cholinergic trophic influences in developing brain. Phar-macol Exp Ther 251:894-900.
169. Navarro HA, Seidler FJ, Schwartz RD, Baker FE, Dobbins SS, Slotkin TA. 1989b. Prenatal exposure to nicotine impairs nervous system develop-ment at a dose which does not affect viability or growth. Brain Res Bull 23:187-192.
170. Navarro HA, Mills E, Seidler FJ, Baker FE, Lappi SE, Tayyeb MI, Spencer JR, Slotkin TA. 1990. Prenatal nicotine exposure impairs beta-adrenergic function: Persistent chronotropic subsensitivity despite recovery from deficits in receptor binding. Brain Res Bull 25:233-237.
171. Newman MB, Shytle RD, Sanberg PR. 1999. Locomotor behavioral effects of prenatal and postnatal nicotine exposure in rat offspring. Behav Phar-macol 10:699-706.
172. Niaura R, Bock B, Lloyd EE, Brown R, Lipsitt LP, Buka S. 2001. Maternal transmission of nicotine dependence: Psychiatric, neurocognitive and prenatal factors. Am J Addict 10:16-29.
173. Niemela A, Jarvenpaa AL. 1996. Is breastfeeding beneficial and maternal smoking harmful to the cognitive development of children? Acta Pae-diatr 85:1202-1206.
174. Nordberg A, Zhang XA, Fredriksson A, Eriksson P. 1991. Neonatal nicotine exposure induces permanent changes in brain nicotinic receptors and behaviour in adult mice. Brain Res Dev Brain Res 63:201-207.
175. O'Callaghan FV, Al Mamun A, O'Callaghan M, Alati R, Williams GM, Najman JM. 2006. Is smoking in pregnancy an independent predictor of academic difficulties at 14 years of age? A birth cohort study. Early Hum Dev 86:71-76.
176. O'Callaghan FV, Al Mamun A, O'Callaghan M, Alati R, Najman JM, Williams GM, Bor W. 2009. Maternal smoking during pregnancy pre-dicts nicotine disorder (dependence or withdrawal) in young adults: A birth cohort study. Aust N Z J Public Health 33:371-377.
177. Ochoa EL, Li L, McNamee MG. 1990. Desensitization of central cholin-ergic mechanisms and neuroadaptation to nicotine. Mol Neurobiol 4:251-287.
178. Oken E, Huh SY, Taveras EM, Rich-Edwards JW, Gillman MW. 2005. As-sociations of maternal prenatal smoking with child adiposity and blood pressure. Obes Res 13:2021-2028.
179. Olds DL, Henderson CR Jr, Tatelbaum R. 1994a. Intellectual impairment in children of women who smoke cigarettes during pregnancy. Pediatrics 93:221-227.
180. Olds DL, Henderson CR Jr, Tatelbaum R. 1994b. Prevention of intellectual impairment in children of women who smoke cigarettes during preg-nancy. Pediatrics 93:228-233.
181. Oncken CA, Hardardottir H, Hatsukami DK, Lupo VR, Rodis JF, Smeltzer JS. 1997. Effects of transdermal nicotine or smoking on nicotine concen-trations and maternal-fetal hemodynamics. Obstet Gynecol 90:569-574.
182. Ortells MO, Barrantes GE. 2010. Tobacco addiction: A biochemical model of nicotine dependence. Med Hypotheses 74:884-894.
183. Papke RL, Kem WR, Soti F. 2009. Activation and desensitization of nico-tinic alpha7-type acetlycholine receptors by benzylidene anabaseines and nicotine. J Pharmacol Exp Ther 329:791-807.
184. Paulson RB, Shanfeld J, Vorhees CV, Sweazy A, Gagni S, Smith AR, Paulson JO. 1993. Behavioral effects of prenatally administered smoke-less tobacco on rat offspring. Neurotoxicol Teratol 15:183-192.
185. Paulson RB, Shanfeld J, Vorhees CV, Cole J, Sweazy A, Paulson JO. 1994. Behavioral effects of smokeless tobacco on the neonate and young Sprague Dawley rat. Teratology 49:293-305.
186. Pauly JR, Sparks JA, Hauser KF, Pauly TH. 2004. In utero nicotine exposure causes persistent, gender-dependant changes in locomotor activity and sensitivity to nicotine in C57Bl/6 mice. Int J Dev Neurosci 22:329-337.
187. Paz R, Barsness B, Martenson T, Tanner D, Allan AM. 2007. Behavioral teratogenicity induced by nonforced maternal nicotine consumption. Neuropsychopharmacology 32:693-699.
188. Peters DA. 1984. Prenatal nicotine exposure increases adrenergic receptor binding in the rat cerebral cortex. Res Commun Chem Pathol Pharmacol 46:307-317.
189. Peters DA, Tang S. 1982. Sex-dependent biological changes following prenatal nicotine exposure in the rat. Pharmacol Biochem Behav 17:1077-1082.
190. Peters DA, Taub H, Tang S. 1979. Postnatal effects of maternal nicotine exposure. Neurobehav Toxicol 1:221-225.
191. Peters MA, Ngan LL. 1982. The effects of totigestational exposure to nico-tine on pre-and postnatal development in the rat. Arch Int Pharmacodyn Ther 257:155-167.
192. Porath AJ, Fried PA. 2005. Effects of prenatal cigarette and marijuana expo-sure on drug use among offspring. Neurotoxicol Teratol 27:267-277.
193. Qiao D, Seidler FJ, Violin JD, Slotkin TA. 2003. Nicotine is a developmen-tal neurotoxicant and neuroprotectant: Stage-selective inhibition of DNA synthesis coincident with shielding from effects of chlorpyrifos. Brain Res Dev Brain Res 147:183-190.
194. Quinn R. 2005. Comparing rat's to human's age: How old is my rat in people years? Nutrition 21:775-777.
195. Rantakallio P. 1983. A follow-up study up to the age of 14 of children whose mothers smoked during pregnancy. Acta Paediatr Scand 72:747-53.
196. Rantakallio P, Laara E, Isohanni M, Moilanen I. 1992. Maternal smoking during pregnancy and delinquency of the offspring: An association without causation? Int J Epidemiol 21:1106-1113.
197. Richardson SA, Tizabi Y. 1994. Hyperactivity in the offspring of nicotine-treated rats: Role of the mesolimbic and nigrostriatal dopamin-ergic pathways. Pharmacol Biochem Behav 47:331-337.
198. Roberts KH, Munafo MR, Rodriguez D, Drury M, Murphy MFG, Neale RE, Nettle D. 2005. Longitudinal analysis of the effect of prenatal nico-tine exposure on subsequent smoking behavior of offspring. Nicotine Tob Res 7:801-808.
199. Romero RD, Chen W-JA. 2004. Gender-related response in open-field ac-tivity following developmental nicotine exposure in rats. Pharmacol Biochem Behav 78:675-681.
200. Roy TS, Sabherwal U. 1994. Effects of prenatal nicotine exposure on the mor-phogenesis of somatosensory cortex. Neurotoxicol Teratol 16:411-421.
201. Roy TS, Sabherwal U. 1998. Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol 20:465-473.
202. Roy TS, Andrews JE, Seidler FJ, Slotkin TA. 1998. Nicotine evokes cell death in embryonic rat brain during neurulation. J Pharmacol Exp Ther 287:1136-1144.
203. Roy TS, Seidler FJ, Slotkin TA. 2002. Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300:124-133.
204. Roza SJ, Verburg BO, Jaddoe VWV, Hofman A, Mackenbach JP, Steegers EAP, Witteman JCM, Verhulst FC, Tiemeier H. 2007. Effects of mater-nal smoking in pregnancy on prenatal brain development: The Genera-tion R Study. Eur J Neurosci 25:611-617.
205. Roza SJ, Verhulst FC, Jaddoe VWV, Steegers EAP, Mackenbach JP, Hofman A, Tiemeier H. 2009. Maternal smoking during pregnancy and child behaviour problems: The Generation R Study. Int J Epidemiol 38:680-689.
206. Sanderson EM, Drasdo AL, McCrea K, Wonnacott S. 1993. Upregulation of nicotinic receptors following continuous infusion of nicotine is brain-region-specific. Brain Res 617:349-352.
207. Sarasin A, Schlumpf M, Muller M, Fleischmann I, Lauber ME, Lichtensteiger W. 2003. Adrenal-mediated rather than direct effects of nicotine as a basis of altered sex steroid synthesis in fetal and neonatal rat. Reprod Toxicol 17:153-162.
208. Schlumpf M, Gahwiler M, Ribary U, Lichtensteiger W. 1988. A new device for monitoring early motor development: Prenatal nicotine-induced changes. Pharmacol Biochem Behav 30:199-203.
209. Schneider T, Bizarro L, Asherson PJE, Stolerman IP. 2010. Gestational ex-posure to nicotine in drinking water: Teratogenic effects and method-ological issues. Behav Pharmacol 21:206-216.
210. Segarra AC, Strand FL. 1989. Perinatal administration of nicotine alters subsequent sexual behavior and testosterone levels of male rats. Brain Res 480:151-159.
211. Seidler FJ, Levin ED, Lappi SE, Slotkin TA. 1992. Fetal nicotine exposure ablates the ability of postnatal nicotine challenge to release norepineph-rine from rat brain regions. Brain Res Dev Brain Res 69:288-291.
212. Shacka JJ, Fennell OB, Robinson SE. 1997. Prenatal nicotine sex-dependently alters agonist-induced locomotion and stereotypy. Neurotoxicol Teratol 19:467-476.
213. Shafey O, Eriksen M, Ross H, Mackay J. 2009. The Tobacco Atlas, 3rd ed. Atlanta: American Cancer Society.
214. Silberg JL, Parr T, Neale MC, Rutter M, Angold A, Eaves LJ. 2003. Mater-nal smoking during pregnancy and risk to boys' conduct disturbance: An examination of the causal hypothesis. Biol Psychiatry 53:130-135.
215. Simpson WJ. 1957. A preliminary report in cigarette smoking and the inci-dence of prematurity. Am J Obstet Gynecol 73:807-815.
216. Slotkin TA. 1998. Fetal nicotine or cocaine exposure: Which one is worse? JPET 285:931-945.
217. Slotkin TA. 2008. If nicotine is a developmental neurotoxicant in animal studies, dare we recommend nicotine replacement therapy in pregnant women and adolescents? Neurotoxicol Teratol 30:1-19.
218. Slotkin TA, Greer N, Faust J, Cho H, Seidler FJ. 1986. Effects of maternal nicotine injections on brain development in the rat: Ornithine decar-boxylase activity, nucleic acids and proteins in discrete brain regions. Brain Res Bull 17:41-50.
219. Slotkin TA, Orband-Miller L, Queen KL, Whitmore WL, Seidler FJ. 1987. Effects of prenatal nicotine exposure on biochemical development of rat brain regions: Maternal drug infusions via osmotic minipumps. J Phar-macol Exp Ther 240:602-611.
220. Slotkin TA, Lappi SE, Tayyeb MI, Seidler FJ. 1991. Chronic prenatal nico-tine exposure sensitizes rat brain to acute postnatal nicotine challenge as assessed with ornithine decarboxylase. Life Sci 49:665-670.
221. Slotkin TA, Lappi SE, Seidler FJ. 1993. Impact of fetal nicotine exposure on development of rat brain regions: Critical sensitive periods or effects of withdrawal? Brain Res Bull 31:319-328.
222. Slotkin TA, McCook EC, Seidler FJ. 1997. Cryptic brain cell injury caused by fetal nicotine exposure is associated with persistent elevations of c-fos protooncogene expression. Brain Res 750:180-188.
223. Slotkin TA, Epps TA, Stenger ML, Sawyer KJ, Seidler FJ. 1999. Cholin-ergic receptors in heart and brainstem of rats exposed to nicotine during development: Implications for hypoxia tolerance and perinatal mortal-ity. Brain Res Dev Brain Res 113:1-12.
224. Slotkin TA, Southard MC, Adam SJ, Cousins MM, Seidler FJ. 2004. Alpha7 nicotinic acetylcholine receptors targeted by cholinergic developmental neurotoxicants: Nicotine and chlorpyrifos. Brain Res Bull 64:227-235.
225. Slotkin TA, Seidler FJ, Qiao D, Aldridge JE, Tate CA, Cousins MM, Proskocil BJ, Sekhon HS, Clark JAL, Stacie L, Spindel ER. 2005. Effects of pre-natal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: Neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology 30:129-44.
226. Slotkin TA, Tate CA, Cousins MM, Seidler FJ. 2006. Prenatal nicotine ex-posure alters the responses to subsequent nicotine administration and withdrawal in adolescence: Serotonin receptors and cell signaling. Neu-ropsychopharmacology 31:2462-2475.
227. Slotkin TA, MacKillop EA, Rudder CL, Ryder IT, Tate CA, Seidler FJ. 2007a. Permanent, sex-selective effects of prenatal or adolescent nico-tine exposure, separately or sequentially, in rat brain regions: Indices of cholinergic and serotonergic synaptic function, cell signaling, and neu-ral cell number and size at 6 months of age. Neuropsychopharmacology 32:1082-1097.
228. Slotkin TA, Ryde IT, Seidler FJ. 2007b. Separate or sequential exposure to nicotine prenatally and in adulthood: Persistent effects on acetylcholine systems in rat brain regions. Brain Res Bull 74:91-103.
229. Slotkin TA, Ryde IT, Seidler FJ. 2010. Additive and synergistic effects of fetal nicotine and dexamethasone exposure on cholinergic synaptic function in adolescence and adulthood: Implications for the adverse consequences of maternal smoking and pharmacotherapy of preterm delivery. Brain Res Bull 81:552-560.
230. Smith LM, Cloak CC, Poland RE, Torday J, Ross MG. 2003. Prenatal nico-tine increases testosterone levels in the fetus and female offspring. Nicotine Tob Res 5:369-374.
231. Smith WT 4th, Seidler FJ, Slotkin TA. 1991. Acute stimulation of ornithine decarboxylase in neonatal rat brain regions by nicotine: A central receptor-mediated process? Brain Res Dev Brain Res 63:85-93.
232. Sobrian SK, Burton LE, Robinson NL, Ashe WK, James H, Stokes DL, Turner LM. 1990. Neurobehavioral and immunological effects of pre-natal cocaine exposure in rat. Pharmacol Biochem Behav 35:617-629.
233. Sobrian SK, Ali SF, Slikker W Jr, Holson RR. 1995. Interactive effects of prenatal cocaine and nicotine exposure on maternal toxicity, postnatal development and behavior in the rat. Mol Neurobiol 11:121-143.
234. Sobrian SK, Marr L, Ressman K. 2003. Prenatal cocaine and/or nicotine exposure produces depression and anxiety in aging rats. Prog Neuropsy-chopharmacol Biol Psychiatry 27:501-518.
235. Sobrian SK, Johnston M, Wright J, Kuhn D, Ameis K. 2008. Prenatal nico-tine and/or cocaine differentially alters nicotine-induced sensitization in aging offspring. Ann N Y Acad Sci 1139:466-477.
236. Somm E, Schwitzgebel VM, Vauthay DM, Camm EJ, Chen CY, Giacobino J, Sizonenko SV, Aubert ML, Huppi PS. 2008. Prenatal nicotine expo-sure alters early pancreatic islet and adipose tissue development with consequences on the control of body weight and glucose metabolism later in life. Endocrinol 149:6289-6299.
237. Somm E, Schwitzgebel VM, Vauthay DM, Aubert ML, Huppi PS. 2009. Prenatal nicotine exposure and the programming of metabolic and car-diovascular disorders. Mol Cell Endocrinol 304:69-77.
238. Sorenson CA, Raskin LA, Suh Y. 1991. The effects of prenatal nicotine on radial-arm maze performance in rats. Pharmacol Biochem Behav 40:991-993.
239. Suzuki K, Sata M, Tanaka T, Kondo N, Yamagata Z. 2010. Recent trends in the prevalence of and factors associated with maternal smoking during pregnancy in Japan. J Obstet Gynaecol Res 36:745-750.
240. Thapar A, Fowler T, Rice F, Scourfield J, van den Bree M, Thomas H, Harold G, Hay D. 2003. Maternal smoking during pregnancy and atten-tion deficit hyperactivity disorder symptoms in offspring. Am J Psychia-try 160:1985-1989.
241. Thomas JD, Garrison ME, Slawecki CJ, Ehlers CL, Riley EP. 2000. Nico-tine exposure during the neonatal brain growth spurt produces hyperac-tivity in preweanling rats. Neurotoxicol Teratol 22:695-701.
242. Tizabi Y, Popke EJ, Rahman MA, Nespor SM, Grunberg NE. 1997. Hyper-activity induced by prenatal nicotine exposure is associated with an in-crease in cortical nicotinic receptors. Pharmacol Biochem Behav 58:141-146.
243. Tizabi Y, Russell LT, Nespor SM, Perry DC, Grunberg NE. 2000. Prenatal nicotine exposure: Effects on locomotor activity and central [125I]alpha-BT binding in rats. Pharmacol Biochem Behav 66:495-500.
244. Tong VT, Dietz PM, England LJ. 2010. Reliance on self-reporting underes-timates pregnancy smoking rates in Scotland, with more than 2, 400 pregnant smokers estimated to be missed each year. Evidence Based Med 15:94-95.
245. Toschke AM, Koletzko B, Slikker W, Hermann M, von Kries R. 2002. Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr 161:445-448.
246. Toschke AM, Montgomery SM, Pfeiffer U, von Kries R. 2003. Early intra-uterine exposure to tobacco-inhaled products and obesity. Am J Epide-miol 158:1068-1074.
247. Trasti N, Vik T, Jacobsen G, Bakketeig LS. 1999. Smoking in pregnancy and children's mental and motor development at age 1 and 5 years. Early Hum Dev 55:137-147.
248. Trauth JA, Seidler FJ, McCook EC, Slotkin TA. 1999. Persistent c-fos in-duction by nicotine in developing rat brain regions: Interaction with hypoxia. Pediatr Res 45:38-45.
249. Vaglenova J, Birru S, Pandiella NM, Breese CR. 2004. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nico-tine exposure. Behav Brain Res 150:159-170.
250. Vaglenova J, Parameswaran K, Suppiramaniam V, Breese CR, Pandiell N, Birru S. 2008. Long-lasting teratogenic effects of nicotine on cognition: Gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 90:527-536.
251. Velazquez-Moctezuma J, Dominguez Salazar E, Cruz Rueda ML. 1993. The effect of prenatal stress on adult sexual behavior in rats depends on the nature of the stressor. Physiol Behav 53:443-448.
252. Vibat CR, Lasalde JA, McNamee MG. 1995. Differential desensitization properties of rat neuronal nicotinic acetylcholine receptor subunit com-binations expressed in Xenopus laevis oocytes. Cell Mol Neurobiol 15:411-425.
253. Vieira CA, de Paiva SA, Funai MN, Bergamaschi MM, Queiroz RH, Giglio JR. 2010. Quantification of nicotine in commercial brand cigarettes: How much is inhaled by the smoker? Biochem Mol Biol Educ 38:330-334.
254. Vik T, Jacobsen G, Vatten L, Bakketeig LS. 1996. Pre-and post-natal growth in children of women who smoked in pregnancy. Early Hum Dev 45:245-255.
255. Villalbi JR, Salvador J, Cano-Serral G, Rodriguez-Sanz MC, Borrell C. 2007. Maternal smoking, social class and outcomes of pregnancy. Pae-diatr Perinat Epidemiol 21:441-447.
256. von Kries R, Toschke AM, Koletzko B, Slikker W Jr. 2002. Maternal smok-ing during pregnancy and childhood obesity. Am J Epidemiol 156: 954-961.
257. von Kries R, Bolte G, Baghi L, Toschke AM. 2006. Parental smoking and childhood obesity: Maternal smoking in pregnancy the critical expo-sure? Int J Epidemiol 37:210-216.
258. von Ziegler NI, Schlumpf M, Lichtensteiger W. 1991. Prenatal nicotine ex-posure selectively affects perinatal forebrain aromatase activity and fe-tal adrenal function in male rats. Brain Res Dev Brain Res 62:23-31.
259. Wakschlag LS, Lahey BB, Loeber R, Green SM, Gordon RA, Leventhal BL. 1997. Maternal smoking during pregnancy and the risk of conduct disorder in boys. Arch Gen Psychiatry 54:670-676.
260. Wakschlag LS, Pickett KE, Leventhal BL. 2000. The association between maternal cigarette smoking and psychiatric diseases or criminal out-come in the offspring. Reprod Toxicol 14:579-580.
261. Wakschlag LS, Pickett KE, Kasza KE, Loeber R. 2006. Is prenatal smoking associated with a developmental pattern of conduct problems in young boys? J Am Acad Child Adolesc Psychiatr 45:461-467.
262. Ward IL. 1984. The prenatal stress syndrome: Current status. Psychoneu-roendocrinol 9:3-11.
263. Wecker L, Pollock VV, Pacheco MA, Pastoor T. 2010. Nicotine-induced up regulation of a4b2 neuronal nicotinic receptors is mediated by the pro-tein kinase C-dependent phosphorylation of a4 subunits. Neurosci 171:12-22.
264. Weinstock M. 2007. Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem Res 32:1730-1740.
265. Weissman MM, Warner V, Wickramaratne PJ, Kandel DB. 1999. Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psychiatry 38:892-899.
266. Williams CM, Kanagasabai T. 1984. Maternal adipose tissue response to nicotine administration in the pregnant rat: Effects on fetal body fat and cellularity. Br J Nutr 51:7-13.
267. Williams GM, O'Callaghan M, Najman JM, Bor W, Andersen MJ, Richards DUC. 1998. Maternal cigarette smoking and child psychiatric morbid-ity: A longitudinal study. Pediatrics 102:e11.
268. Wonnacott S. 1990. The paradox of nicotinic acetylcholine receptor upregu-lation by nicotine. Trends Pharmacol Sci 11:216-219.
269. Xiao C, Nashmi R, McKinney S, Cai H, McIntosh JM, Lester HA. 2009. Chronic nicotine selectively enhances alpha4beta2* nicotinic acetyl-choline receptors in the nigrostriatal dopamine pathway. J Neurosci 29:12428-12439.
270. Xu Z, Seidler FJ, Ali SF, Slikker W Jr, Slotkin TA. 2001. Fetal and adoles-cent nicotine administration: Effects on CNS serotonergic systems. Brain Res 914:166-178.
271. Yanai J, Pick CG, Rogel-Fuchs Y, Zahalka EA. 1992. Alterations in hip-pocampal cholinergic receptors and hippocampal behaviors after early exposure to nicotine. Brain Res Bull 29:363-368.
272. Younoszai MK, Peloso J, Haworth JC. 1969. Fetal growth retardation in rats exposed to cigarette smoke during pregnancy. Am J Obstet Gynecol 104:1207-1213.
273. Zahalka EA, Seidler FJ, Lappi SE, McCook EC, Yanai J, Slotkin TA. 1992. Deficits in development of central cholinergic pathways caused by fetal nicotine exposure: Differential effects on choline acetyltransferase activ-ity and [3H]hemicholinium-3 binding. Neurotoxicol Teratol 14:375-382.
274. Zahalka EA, Seidler FJ, Yanai J, Slotkin TA. 1993. Fetal nicotine exposure alters ontogeny of M1-receptors and their link to G-proteins. Neurotoxi-col Teratol 15:107-115.
275. Zambrano CA, Marks MJ, Cassels BK, Maccioni RB. 2009. In vivo effects of 3-iodocytisine: Pharmacological and genetic analysis of hypothermia and evaluation of chronic treatment on nicotinic binding sites. Neuro-pharmacology 57:332-342.
276. Zbuzek VK, Chin CW. 1994. Prenatal nicotine exposure increased duration of nicotine-induced analgesia in adult rats. Psychopharmacology (Berl) 113:534-538.