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Hyperactivity, increased nicotine consumption and impaired performance in the five-choice serial reaction time task in adolescent rats prenatally exposed to nicotine

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Abstract

Rationale

Prenatal exposure to nicotine has been linked to accelerated risk for different psychiatric disorders, including conduct disorder, attention deficit hyperactivity disorder (ADHD) and drug abuse. We examine a potential link between prenatal nicotine exposure, hyperactivity, anxiety, nicotine consumption, and cognitive performance in rats.

Methods

Adolescent offspring of females exposed during pregnancy to 0.06 mg/ml nicotine solution as the only source of water and of a group of pair-fed females, used as a control for anorexic effects of nicotine, were evaluated in a battery of tests, including locomotor activity, the elevated plus maze, two-bottle free-choice nicotine solution consumption, the five-choice serial reaction time test (5-CSRTT) and a delay-discounting test. All tests were conducted between postnatal day (PND) 25 and PND 50.

Results

Nicotine-exposed animals expressed hyperactivity, increased number of open arms entries in the elevated plus maze and increased numbers of anticipatory responses in the 5-CSRTT. Decreased aversion for nicotine solution in the free-choice test and decreased numbers of omission errors in the 5-CSRTT were observed both in nicotine-exposed and pair-fed offspring. Neither nicotine exposure nor pair-feeding had an effect on impulsive choice in a delay-discounting test.

Conclusions

Our study confirms deleterious effects of prenatal nicotine exposure on important aspects of behaviour and inhibitory control in adolescent rats and supports epidemiological findings that show increased levels of symptoms of ADHD and related disorders among those whose mothers smoked during their pregnancy. It also suggests a link between food restriction during pregnancy and addiction-related behaviours in offspring.

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References

  • Adams J (1986) Methods in behavioral teratology. Plenum, York, pp 67–97

    Book  Google Scholar 

  • Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15:341–352

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Antrop I, Roeyers H, Van OP, Buysse A (2000) Stimulation seeking and hyperactivity in children with ADHD. J Child Psychol Psychiatry 41:225–231

    Article  PubMed  CAS  Google Scholar 

  • Bardo MT, Dwoskin LP (2004) Biological connection between novelty- and drug-seeking motivational systems. Nebr Symp Motiv 50:127–158

    PubMed  Google Scholar 

  • Barkley RA, Cox D (2007) A review of driving risks and impairments associated with attention-deficit/hyperactivity disorder and the effects of stimulant medication on driving performance. J Safety Res 38:113–128

    Article  PubMed  Google Scholar 

  • Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83–144

    PubMed  CAS  Google Scholar 

  • Benowitz NL, Hukkanen J, Jacob P III (2009) Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol 192:29–60

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Clancy B, Finlay BL, Darlington RB, Anand KJ (2007) Extrapolating brain development from experimental species to humans. Neurotoxicology 28:931–937

    Article  PubMed  Google Scholar 

  • Cornelius MD, Leech SL, Goldschmidt L, Day NL (2000) Prenatal tobacco exposure: is it a risk factor for early tobacco experimentation? Nicotine Tob Res 2:45–52

    Article  PubMed  CAS  Google Scholar 

  • D’Onofrio BM, Van Hulle CA, Waldman ID, Rodgers JL, Harden KP, Rathouz PJ, Lahey BB (2008) Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Dev Psychopathol 20:139–164

    PubMed  Google Scholar 

  • Day N, Cornelius M, Goldschmidt L, Richardson G, Robles N, Taylor P (1992) The effects of prenatal tobacco and marijuana use on offspring growth from birth through 3 years of age. Neurotoxicol Teratol 14:407–414

    Article  PubMed  CAS  Google Scholar 

  • Dwyer JB, Broide RS, Leslie FM (2008) Nicotine and brain development. Birth Defects Res C Embryo Today 84:30–44

    Article  PubMed  CAS  Google Scholar 

  • Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 40:630–641

    Article  PubMed  CAS  Google Scholar 

  • Eskenazi B, Prehn AW, Christianson RE (1995) Passive and active maternal smoking as measured by serum cotinine: the effect on birthweight. Am J Public Health 85:395–398

    Article  PubMed  CAS  Google Scholar 

  • Evenden J (1999a) Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol 13:180–192

    Article  PubMed  CAS  Google Scholar 

  • Evenden JL (1999b) Varieties of impulsivity. Psychopharmacology (Berl) 146:348–361

    Article  CAS  Google Scholar 

  • Fried PA, Watkinson B (2001) Differential effects on facets of attention in adolescents prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 23:421–430

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Fuemmeler BF, Kollins SH, McClernon FJ (2007) Attention deficit hyperactivity disorder symptoms predict nicotine dependence and progression to regular smoking from adolescence to young adulthood. J Pediatr Psychol 32:1203–1213

    Article  PubMed  Google Scholar 

  • Genedani S, Bernardi M, Bertolini A (1983) Sex-linked differences in avoidance learning in the offspring of rats treated with nicotine during pregnancy. Psychopharmacology (Berl) 80:93–95

    Article  CAS  Google Scholar 

  • Guarnieri DJ, Brayton CE, Richards SM, Maldonado-Aviles J, Trinko JR, Nelson J, Taylor JR, Gourley SL, DiLeone RJ (2012) Gene profiling reveals a role for stress hormones in the molecular and behavioral response to food restriction. Biol Psychiatry 71:358–365

    Article  PubMed  CAS  Google Scholar 

  • Hack M, Taylor HG, Klein N, Eiben R, Schatschneider C, Mercuri-Minich N (1994) School-age outcomes in children with birth weights under 750 g. N Engl J Med 331:753–759

    Article  PubMed  CAS  Google Scholar 

  • Hahn B, Shoaib M, Stolerman IP (2002) Nicotine-induced enhancement of attention in the five-choice serial reaction time task: the influence of task demands. Psychopharmacology (Berl) 162:129–137

    Article  CAS  Google Scholar 

  • Heath CJ, Horst NK, Picciotto MR (2010) Oral nicotine consumption does not affect maternal care or early development in mice but results in modest hyperactivity in adolescence. Physiol Behav 101:764–769

    Article  PubMed  CAS  Google Scholar 

  • Hultman CM, Torrang A, Tuvblad C, Cnattingius S, Larsson JO, Lichtenstein P (2007) Birth weight and attention-deficit/hyperactivity symptoms in childhood and early adolescence: a prospective Swedish twin study. J Am Acad Child Adolesc Psychiatry 46:370–377

    Article  PubMed  Google Scholar 

  • Jacobsen LK, Slotkin TA, Mencl WE, Frost SJ, Pugh KR (2007) Gender-specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology 32:2453–2464

    Article  PubMed  CAS  Google Scholar 

  • Jauniaux E, Burton GJ (2007) Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 83:699–706

    Article  PubMed  CAS  Google Scholar 

  • Jensen TK, Henriksen TB, Hjollund NH, Scheike T, Kolstad H, Giwercman A, Ernst E, Bonde JP, Skakkebaek NE, Olsen J (1998) Adult and prenatal exposures to tobacco smoke as risk indicators of fertility among 430 Danish couples. Am J Epidemiol 148:992–997

    Article  PubMed  CAS  Google Scholar 

  • Jo YH, Talmage DA, Role LW (2002) Nicotinic receptor-mediated effects on appetite and food intake. J Neurobiol 53:618–632

    Article  PubMed  CAS  Google Scholar 

  • Klein LC, Stine MM, Pfaff DW, Vandenbergh DJ (2003) Laternal nicotine exposure increases nicotine preference in periadolescent male but not female C57B1/6 J mice. Nicotine Tob Res 5:117–124

    Article  PubMed  Google Scholar 

  • Kollins SH, McClernon FJ, Fuemmeler BF (2005) Association between smoking and attention-deficit/hyperactivity disorder symptoms in a population-based sample of young adults. Arch Gen Psychiatry 62:1142–1147

    Article  PubMed  Google Scholar 

  • Kotimaa AJ, Moilanen I, Taanila A, Ebeling H, Smalley SL, McGough JJ, Hartikainen AL, Jarvelin MR (2003) Maternal smoking and hyperactivity in 8-year-old children. J Am Acad Child Adolesc Psychiatry 42:826–833

    Article  PubMed  Google Scholar 

  • Kristjansson EA, Fried PA, Watkinson B (1989) Maternal smoking during pregnancy affects children’s vigilance performance. Drug Alcohol Depend 24:11–19

    Article  PubMed  CAS  Google Scholar 

  • Laviola G, Macri S, Morley-Fletcher S, Adriani W (2003) Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev 27:19–31

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Levin ED, Briggs SJ, Christopher NC, Rose JE (1993) Prenatal nicotine exposure and cognitive performance in rats. Neurotoxicol Teratol 15:251–260

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Levin ED, Wilkerson A, Jones JP, Christopher NC, Briggs SJ (1996) Prenatal nicotine effects on memory in rats: pharmacological and behavioral challenges. Brain Res Dev Brain Res 97:207–215

    Article  PubMed  CAS  Google Scholar 

  • Maehler R, Dadmarz M, Vogel WH (2000) Determinants of the voluntary consumption of nicotine by rats. Neuropsychobiology 41:200–204

    Article  PubMed  CAS  Google Scholar 

  • Maher BS, Marazita ML, Ferrell RE, Vanyukov MM (2002) Dopamine system genes and attention deficit hyperactivity disorder: a meta-analysis. Psychiatr Genet 12:207–215

    Article  PubMed  Google Scholar 

  • Marco EM, Macri S, Laviola G (2011) Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res 19:286–307

    Article  PubMed  Google Scholar 

  • McCartney JS, Fried PA, Watkinson B (1994) Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicol Teratol 16:269–276

    Article  PubMed  CAS  Google Scholar 

  • McClernon FJ, Fuemmeler BF, Kollins SH, Kail ME, Ashley-Koch AE (2008) Interactions between genotype and retrospective ADHD symptoms predict lifetime smoking risk in a sample of young adults. Nicotine Tob Res 10:117–127

    Article  PubMed  Google Scholar 

  • McNamara J, Vervaeke SL, Willoughby T (2008) Learning disabilities and risk-taking behavior in adolescents: a comparison of those with and without comorbid attention-deficit/hyperactivity disorder. J Learn Disabil 41:561–574

    Article  PubMed  Google Scholar 

  • Milberger S, Biederman J, Faraone SV, Jones J (1998) Further evidence of an association between maternal smoking during pregnancy and attention deficit hyperactivity disorder: findings from a high-risk sample of siblings. J Clin Child Psychol 27:352–358

    Article  PubMed  CAS  Google Scholar 

  • Mill J, Petronis A (2008) Pre- and peri-natal environmental risks for attention-deficit hyperactivity disorder (ADHD): the potential role of epigenetic processes in mediating susceptibility. J Child Psychol Psychiatry 49:1020–1030

    Article  PubMed  Google Scholar 

  • Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC (2001) Psychiatric aspects of impulsivity. Am J Psychiatry 158:1783–1793

    Article  PubMed  CAS  Google Scholar 

  • Munafo M, Murphy M, Whiteman D, Hey K (2002) Does cigarette smoking increase time to conception? J Biosoc Sci 34:65–73

    PubMed  Google Scholar 

  • Munafo MR, Johnstone EC (2008) Genes and cigarette smoking. Addiction 103:893–904

    Article  PubMed  Google Scholar 

  • Murphy K, Barkley RA (1996) Attention deficit hyperactivity disorder adults: comorbidities and adaptive impairments. Compr Psychiatry 37:393–401

    Article  PubMed  CAS  Google Scholar 

  • Murrin LC, Ferrer JR, Zeng WY, Haley NJ (1987) Nicotine administration to rats: methodological considerations. Life Sci 40:1699–1708

    Article  PubMed  CAS  Google Scholar 

  • Nunez H, Ruiz S, Soto-Moyano R, Navarrete M, Valladares L, White A, Perez H (2008) Fetal undernutrition induces overexpression of CRH mRNA and CRH protein in hypothalamus and increases CRH and corticosterone in plasma during postnatal life in the rat. Neurosci Lett 448:115–119

    Article  PubMed  CAS  Google Scholar 

  • Orlebeke JF, Knol DL, Verhulst FC (1997) Increase in child behavior problems resulting from maternal smoking during pregnancy. Arch Environ Health 52:317–321

    Article  PubMed  CAS  Google Scholar 

  • Orlebeke JF, Knol DL, Verhulst FC (1999) Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health 54:15–19

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947–957

    PubMed  CAS  Google Scholar 

  • Pellow S, Chopin P, File SE, Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149–167

    Article  PubMed  CAS  Google Scholar 

  • Peters MA, Ngan LL (1982) The effects of totigestational exposure to nicotine on pre- and postnatal development in the rat. Arch Int Pharmacodyn Ther 257:155–167

    PubMed  CAS  Google Scholar 

  • Redolat R, Perez-Martinez A, Carrasco MC, Mesa P (2009) Individual differences in novelty-seeking and behavioral responses to nicotine: a review of animal studies. Curr Drug Abuse Rev 2:230–242

    Article  PubMed  CAS  Google Scholar 

  • Ribary U, Lichtensteiger W (1989) Effects of acute and chronic prenatal nicotine treatment on central catecholamine systems of male and female rat fetuses and offspring. J Pharmacol Exp Ther 248:786–792

    PubMed  CAS  Google Scholar 

  • Roberts KH, Munafo MR, Rodriguez D, Drury M, Murphy MF, Neale RE, Nettle D (2005) Longitudinal analysis of the effect of prenatal nicotine exposure on subsequent smoking behavior of offspring. Nicotine Tob Res 7:801–808

    Article  PubMed  CAS  Google Scholar 

  • Romero RD, Chen WJ (2004) Gender-related response in open-field activity following developmental nicotine exposure in rats. Pharmacol Biochem Behav 78:675–681

    Article  PubMed  CAS  Google Scholar 

  • Rutherford HJ, Mayes LC, Potenza MN (2010) Neurobiology of adolescent substance use disorders: implications for prevention and treatment. Child Adolesc Psychiatr Clin N Am 19:479–492

    Article  PubMed  Google Scholar 

  • Sagvolden T, Aase H, Zeiner P, Berger D (1998) Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behav Brain Res 94:61–71

    Article  PubMed  CAS  Google Scholar 

  • Salihu HM, Aliyu MH, Kirby RS (2005) In utero nicotine exposure and fetal growth inhibition among twins. Am J Perinatol 22:421–427

    Article  PubMed  Google Scholar 

  • Scheres A, Dijkstra M, Ainslie E, Balkan J, Reynolds B, Sonuga-Barke E, Castellanos FX (2006) Temporal and probabilistic discounting of rewards in children and adolescents: effects of age and ADHD symptoms. Neuropsychologia 44:2092–2103

    Article  PubMed  Google Scholar 

  • Schneider T, Bizarro L, Asherson PJ, Stolerman IP (2010) Gestational exposure to nicotine in drinking water: teratogenic effects and methodological issues. Behav Pharmacol 21:206–216

    Article  PubMed  CAS  Google Scholar 

  • Schneider T, Ilott N, Brolese G, Bizarro L, Asherson PJ, Stolerman IP (2011) Prenatal exposure to nicotine impairs performance of the 5-choice serial reaction time task in adult rats. Neuropsychopharmacology 36:1114–1125

    Article  PubMed  CAS  Google Scholar 

  • Sexton M, Fox NL, Hebel JR (1990) Prenatal exposure to tobacco: II. Effects on cognitive functioning at age three. Int J Epidemiol 19:72–77

    Article  PubMed  CAS  Google Scholar 

  • Shacka JJ, Fennell OB, Robinson SE (1997) Prenatal nicotine sex-dependently alters agonist-induced locomotion and stereotypy. Neurotoxicol Teratol 19:467–476

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    Article  PubMed  CAS  Google Scholar 

  • Springate JE (1981) The neuroanatomic basis of early motor development: a review. J Dev Behav Pediatr 2:146–150

    Article  PubMed  CAS  Google Scholar 

  • Steinberg L (2004) Risk taking in adolescence: what changes, and why? Ann N Y Acad Sci 1021:51–58

    Article  PubMed  Google Scholar 

  • Taylor HG, Filipek PA, Juranek J, Bangert B, Minich N, Hack M (2011) Brain volumes in adolescents with very low birth weight: effects on brain structure and associations with neuropsychological outcomes. Dev Neuropsychol 36:96–117

    Article  PubMed  Google Scholar 

  • Taylor HG, Minich NM, Klein N, Hack M (2004) Longitudinal outcomes of very low birth weight: neuropsychological findings. J Int Neuropsychol Soc 10:149–163

    PubMed  Google Scholar 

  • Thapar A, Fowler T, Rice F, Scourfield J, van den Bree M, Thomas H, Harold G, Hay D (2003) Maternal smoking during pregnancy and attention deficit hyperactivity disorder symptoms in offspring. Am J Psychiatry 160:1985–1989

    Article  PubMed  Google Scholar 

  • Thapar A, Rice F, Hay D, Boivin J, Langley K, van den Bree M, Rutter M, Harold G (2009) Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 66:722–727

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vaglenova J, Birru S, Pandiella NM, Breese CR (2004) An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav Brain Res 150:159–170

    Article  PubMed  CAS  Google Scholar 

  • Vaglenova J, Parameshwaran K, Suppiramaniam V, Breese CR, Pandiella 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

    Article  PubMed  CAS  Google Scholar 

  • Vucetic Z, Totoki K, Schoch H, Whitaker KW, Hill-Smith T, Lucki I, Reyes TM (2010) Early life protein restriction alters dopamine circuitry. Neuroscience 168:359–370

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wermter AK, Laucht M, Schimmelmann BG, Banaschweski T, Sonuga-Barke EJ, Rietschel M, Becker K (2010) From nature versus nurture, via nature and nurture, to gene × environment interaction in mental disorders. Eur Child Adolesc Psychiatry 19:199–210

    Article  PubMed  Google Scholar 

  • Winstanley CA, Eagle DM, Robbins TW (2006) Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin Psychol Rev 26:379–395

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Li N, Yang J, Zhang T, Yang Z (2010) Effects of maternal food restriction on physical growth and neurobehavior in newborn Wistar rats. Brain Res Bull 83:1–8

    Article  PubMed  Google Scholar 

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Acknowledgments

The research was supported by a grant from the Wellcome Trust (079314).

Conflict of interest

Philip JE Asherson has received funding for his work on advisory boards, consultancy or industry-sponsored educational activities from Janssen-Cilag, Eli-Lilly, Shire and Flynn Pharma. Ian P Stolerman has received compensation in the past 3 years for professional services to Elsevier Science Publishers, Springer-Verlag and the US National Institute on Drug Abuse. The other authors declare no conflict of interest.

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Schneider, T., Bizarro, L., Asherson, P.J.E. et al. Hyperactivity, increased nicotine consumption and impaired performance in the five-choice serial reaction time task in adolescent rats prenatally exposed to nicotine. Psychopharmacology 223, 401–415 (2012). https://doi.org/10.1007/s00213-012-2728-7

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