Advertisement

Psychopharmacology

, Volume 223, Issue 4, pp 401–415 | Cite as

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

  • T. SchneiderEmail author
  • L. Bizarro
  • P. J. E. Asherson
  • I. P. Stolerman
Original Investigation

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.

Keywords

Nicotine Gestation Hyperactivity Impulsivity Adolescence ADHD 

Notes

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.

References

  1. Adams J (1986) Methods in behavioral teratology. Plenum, York, pp 67–97CrossRefGoogle Scholar
  2. Adriani W, Laviola G (2004) Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15:341–352PubMedCrossRefGoogle Scholar
  3. Ajarem JS, Ahmad M (1998) Prenatal nicotine exposure modifies behavior of mice through early development. Pharmacol Biochem Behav 59:313–318PubMedCrossRefGoogle Scholar
  4. Antrop I, Roeyers H, Van OP, Buysse A (2000) Stimulation seeking and hyperactivity in children with ADHD. J Child Psychol Psychiatry 41:225–231PubMedCrossRefGoogle Scholar
  5. Bardo MT, Dwoskin LP (2004) Biological connection between novelty- and drug-seeking motivational systems. Nebr Symp Motiv 50:127–158PubMedGoogle Scholar
  6. 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 38:113–128PubMedCrossRefGoogle Scholar
  7. 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 14:83–144PubMedGoogle Scholar
  8. Benowitz NL, Hukkanen J, Jacob P III (2009) Nicotine chemistry, metabolism, kinetics and biomarkers. Handb Exp Pharmacol 192:29–60PubMedCrossRefGoogle Scholar
  9. 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 4:545–548PubMedGoogle Scholar
  10. Clancy B, Finlay BL, Darlington RB, Anand KJ (2007) Extrapolating brain development from experimental species to humans. Neurotoxicology 28:931–937PubMedCrossRefGoogle Scholar
  11. Cornelius MD, Leech SL, Goldschmidt L, Day NL (2000) Prenatal tobacco exposure: is it a risk factor for early tobacco experimentation? Nicotine Tob Res 2:45–52PubMedCrossRefGoogle Scholar
  12. 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 20:139–164PubMedGoogle Scholar
  13. 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 14:407–414PubMedCrossRefGoogle Scholar
  14. Dwyer JB, Broide RS, Leslie FM (2008) Nicotine and brain development. Birth Defects Res C Embryo Today 84:30–44PubMedCrossRefGoogle Scholar
  15. Ernst M, Moolchan ET, Robinson ML (2001) Behavioral and neural consequences of prenatal exposure to nicotine. J Am Acad Child Adolesc Psychiatry 40:630–641PubMedCrossRefGoogle Scholar
  16. 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 85:395–398PubMedCrossRefGoogle Scholar
  17. Evenden J (1999a) Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol 13:180–192PubMedCrossRefGoogle Scholar
  18. Evenden JL (1999b) Varieties of impulsivity. Psychopharmacology (Berl) 146:348–361CrossRefGoogle Scholar
  19. Fried PA, Watkinson B (2001) Differential effects on facets of attention in adolescents prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 23:421–430PubMedCrossRefGoogle Scholar
  20. 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 25:427–436PubMedCrossRefGoogle Scholar
  21. 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 32:1203–1213PubMedCrossRefGoogle Scholar
  22. 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) 80:93–95CrossRefGoogle Scholar
  23. 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 71:358–365PubMedCrossRefGoogle Scholar
  24. 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 331:753–759PubMedCrossRefGoogle Scholar
  25. 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) 162:129–137CrossRefGoogle Scholar
  26. 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 101:764–769PubMedCrossRefGoogle Scholar
  27. 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 46:370–377PubMedCrossRefGoogle Scholar
  28. 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 32:2453–2464PubMedCrossRefGoogle Scholar
  29. Jauniaux E, Burton GJ (2007) Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit. Early Hum Dev 83:699–706PubMedCrossRefGoogle Scholar
  30. 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 148:992–997PubMedCrossRefGoogle Scholar
  31. Jo YH, Talmage DA, Role LW (2002) Nicotinic receptor-mediated effects on appetite and food intake. J Neurobiol 53:618–632PubMedCrossRefGoogle Scholar
  32. 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 5:117–124PubMedCrossRefGoogle Scholar
  33. 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 62:1142–1147PubMedCrossRefGoogle Scholar
  34. 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 42:826–833PubMedCrossRefGoogle Scholar
  35. Kristjansson EA, Fried PA, Watkinson B (1989) Maternal smoking during pregnancy affects children’s vigilance performance. Drug Alcohol Depend 24:11–19PubMedCrossRefGoogle Scholar
  36. 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 27:19–31PubMedCrossRefGoogle Scholar
  37. 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 85:575–583PubMedCrossRefGoogle Scholar
  38. Levin ED, Briggs SJ, Christopher NC, Rose JE (1993) Prenatal nicotine exposure and cognitive performance in rats. Neurotoxicol Teratol 15:251–260PubMedCrossRefGoogle Scholar
  39. 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 85:669–674PubMedCrossRefGoogle Scholar
  40. 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 97:207–215PubMedCrossRefGoogle Scholar
  41. Maehler R, Dadmarz M, Vogel WH (2000) Determinants of the voluntary consumption of nicotine by rats. Neuropsychobiology 41:200–204PubMedCrossRefGoogle Scholar
  42. Maher BS, Marazita ML, Ferrell RE, Vanyukov MM (2002) Dopamine system genes and attention deficit hyperactivity disorder: a meta-analysis. Psychiatr Genet 12:207–215PubMedCrossRefGoogle Scholar
  43. Marco EM, Macri S, Laviola G (2011) Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res 19:286–307PubMedCrossRefGoogle Scholar
  44. McCartney JS, Fried PA, Watkinson B (1994) Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicol Teratol 16:269–276PubMedCrossRefGoogle Scholar
  45. 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 10:117–127PubMedCrossRefGoogle Scholar
  46. 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 41:561–574PubMedCrossRefGoogle Scholar
  47. 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 27:352–358PubMedCrossRefGoogle Scholar
  48. 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 49:1020–1030PubMedCrossRefGoogle Scholar
  49. Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC (2001) Psychiatric aspects of impulsivity. Am J Psychiatry 158:1783–1793PubMedCrossRefGoogle Scholar
  50. Munafo M, Murphy M, Whiteman D, Hey K (2002) Does cigarette smoking increase time to conception? J Biosoc Sci 34:65–73PubMedGoogle Scholar
  51. Munafo MR, Johnstone EC (2008) Genes and cigarette smoking. Addiction 103:893–904PubMedCrossRefGoogle Scholar
  52. Murphy K, Barkley RA (1996) Attention deficit hyperactivity disorder adults: comorbidities and adaptive impairments. Compr Psychiatry 37:393–401PubMedCrossRefGoogle Scholar
  53. Murrin LC, Ferrer JR, Zeng WY, Haley NJ (1987) Nicotine administration to rats: methodological considerations. Life Sci 40:1699–1708PubMedCrossRefGoogle Scholar
  54. 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 448:115–119PubMedCrossRefGoogle Scholar
  55. Orlebeke JF, Knol DL, Verhulst FC (1997) Increase in child behavior problems resulting from maternal smoking during pregnancy. Arch Environ Health 52:317–321PubMedCrossRefGoogle Scholar
  56. Orlebeke JF, Knol DL, Verhulst FC (1999) Child behavior problems increased by maternal smoking during pregnancy. Arch Environ Health 54:15–19PubMedCrossRefGoogle Scholar
  57. 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 49:293–305PubMedCrossRefGoogle Scholar
  58. Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947–957PubMedGoogle Scholar
  59. 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 14:149–167PubMedCrossRefGoogle Scholar
  60. Peters MA, Ngan LL (1982) The effects of totigestational exposure to nicotine on pre- and postnatal development in the rat. Arch Int Pharmacodyn Ther 257:155–167PubMedGoogle Scholar
  61. 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 2:230–242PubMedCrossRefGoogle Scholar
  62. 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 248:786–792PubMedGoogle Scholar
  63. 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 7:801–808PubMedCrossRefGoogle Scholar
  64. Romero RD, Chen WJ (2004) Gender-related response in open-field activity following developmental nicotine exposure in rats. Pharmacol Biochem Behav 78:675–681PubMedCrossRefGoogle Scholar
  65. Rutherford HJ, Mayes LC, Potenza MN (2010) Neurobiology of adolescent substance use disorders: implications for prevention and treatment. Child Adolesc Psychiatr Clin N Am 19:479–492PubMedCrossRefGoogle Scholar
  66. Sagvolden T, Aase H, Zeiner P, Berger D (1998) Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behav Brain Res 94:61–71PubMedCrossRefGoogle Scholar
  67. Salihu HM, Aliyu MH, Kirby RS (2005) In utero nicotine exposure and fetal growth inhibition among twins. Am J Perinatol 22:421–427PubMedCrossRefGoogle Scholar
  68. 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 44:2092–2103PubMedCrossRefGoogle Scholar
  69. Schneider T, Bizarro L, Asherson PJ, Stolerman IP (2010) Gestational exposure to nicotine in drinking water: teratogenic effects and methodological issues. Behav Pharmacol 21:206–216PubMedCrossRefGoogle Scholar
  70. 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 36:1114–1125PubMedCrossRefGoogle Scholar
  71. Sexton M, Fox NL, Hebel JR (1990) Prenatal exposure to tobacco: II. Effects on cognitive functioning at age three. Int J Epidemiol 19:72–77PubMedCrossRefGoogle Scholar
  72. Shacka JJ, Fennell OB, Robinson SE (1997) Prenatal nicotine sex-dependently alters agonist-induced locomotion and stereotypy. Neurotoxicol Teratol 19:467–476PubMedCrossRefGoogle Scholar
  73. 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 30:1–19PubMedCrossRefGoogle Scholar
  74. 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 31:319–328Google Scholar
  75. Sorenson CA, Raskin LA, Suh Y (1991) The effects of prenatal nicotine on radial-arm maze performance in rats. Pharmacol Biochem Behav 40:991–993PubMedCrossRefGoogle Scholar
  76. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463PubMedCrossRefGoogle Scholar
  77. Springate JE (1981) The neuroanatomic basis of early motor development: a review. J Dev Behav Pediatr 2:146–150PubMedCrossRefGoogle Scholar
  78. Steinberg L (2004) Risk taking in adolescence: what changes, and why? Ann N Y Acad Sci 1021:51–58PubMedCrossRefGoogle Scholar
  79. 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 36:96–117PubMedCrossRefGoogle Scholar
  80. Taylor HG, Minich NM, Klein N, Hack M (2004) Longitudinal outcomes of very low birth weight: neuropsychological findings. J Int Neuropsychol Soc 10:149–163PubMedGoogle Scholar
  81. 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 160:1985–1989PubMedCrossRefGoogle Scholar
  82. 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 66:722–727PubMedCrossRefGoogle Scholar
  83. 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 66:495–500PubMedCrossRefGoogle Scholar
  84. 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 150:159–170PubMedCrossRefGoogle Scholar
  85. 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 90:527–536PubMedCrossRefGoogle Scholar
  86. Vucetic Z, Totoki K, Schoch H, Whitaker KW, Hill-Smith T, Lucki I, Reyes TM (2010) Early life protein restriction alters dopamine circuitry. Neuroscience 168:359–370PubMedCrossRefGoogle Scholar
  87. 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 54:670–676PubMedCrossRefGoogle Scholar
  88. 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 38:892–899PubMedCrossRefGoogle Scholar
  89. 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 19:199–210PubMedCrossRefGoogle Scholar
  90. Winstanley CA, Eagle DM, Robbins TW (2006) Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin Psychol Rev 26:379–395PubMedCrossRefGoogle Scholar
  91. Winzer-Serhan UH (2008) Long-term consequences of maternal smoking and developmental chronic nicotine exposure. Front Biosci 13:636–649PubMedCrossRefGoogle Scholar
  92. 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 83:1–8PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • T. Schneider
    • 1
    • 4
    Email author
  • L. Bizarro
    • 2
  • P. J. E. Asherson
    • 3
  • I. P. Stolerman
    • 1
  1. 1.Section of Behavioural Pharmacology, Institute of Psychiatry P048King’s College LondonLondonUK
  2. 2.Departamento de Psicologia do Desenvolvimento e da Personalidade, Instituto de PsicologiaUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  3. 3.MRC Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry P080King’s College LondonLondonUK
  4. 4.Experimental PsychologyUniversity of OxfordOxfordUK

Personalised recommendations