Prenatal exposure to drugs: effects on brain development and implications for policy and education (original) (raw)

• Pinto, C. Medical officials question arrest of pregnant patient. The Tennessean A1 (24 Apr 2008).
• Seckl, J. R. & Meaney, M. J. Glucocorticoid “programming” and PTSD risk. Ann. NY Acad. Sci. 1071, 351–378 (2006).
  CAS PubMed Google Scholar
• Levitt, P. Prenatal effects of drugs of abuse on brain development. Drug Alcohol Depend. 51, 109–125 (1998).
  CAS PubMed Google Scholar
• Thadani, P. V. The intersection of stress, drug abuse and development. Psychoneuroendocrinology 27, 221–230 (2002).
  PubMed Google Scholar
• Randall, C. L. Alcohol and pregnancy: highlights from three decades of research. J. Stud. Alcohol 62, 554–561 (2001).
  CAS PubMed Google Scholar
• Malanga, C. J. & Kosofsky, B. E. Mechanisms of action of drugs of abuse on the developing fetal brain. Clin. Perinatol. 26, 17–37, v–vi (1999).
  CAS PubMed Google Scholar
• Clancy, B., Darlington, R. B. & Finlay, B. L. Translating developmental time across mammalian species. Neuroscience 105, 7–17 (2001).
  CAS PubMed Google Scholar
• Clancy, B., Finlay, B. L., Darlington, R. B. & Anand, K. J. Extrapolating brain development from experimental species to humans. Neurotoxicology 28, 931–937 (2007).
  PubMed Google Scholar
• Clancy, B. et al. Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics 5, 79–94 (2007).
  PubMed Google Scholar
• Volkow, N. D., Fowler, J. S., Wang, G. J., Swanson, J. M. & Telang, F. Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch. Neurol. 64, 1575–1579 (2007).
  PubMed Google Scholar
• Wise, R. A. Dopamine, learning and motivation. Nature Rev. Neurosci. 5, 483–494 (2004).
  CAS Google Scholar
• Goldman-Rakic, P. S., Lidow, M. S. & Gallager, D. W. Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex. J. Neurosci. 10, 2125–2138 (1990).
  CAS PubMed PubMed Central Google Scholar
• Djamgoz, M. B. & Wagner, H. J. Localization and function of dopamine in the adult vertebrate retina. Neurochem. Int. 20, 139–191 (1992).
  CAS PubMed Google Scholar
• De Souza, E. B. & Kuhar, M. J. Dopamine receptors in the anterior lobe of the human pituitary gland: autoradiographic localization. Brain Res. 306, 391–395 (1984).
  CAS PubMed Google Scholar
• Murrin, L. C., Gale, K. & Kuhar, M. J. Autoradiographic localization of neuroleptic and dopamine receptors in the caudate-putamen and substantia nigra: effects of lesions. Eur. J. Pharmacol. 60, 229–235 (1979).
  CAS PubMed Google Scholar
• Chasnoff, I. J., Burns, W. J., Schnoll, S. H. & Burns, K. A. Cocaine use in pregnancy. N. Engl. J. Med. 313, 666–669 (1985).
  CAS PubMed Google Scholar
• Chasnoff, I. J., Burns, K. A. & Burns, W. J. Cocaine use in pregnancy: perinatal morbidity and mortality. Neurotoxicol. Teratol. 9, 291–293 (1987).
  CAS PubMed Google Scholar
• Bauchner, H., Zuckerman, B., Amaro, H., Frank, D. A. & Parker, S. Teratogenicity of cocaine. J. Pediatr. 111, 160–161 (1987).
  CAS PubMed Google Scholar
• Dow-Edwards, D., Mayes, L., Spear, L. & Hurd, Y. Cocaine and development: clinical, behavioral, and neurobiological perspectives–a symposium report. Neurotoxicol. Teratol. 21, 481–490 (1999).
  CAS PubMed Google Scholar
• Gingras, J. L. & O'Donnell, K. J. State control in the substance-exposed fetus. I. The fetal neurobehavioral profile: an assessment of fetal state, arousal, and regulation competency. Ann. NY Acad. Sci. 846, 262–276 (1998).
  CAS PubMed Google Scholar
• Karmel, B. Z. & Gardner, J. M. Prenatal cocaine exposure effects on arousal-modulated attention during the neonatal period. Dev. Psychobiol. 29, 463–480 (1996).
  CAS PubMed Google Scholar
• Mayes, L. C., Grillon, C., Granger, R. & Schottenfeld, R. Regulation of arousal and attention in preschool children exposed to cocaine prenatally. Ann. NY Acad. Sci. 846, 126–143 (1998).
  CAS PubMed Google Scholar
• Richardson, G. A., Hamel, S. C., Goldschmidt, L. & Day, N. L. The effects of prenatal cocaine use on neonatal neurobehavioral status. Neurotoxicol. Teratol. 18, 519–528 (1996).
  CAS PubMed Google Scholar
• Singer, L. T. et al. Cognitive outcomes of preschool children with prenatal cocaine exposure. JAMA 291, 2448–2456 (2004).
  CAS PubMed Google Scholar
• Mayes, L. C. Exposure to cocaine: behavioral outcomes in preschool and school-age children. NIDA Res. Monogr. 164, 211–229 (1996).
  CAS PubMed Google Scholar
• Mayes, L. C., Bornstein, M. H., Chawarska, K. & Granger, R. H. Information processing and developmental assessments in 3-month-old infants exposed prenatally to cocaine. Pediatrics 95, 539–545 (1995).
  CAS PubMed Google Scholar
• Mayes, L. C., Cicchetti, D., Acharyya, S. & Zhang, H. Developmental trajectories of cocaine-and-other-drug-exposed and non-cocaine-exposed children. J. Dev. Behav. Pediatr. 24, 323–335 (2003).
  PubMed Google Scholar
• Richardson, G. A., Conroy, M. L. & Day, N. L. Prenatal cocaine exposure: effects on the development of school-age children. Neurotoxicol. Teratol. 18, 627–634 (1996).
  CAS PubMed Google Scholar
• Richardson, G. A. Prenatal cocaine exposure. A longitudinal study of development. Ann. NY Acad. Sci. 846, 144–152 (1998).
  CAS PubMed Google Scholar
• Gabriel, M., Taylor, C. & Burhans, L. In utero cocaine, discriminative avoidance learning with low-salient stimuli and learning-related neuronal activity in rabbits (Oryctolagus cuniculus). Behav. Neurosci. 117, 912–926 (2003).
  CAS PubMed Google Scholar
• Morrow, B. A., Elsworth, J. D. & Roth, R. H. Prenatal cocaine exposure disrupts non-spatial, short-term memory in adolescent and adult male rats. Behav. Brain Res. 129, 217–223 (2002).
  CAS PubMed Google Scholar
• Thompson, B. L., Levitt, P. & Stanwood, G. D. Prenatal cocaine exposure specifically alters spontaneous alternation behavior. Behav. Brain Res. 164, 107–116 (2005).
  CAS PubMed Google Scholar
• Levine, T. P. et al. Effects of prenatal cocaine exposure on special education in school-aged children. Pediatrics 122, e83–e91 (2008).
  PubMed Google Scholar
• Harvey, J. A. Cocaine effects on the developing brain: current status. Neurosci. Biobehav. Rev. 27, 751–764 (2004).
  CAS PubMed Google Scholar
• Lidow, M. S. Consequences of prenatal cocaine exposure in nonhuman primates. Brain Res. Dev. Brain Res. 147, 23–36 (2003).
  CAS PubMed Google Scholar
• Mayes, L. C. A behavioral teratogenic model of the impact of prenatal cocaine exposure on arousal regulatory systems. Neurotoxicol. Teratol. 24, 385–395 (2002).
  CAS PubMed Google Scholar
• Stanwood, G. D. & Levitt, P. Drug exposure early in life: functional repercussions of changing neuropharmacology during sensitive periods of brain development. Curr. Opin. Pharmacol. 4, 65–71 (2004).
  CAS PubMed Google Scholar
• Parlaman, J. P., Thompson, B. L., Levitt, P. & Stanwood, G. D. Pharmacokinetic profile of cocaine following intravenous administration in the female rabbit. Eur. J. Pharmacol. 563, 124–129 (2007).
  CAS PubMed PubMed Central Google Scholar
• Evans, S. M., Cone, E. J. & Henningfield, J. E. Arterial and venous cocaine plasma concentrations in humans: relationship to route of administration, cardiovascular effects and subjective effects. J. Pharmacol. Exp. Ther. 279, 1345–1356 (1996).
  CAS PubMed Google Scholar
• Jenkins, A. J., Keenan, R. M., Henningfield, J. E. & Cone, E. J. Correlation between pharmacological effects and plasma cocaine concentrations after smoked administration. J. Anal. Toxicol. 26, 382–392 (2002).
  CAS PubMed Google Scholar
• Friedman, E., Yadin, E. & Wang, H. Y. Effect of prenatal cocaine on dopamine receptor-G protein coupling in mesocortical regions of the rabbit brain. Neuroscience 70, 739–747 (1996).
  CAS PubMed Google Scholar
• Jones, L. B. et al. In utero cocaine-induced dysfunction of dopamine D1 receptor signaling and abnormal differentiation of cerebral cortical neurons. J. Neurosci. 20, 4606–4614 (2000).
  CAS PubMed PubMed Central Google Scholar
• Wang, H. Y., Runyan, S., Yadin, E. & Friedman, E. Prenatal exposure to cocaine selectively reduces D1 dopamine receptor-mediated activation of striatal Gs proteins. J. Pharmacol. Exp. Ther. 273, 492–498 (1995).
  CAS PubMed Google Scholar
• Stanwood, G. D., Parlaman, J. P. & Levitt, P. Anatomical abnormalities in dopaminoceptive regions of the cerebral cortex of dopamine D1 receptor mutant mice. J. Comp. Neurol. 487, 270–282 (2005).
  CAS PubMed Google Scholar
• Stanwood, G. D., Washington, R. A., Shumsky, J. S. & Levitt, P. Prenatal cocaine exposure produces consistent developmental alterations in dopamine-rich regions of the cerebral cortex. Neuroscience 106, 5–14 (2001).
  CAS PubMed Google Scholar
• Murphy, E. H. et al. Cocaine administration in pregnant rabbits alters cortical structure and function in their progeny in the absence of maternal seizures. Exp. Brain Res. 114, 433–441 (1997).
  CAS PubMed Google Scholar
• Stanwood, G. D. & Levitt, P. Prenatal exposure to cocaine produces unique developmental and long-term adaptive changes in dopamine D1 receptor activity and subcellular distribution. J. Neurosci. 27, 152–157 (2007).
  CAS PubMed PubMed Central Google Scholar
• Clark, L., Cools, R. & Robbins, T. W. The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn. 55, 41–53 (2004).
  CAS PubMed Google Scholar
• Collette, F. & Van der Linden, M. Brain imaging of the central executive component of working memory. Neurosci. Biobehav. Rev. 26, 105–125 (2002).
  PubMed Google Scholar
• Elliott, R. Executive functions and their disorders. Br. Med. Bull. 65, 49–59 (2003).
  PubMed Google Scholar
• Elston, G. N. Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb. Cortex 13, 1124–1138 (2003).
  PubMed Google Scholar
• Goldman-Rakic, P. S. Regional and cellular fractionation of working memory. Proc. Natl Acad. Sci. USA 93, 13473–13480 (1996).
  CAS PubMed PubMed Central Google Scholar
• Goldman-Rakic, P. S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 1445–1453 (1996).
  CAS PubMed Google Scholar
• Stanwood, G. D., Washington, R. A. & Levitt, P. Identification of a sensitive period of prenatal cocaine exposure that alters the development of the anterior cingulate cortex. Cereb. Cortex 11, 430–440 (2001).
  CAS PubMed Google Scholar
• Crandall, J. E., Hackett, H. E., Tobet, S. A., Kosofsky, B. E. & Bhide, P. G. Cocaine exposure decreases GABA neuron migration from the ganglionic eminence to the cerebral cortex in embryonic mice. Cereb. Cortex 14, 665–675 (2004).
  PubMed Google Scholar
• Gressens, P., Kosofsky, B. E. & Evrard, P. Cocaine-induced disturbances of corticogenesis in the developing murine brain. Neurosci. Lett. 140, 113–116 (1992).
  CAS PubMed Google Scholar
• Lidow, M. S. Prenatal cocaine exposure adversely affects development of the primate cerebral cortex. Synapse 21, 332–341 (1995).
  CAS PubMed Google Scholar
• Lidow, M. S. & Song, Z. M. Effect of cocaine on cell proliferation in the cerebral wall of monkey fetuses. Cereb. Cortex 11, 545–551 (2001).
  CAS PubMed Google Scholar
• Ren, J. Q., Malanga, C. J., Tabit, E. & Kosofsky, B. E. Neuropathological consequences of prenatal cocaine exposure in the mouse. Int. J. Dev. Neurosci. 22, 309–320 (2004).
  CAS PubMed PubMed Central Google Scholar
• Lidow, M. S. & Song, Z. M. Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J. Comp. Neurol. 435, 263–275 (2001).
  CAS PubMed Google Scholar
• Crandall, J. E. et al. Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J. Neurosci. 27, 3813–3822 (2007).
  CAS PubMed PubMed Central Google Scholar
• Ohtani, N., Goto, T., Waeber, C. & Bhide, P. G. Dopamine modulates cell cycle in the lateral ganglionic eminence. J. Neurosci. 23, 2840–2850 (2003).
  CAS PubMed PubMed Central Google Scholar
• Harvey, J. A. et al. Effects of prenatal exposure to cocaine on the developing brain: anatomical, chemical, physiological and behavioral consequences. Neurotox. Res. 3, 117–143 (2001).
  CAS PubMed Google Scholar
• Stanwood, G. D. & Levitt, P. Repeated i.v. cocaine exposure produces long-lasting behavioral sensitization in pregnant adults, but behavioral tolerance in their offspring. Neuroscience 122, 579–583 (2003).
  CAS PubMed Google Scholar
• Johnston, L. D., O'Malley, P. M., Bachman, J. G. & Schulenberg, J. E. Monitoring the Future national survey results on drug use, 1975–2007. Volume I: secondary school students. NIH Publication No. 08–6418A (National Institute on Drug Abuse, Bethesda, Maryland, 2008).
• Smith, L. M. et al. Prenatal methamphetamine use and neonatal neurobehavioral outcome. Neurotoxicol. Teratol. 30, 20–28 (2008).
  CAS PubMed Google Scholar
• Smith, L. M. et al. The infant development, environment, and lifestyle study: effects of prenatal methamphetamine exposure, polydrug exposure, and poverty on intrauterine growth. Pediatrics 118, 1149–1156 (2006).
  PubMed Google Scholar
• Petrou, S., Sach, T. & Davidson, L. The long-term costs of preterm birth and low birth weight: results of a systematic review. Child Care Health Dev. 27, 97–115 (2001).
  CAS PubMed Google Scholar
• Chaikind, S. & Corman, H. The impact of low birthweight on special education costs. J. Health Econ. 10, 291–311 (1991).
  CAS PubMed Google Scholar
• Cernerud, L., Eriksson, M., Jonsson, B., Steneroth, G. & Zetterstrom, R. Amphetamine addiction during pregnancy: 14-year follow-up of growth and school performance. Acta Paediatr. 85, 204–208 (1996).
  CAS PubMed Google Scholar
• Chang, L. et al. Smaller subcortical volumes and cognitive deficits in children with prenatal methamphetamine exposure. Psychiatry Res. 132, 95–106 (2004).
  CAS PubMed Google Scholar
• Chang, L., Alicata, D., Ernst, T. & Volkow, N. Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 102 (Suppl. 1), 16–32 (2007).
  PubMed Google Scholar
• Derauf, C. et al. Demographic and psychosocial characteristics of mothers using methamphetamine during pregnancy: preliminary results of the Infant Development, Environment, And Lifestyle study (IDEAL). Am. J. Drug Alcohol Abuse 33, 281–289 (2007).
  PubMed PubMed Central Google Scholar
• Melo, P., Rodrigues, L. G., Silva, M. C. & Tavares, M. A. Effects of prenatal exposure to methamphetamine on the development of the rat retina. Ann. NY Acad. Sci. 1074, 590–603 (2006).
  CAS PubMed Google Scholar
• Melo, P., Moreno, V. Z., Vazquez, S. P., Pinazo-Duran, M. D. & Tavares, M. A. Myelination changes in the rat optic nerve after prenatal exposure to methamphetamine. Brain Res. 1106, 21–29 (2006).
  CAS PubMed Google Scholar
• Slamberova, R., Pometlova, M. & Charousova, P. Postnatal development of rat pups is altered by prenatal methamphetamine exposure. Prog. Neuropsychopharmacol. Biol. Psychiatry 30, 82–88 (2006).
  CAS PubMed Google Scholar
• Slamberova, R., Pometlova, M., Syllabova, L. & Mancuskova, M. Learning in the place navigation task, not the new-learning task, is altered by prenatal methamphetamine exposure. Brain Res. Dev. Brain Res. 157, 217–219 (2005).
  CAS PubMed Google Scholar
• Nasif, F. J., Cuadra, G. R. & Ramirez, O. A. Permanent alteration of central noradrenergic system by prenatally administered amphetamine. Brain Res. Dev. Brain Res. 112, 181–188 (1999).
  CAS PubMed Google Scholar
• Gomes-da-Silva, J. et al. Prenatal exposure to methamphetamine in the rat: ontogeny of tyrosine hydroxylase mRNA expression in mesencephalic dopaminergic neurons. Ann. NY Acad. Sci. 965, 68–77 (2002).
  CAS PubMed Google Scholar
• Cabrera, T. M., Levy, A. D., Li, Q., van de Kar, L. D. & Battaglia, G. Prenatal methamphetamine attenuates serotonin mediated renin secretion in male and female rat progeny: evidence for selective long-term dysfunction of serotonin pathways in brain. Synapse 15, 198–208 (1993).
  CAS PubMed Google Scholar
• Slamberova, R., Pometlova, M. & Rokyta, R. Effect of methamphetamine exposure during prenatal and preweaning periods lasts for generations in rats. Dev. Psychobiol. 49, 312–322 (2007).
  CAS PubMed Google Scholar
• Rogers, J. M. Tobacco and pregnancy: overview of exposures and effects. Birth Defects Res. C Embryo Today 84, 1–15 (2008).
  CAS PubMed Google Scholar
• Hollins, K. Consequences of antenatal mental health problems for child health and development. Curr. Opin. Obstet. Gynecol. 19, 568–572 (2007).
  PubMed Google Scholar
• Hack, M. Young adult outcomes of very-low-birth-weight children. Semin. Fetal Neonatal Med. 11, 127–137 (2006).
  PubMed Google Scholar
• Gianni, M. L. et al. Twelve-month neurofunctional assessment and cognitive performance at 36 months of age in extremely low birth weight infants. Pediatrics 120, 1012–1019 (2007).
  PubMed Google Scholar
• Lambe, M., Hultman, C., Torrang, A., Maccabe, J. & Cnattingius, S. Maternal smoking during pregnancy and school performance at age 15. Epidemiology 17, 524–530 (2006).
  PubMed Google Scholar
• George, L., Granath, F., Johansson, A. L., Anneren, G. & Cnattingius, S. Environmental tobacco smoke and risk of spontaneous abortion. Epidemiology 17, 500–505 (2006).
  PubMed Google Scholar
• Cnattingius, S. The epidemiology of smoking during pregnancy: smoking prevalence, maternal characteristics, and pregnancy outcomes. Nicotine Tob. Res. 6 (Suppl. 2), S125–S140 (2004).
  PubMed Google Scholar
• DiFranza, J. R., Aligne, C. A. & Weitzman, M. Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113, 1007–1015 (2004).
  PubMed Google Scholar
• Fried, P. A., Watkinson, B. & Gray, R. Differential effects on cognitive functioning in 13- to 16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 25, 427–436 (2003).
  CAS PubMed Google Scholar
• Fried, P. A. & Watkinson, B. Differential effects on facets of attention in adolescents prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 23, 421–430 (2001).
  CAS PubMed Google Scholar
• Makin, J., Fried, P. A. & Watkinson, B. A comparison of active and passive smoking during pregnancy: long-term effects. Neurotoxicol. Teratol. 13, 5–12 (1991).
  CAS PubMed Google Scholar
• Eskenazi, B., Prehn, A. W. & Christianson, R. E. Passive and active maternal smoking as measured by serum cotinine: the effect on birthweight. Am. J. Public Health 85, 395–398 (1995).
  CAS PubMed PubMed Central Google Scholar
• Langley, K., Rice, F., van den Bree, M. B. & Thapar, A. Maternal smoking during pregnancy as an environmental risk factor for attention deficit hyperactivity disorder behaviour. A review. Minerva Pediatr. 57, 359–371 (2005).
  CAS PubMed Google Scholar
• Gaither, K. H., Huber, L. R., Thompson, M. E. & Huet-Hudson, Y. M. Does the use of nicotine replacement therapy during pregnancy affect pregnancy outcomes? Matern. Child Health J. 14 May 2008 (doi: 10.1007/s10995-008-0361-1).
  PubMed Google Scholar
• Schroeder, D. R. et al. Nicotine patch use in pregnant smokers: smoking abstinence and delivery outcomes. J. Matern. Fetal Neonatal Med. 11, 100–107 (2002).
  CAS PubMed Google Scholar
• Pauly, J. R. & Slotkin, T. A. Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr. 97, 1331–1337 (2008).
  PubMed Google Scholar
• Slotkin, T. A. 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 (2008).
  CAS PubMed Google Scholar
• Sarasin, A. et al. 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 (2003).
  CAS PubMed Google Scholar
• Dwyer, J. B., Broide, R. S. & Leslie, F. M. Nicotine and brain development. Birth Defects Res. C Embryo Today 84, 30–44 (2008).
  CAS PubMed Google Scholar
• Navarro, H. A. et al. Prenatal exposure to nicotine impairs nervous system development at a dose which does not affect viability or growth. Brain Res. Bull. 23, 187–192 (1989).
  CAS PubMed Google Scholar
• Roy, T. S., Seidler, F. J. & Slotkin, T. A. Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J. Pharmacol. Exp. Ther. 300, 124–133 (2002).
  CAS PubMed Google Scholar
• Paz, R., Barsness, B., Martenson, T., Tanner, D. & Allan, A. M. Behavioral teratogenicity induced by nonforced maternal nicotine consumption. Neuropsychopharmacology 32, 693–699 (2007).
  CAS PubMed Google Scholar
• Levin, E. D. et al. Increased nicotine self-administration following prenatal exposure in female rats. Pharmacol. Biochem. Behav. 85, 669–674 (2006).
  CAS PubMed PubMed Central Google Scholar
• Vaglenova, J., Birru, S., Pandiella, N. M. & Breese, C. R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav. Brain Res. 150, 159–170 (2004).
  CAS PubMed Google Scholar
• Slotkin, T. A. Fetal nicotine or cocaine exposure: which one is worse? J. Pharmacol. Exp. Ther. 285, 931–945 (1998).
  CAS PubMed Google Scholar
• Sarter, M., Hasselmo, M. E., Bruno, J. P. & Givens, B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Brain Res. Rev. 48, 98–111 (2005).
  CAS PubMed Google Scholar
• Liang, K. et al. Neonatal nicotine exposure impairs nicotinic enhancement of central auditory processing and auditory learning in adult rats. Eur. J. Neurosci. 24, 857–866 (2006).
  PubMed Google Scholar
• Barbieri, R. L., Gochberg, J. & Ryan, K. J. Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J. Clin. Invest. 77, 1727–1733 (1986).
  CAS PubMed PubMed Central Google Scholar
• Fried, P. A., James, D. S. & Watkinson, B. Growth and pubertal milestones during adolescence in offspring prenatally exposed to cigarettes and marihuana. Neurotoxicol. Teratol. 23, 431–436 (2001).
  CAS PubMed Google Scholar
• Treiman, D. M. GABAergic mechanisms in epilepsy. Epilepsia 42 (Suppl. 3), 8–12 (2001).
  PubMed Google Scholar
• Huang, Z. J., Di Cristo, G. & Ango, F. Development of GABA innervation in the cerebral and cerebellar cortices. Nature Rev. Neurosci. 8, 673–686 (2007).
  CAS Google Scholar
• Feng, M. J., Yan, S. E. & Yan, Q. S. Effects of prenatal alcohol exposure on brain-derived neurotrophic factor and its receptor tyrosine kinase B in offspring. Brain Res. 1042, 125–132 (2005).
  CAS PubMed Google Scholar
• Miller, M. W. Expression of transforming growth factor-β in developing rat cerebral cortex: effects of prenatal exposure to ethanol. J. Comp. Neurol. 460, 410–424 (2003).
  CAS PubMed Google Scholar
• Borodinsky, L. N. et al. GABA-induced neurite outgrowth of cerebellar granule cells is mediated by GABAA receptor activation, calcium influx and CaMKII and erk1/2 pathways. J. Neurochem. 84, 1411–1420 (2003).
  CAS PubMed Google Scholar
• Schwartz, J. P. Neurotransmitters as neurotrophic factors: a new set of functions. Int. Rev. Neurobiol. 34, 1–23 (1992).
  CAS PubMed Google Scholar
• Schwartz, M. L. & Meinecke, D. L. Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. Cereb. Cortex 2, 16–37 (1992).
  CAS PubMed Google Scholar
• Walker, A., Rosenberg, M. & Balaban-Gil, K. Neurodevelopmental and neurobehavioral sequelae of selected substances of abuse and psychiatric medications in utero. Child Adolesc. Psychiatr. Clin. N. Am. 8, 845–867 (1999).
  CAS PubMed Google Scholar
• Kosofsky, B. E. Specificity of neurobehavioral outcomes associated with prenatal alcohol exposure. J. Womens Health 7, 603–604 (1998).
  CAS PubMed Google Scholar
• Chiriboga, C. A. Fetal alcohol and drug effects. Neurologist 9, 267–279 (2003).
  PubMed Google Scholar
• Bada, H. S. et al. Low birth weight and preterm births: etiologic fraction attributable to prenatal drug exposure. J. Perinatol. 25, 631–637 (2005).
  PubMed Google Scholar
• Loebstein, R. & Koren, G. Pregnancy outcome and neurodevelopment of children exposed in utero to psychoactive drugs: the Motherisk experience. J. Psychiatry Neurosci. 22, 192–196 (1997).
  CAS PubMed PubMed Central Google Scholar
• Fried, P. A., Watkinson, B. & Gray, R. A follow-up study of attentional behavior in 6-year-old children exposed prenatally to marihuana, cigarettes, and alcohol. Neurotoxicol. Teratol. 14, 299–311 (1992).
  CAS PubMed Google Scholar
• Linnet, K. M. et al. Maternal lifestyle factors in pregnancy risk of attention deficit hyperactivity disorder and associated behaviors: review of the current evidence. Am. J. Psychiatry 160, 1028–1040 (2003).
  PubMed Google Scholar
• Williams, J. H. & Ross, L. Consequences of prenatal toxin exposure for mental health in children and adolescents: a systematic review. Eur. Child Adolesc. Psychiatry 16, 243–253 (2007).
  PubMed Google Scholar
• Snow, M. E. & Keiver, K. Prenatal ethanol exposure disrupts the histological stages of fetal bone development. Bone 41, 181–187 (2007).
  CAS PubMed PubMed Central Google Scholar
• Simpson, M. E., Duggal, S. & Keiver, K. Prenatal ethanol exposure has differential effects on fetal growth and skeletal ossification. Bone 36, 521–532 (2005).
  CAS PubMed Google Scholar
• Johnston, M. C. & Bronsky, P. T. Prenatal craniofacial development: new insights on normal and abnormal mechanisms. Crit. Rev. Oral Biol. Med. 6, 368–422 (1995).
  CAS PubMed Google Scholar
• Randall, C. L. & Taylor, W. J. Prenatal ethanol exposure in mice: teratogenic effects. Teratology 19, 305–311 (1979).
  CAS PubMed Google Scholar
• Miller, M. W. & Dow-Edwards, D. L. Structural and metabolic alterations in rat cerebral cortex induced by prenatal exposure to ethanol. Brain Res. 474, 316–326 (1988).
  CAS PubMed Google Scholar
• Miller, M. W. Effect of prenatal exposure to ethanol on glutamate and GABA immunoreactivity in macaque somatosensory and motor cortices: critical timing of exposure. Neuroscience 138, 97–107 (2006).
  CAS PubMed Google Scholar
• Miller, M. W. Effect of early exposure to ethanol on the protein and DNA contents of specific brain regions in the rat. Brain Res. 734, 286–294 (1996).
  CAS PubMed Google Scholar
• Mooney, S. M. & Miller, M. W. Episodic exposure to ethanol during development differentially affects brainstem nuclei in the macaque. J. Neurocytol. 30, 973–982 (2001).
  CAS PubMed Google Scholar
• Barrow Heaton, M. B. et al. Prenatal ethanol exposure reduces spinal cord motoneuron number in the fetal rat but does not affect GDNF target tissue protein. Dev. Neurosci. 21, 444–452 (1999).
  CAS PubMed Google Scholar
• Shetty, A. K. & Phillips, D. E. Effects of prenatal ethanol exposure on the development of Bergmann glia and astrocytes in the rat cerebellum: an immunohistochemical study. J. Comp. Neurol. 321, 19–32 (1992).
  CAS PubMed Google Scholar
• Redila, V. A. et al. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 16, 305–311 (2006).
  CAS PubMed Google Scholar
• Ozer, E., Sarioglu, S. & Gure, A. Effects of prenatal ethanol exposure on neuronal migration, neuronogenesis and brain myelination in the mice brain. Clin. Neuropathol. 19, 21–25 (2000).
  CAS PubMed Google Scholar
• Honse, Y., Nixon, K. M., Browning, M. D. & Leslie, S. W. Cell surface expression of NR1 splice variants and NR2 subunits is modified by prenatal ethanol exposure. Neuroscience 122, 689–698 (2003).
  CAS PubMed Google Scholar
• Hughes, P. D., Wilson, W. R. & Leslie, S. W. Effect of gestational ethanol exposure on the NMDA receptor complex in rat forebrain: from gene transcription to cell surface. Brain Res. Dev. Brain Res. 129, 135–145 (2001).
  CAS PubMed Google Scholar
• Zhang, X., Sliwowska, J. H. & Weinberg, J. Prenatal alcohol exposure and fetal programming: effects on neuroendocrine and immune function. Exp. Biol. Med. (Maywood) 230, 376–388 (2005).
  CAS Google Scholar
• Wilcoxon, J. S., Kuo, A. G., Disterhoft, J. F. & Redei, E. E. Behavioral deficits associated with fetal alcohol exposure are reversed by prenatal thyroid hormone treatment: a role for maternal thyroid hormone deficiency in FAE. Mol. Psychiatry 10, 961–971 (2005).
  CAS PubMed Google Scholar
• Champagne, F. & Meaney, M. J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity. Prog. Brain Res. 133, 287–302 (2001).
  CAS PubMed Google Scholar
• Kallen, B. & Otterblad Olausson, P. Antidepressant drugs during pregnancy and infant congenital heart defect. Reprod. Toxicol. 21, 221–222 (2006).
  PubMed Google Scholar
• Kallen, B. A. & Otterblad Olausson, P. Maternal drug use in early pregnancy and infant cardiovascular defect. Reprod. Toxicol. 17, 255–261 (2003).
  CAS PubMed Google Scholar
• Buznikov, G. A., Shmukler, Y. B. & Lauder, J. M. From oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell. Mol. Neurobiol. 16, 537–559 (1996).
  CAS PubMed Google Scholar
• Lauder, J. M. Hormonal and humoral influences on brain development. Psychoneuroendocrinology 8, 121–155 (1983).
  CAS PubMed Google Scholar
• Whitaker-Azmitia, P. M., Druse, M., Walker, P. & Lauder, J. M. Serotonin as a developmental signal. Behav. Brain Res. 73, 19–29 (1996).
  CAS PubMed Google Scholar
• Bonnin, A., Peng, W., Hewlitt, W. & Levitt, P. Expression mapping of 5-HT1 serotonin receptor subtypes during fetal and early postnatal mouse forebrain development. Neuroscience 141, 781–794 (2006).
  CAS PubMed Google Scholar
• Bonnin, A., Torii, M., Wang, L., Rakic, P. & Levitt, P. Serotonin modulates the response of embryonic thalamocortical axons to netrin-1. Nature Neurosci. 10, 588–597 (2007).
  CAS PubMed Google Scholar
• Lambe, E. K., Krimer, L. S. & Goldman-Rakic, P. S. Differential postnatal development of catecholamine and serotonin inputs to identified neurons in prefrontal cortex of rhesus monkey. J. Neurosci. 20, 8780–8787 (2000).
  CAS PubMed PubMed Central Google Scholar
• Whitaker-Azmitia, P. M., Lauder, J. M., Shemmer, A. & Azmitia, E. C. Postnatal changes in serotonin receptors following prenatal alterations in serotonin levels: further evidence for functional fetal serotonin receptors. Brain Res. 430, 285–289 (1987).
  CAS PubMed Google Scholar
• Persico, A. M., Di Pino, G. & Levitt, P. Multiple receptors mediate the trophic effects of serotonin on ventroposterior thalamic neurons in vitro. Brain Res. 1095, 17–25 (2006).
  CAS PubMed Google Scholar
• Gross, C. et al. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416, 396–400 (2002).
  CAS PubMed Google Scholar
• Ansorge, M. S., Zhou, M., Lira, A., Hen, R. & Gingrich, J. A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 306, 879–881 (2004).
  CAS PubMed Google Scholar
• Maschi, S. et al. Neonatal outcome following pregnancy exposure to antidepressants: a prospective controlled cohort study. BJOG 115, 283–289 (2008).
  CAS PubMed Google Scholar
• Andrade, S. E. et al. Use of antidepressant medications during pregnancy: a multisite study. Am. J. Obstet. Gynecol. 198, 194 e1–e5 (2008).
  PubMed Google Scholar
• Pearson, K. H. et al. Birth outcomes following prenatal exposure to antidepressants. J. Clin. Psychiatry 68, 1284–1289 (2007).
  CAS PubMed Google Scholar
• Oberlander, T. F. et al. Infant serotonin transporter (SLC6A4) promoter genotype is associated with adverse neonatal outcomes after prenatal exposure to serotonin reuptake inhibitor medications. Mol. Psychiatry 13, 65–73 (2008).
  CAS PubMed Google Scholar
• Einarson, A. et al. Evaluation of the risk of congenital cardiovascular defects associated with use of paroxetine during pregnancy. Am. J. Psychiatry 165, 749–752 (2008).
  PubMed Google Scholar
• Zuo, J. et al. Distinct neurobehavioral consequences of prenatal exposure to sulpiride (SUL) and risperidone (RIS) in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 387–397 (2008).
  CAS PubMed Google Scholar
• Singh, Y., Jaiswal, A. K., Singh, M. & Bhattacharya, S. K. Effect of prenatal haloperidol administration on anxiety patterns in rats. Indian J. Exp. Biol. 35, 1284–1290 (1997).
  CAS PubMed Google Scholar
• Castro, R., Brito, B., Segovia, J., Martin-Trujillo, J. M. & Notario, V. Prenatal haloperidol induces a selective reduction in the expression of plasticity-related genes in neonate rat forebrain. Brain Res. Mol. Brain Res. 26, 74–80 (1994).
  CAS PubMed Google Scholar
• Leonard, B. E. Effect of psychotropic drugs administered to pregnant rats on the behaviour of the offspring. Neuropharmacology 20, 1237–1242 (1981).
  CAS PubMed Google Scholar
• Miller, J. C. & Friedhoff, A. J. Prenatal neurotransmitter programming of postnatal receptor function. Prog. Brain Res. 73, 509–522 (1988).
  CAS PubMed Google Scholar
• Trixler, M., Gati, A., Fekete, S. & Tenyi, T. Use of antipsychotics in the management of schizophrenia during pregnancy. Drugs 65, 1193–1206 (2005).
  CAS PubMed Google Scholar
• Gentile, S. Clinical utilization of atypical antipsychotics in pregnancy and lactation. Ann. Pharmacother. 38, 1265–1271 (2004).
  CAS PubMed Google Scholar
• Landmark, C. J. Targets for antiepileptic drugs in the synapse. Med. Sci. Monit. 13, RA1–RA7 (2007).
  CAS PubMed Google Scholar
• Gottlicher, M. Valproic acid: an old drug newly discovered as inhibitor of histone deacetylases. Ann. Hematol. 83 (Suppl. 1), S91–S92 (2004).
  PubMed Google Scholar
• Carrim, Z. I., McKay, L., Sidiki, S. S. & Lavy, T. E. Early intervention for the ocular and neurodevelopmental sequelae of Fetal Valproate Syndrome. J. Paediatr. Child. Health 43, 643–645 (2007).
  PubMed Google Scholar
• Duncan, S. Teratogenesis of sodium valproate. Curr. Opin. Neurol. 20, 175–180 (2007).
  CAS PubMed Google Scholar
• Schneider, T. et al. Gender-specific behavioral and immunological alterations in an animal model of autism induced by prenatal exposure to valproic acid. Psychoneuroendocrinology 33, 728–740 (2008).
  CAS PubMed Google Scholar
• Schneider, T. & Przewlocki, R. Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30, 80–89 (2005).
  CAS PubMed Google Scholar
• Rinaldi, T., Kulangara, K., Antoniello, K. & Markram, H. Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc. Natl Acad. Sci. USA 104, 13501–13506 (2007).
  CAS PubMed PubMed Central Google Scholar
• Rinaldi, T., Silberberg, G. & Markram, H. Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb. Cortex 18, 763–770 (2008).
  PubMed Google Scholar
• Travis, B. E. & McCullough, J. M. Pharmacotherapy of preterm labor. Pharmacotherapy 13, 28–36 (1993).
  CAS PubMed Google Scholar
• Zerrate, M. C. et al. Neuroinflammation and behavioral abnormalities after neonatal terbutaline treatment in rats: implications for autism. J. Pharmacol. Exp. Ther. 322, 16–22 (2007).
  CAS PubMed Google Scholar
• Meyer, A., Seidler, F. J., Aldridge, J. E. & Slotkin, T. A. Developmental exposure to terbutaline alters cell signaling in mature rat brain regions and augments the effects of subsequent neonatal exposure to the organophosphorus insecticide chlorpyrifos. Toxicol. Appl. Pharmacol. 203, 154–166 (2005).
  CAS PubMed Google Scholar
• Rhodes, M. C. et al. Terbutaline is a developmental neurotoxicant: effects on neuroproteins and morphology in cerebellum, hippocampus, and somatosensory cortex. J. Pharmacol. Exp. Ther. 308, 529–537 (2004).
  CAS PubMed Google Scholar
• Pitzer, M., Schmidt, M. H., Esser, G. & Laucht, M. Child development after maternal tocolysis with beta-sympathomimetic drugs. Child Psychiatry Hum. Dev. 31, 165–182 (2001).
  CAS PubMed Google Scholar
• Hadders-Algra, M., Touwen, B. C. & Huisjes, H. J. Long-term follow-up of children prenatally exposed to ritodrine. Br. J. Obstet. Gynaecol. 93, 156–161 (1986).
  CAS PubMed Google Scholar
• Connors, S. L. et al. beta2-adrenergic receptor activation and genetic polymorphisms in autism: data from dizygotic twins. J. Child Neurol. 20, 876–884 (2005).
  PubMed Google Scholar
• Thornton, J. G. Maintenance tocolysis. BJOG 112 (Suppl. 1), 118–121 (2005).
  CAS PubMed Google Scholar
• Reese, S., Gandy, O. & Grant, A. (eds) Framing Public Life: Perspectives on Media and Our Understanding of the Social World (Lawrence Erlbaum Associates, Philadelphia, 1993).
  Google Scholar
• Entman, R. M. Framing: toward clarification of a fractured paradigm. J. Commun. 43, 51–58 (1993).
  Google Scholar
• Entman, R. M. Projections of Power (Univ. Chicago Press, 2004).
  Google Scholar
• Bales, S. N. Communicating early childhood education: using strategic frame analysis to shape dialogue. Bulletin of Zero to Three 19 (1999).
• National Advisory Mental Health Council. Transformative neurodevelopmental research in mental illness. National Institute of Mental Health [online], (2008).
• Whitaker-Azmitia, P. M. Serotonin and brain development: role in human developmental diseases. Brain Res. Bull. 56, 479–485 (2001).
  CAS PubMed Google Scholar
• Represa, A. & Ben-Ari, Y. Trophic actions of GABA on neuronal development. Trends Neurosci. 28, 278–283 (2005).
  CAS PubMed Google Scholar
• Nguyen, L. et al. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305, 187–202 (2001).
  CAS PubMed Google Scholar
• Lauder, J. M. & Schambra, U. B. Morphogenetic roles of acetylcholine. Environ. Health Perspect. 107 (Suppl. 1), 65–69 (1999).
  CAS PubMed PubMed Central Google Scholar
• Levitt, P., Harvey, J. A., Friedman, E., Simansky, K. & Murphy, E. H. New evidence for neurotransmitter influences on brain development. Trends Neurosci. 20, 269–274 (1997).
  CAS PubMed Google Scholar
• Song, Z. M. et al. D1 dopamine receptor regulation of microtubule-associated protein-2 phosphorylation in developing cerebral cortical neurons. J. Neurosci. 22, 6092–6105 (2002).
  CAS PubMed PubMed Central Google Scholar
• Lauder, J. M., Wallace, J. A. & Krebs, H. Roles for serotonin in neuroembryogenesis. Adv. Exp. Med. Biol. 133, 477–506 (1981).
  CAS PubMed Google Scholar
• Behar, T. N., Schaffner, A. E., Scott, C. A., Greene, C. L. & Barker, J. L. GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb. Cortex 10, 899–909 (2000).
  CAS PubMed Google Scholar
• Brazel, C. Y., Nunez, J. L., Yang, Z. & Levison, S. W. Glutamate enhances survival and proliferation of neural progenitors derived from the subventricular zone. Neuroscience 131, 55–65 (2005).
  CAS PubMed Google Scholar
• Budetti, P. P. et al. ED359734 - An Analysis of Resources to Aid Drug-Exposed Infants and Their Families (George Washington Univ., Washington DC, 1993).
  Google Scholar
• Poland, M. L., Dombrowski, M. P., Ager, J. W. & Sokol, R. J. Punishing pregnant drug users: enhancing the flight from care. Drug Alcohol Depend. 31, 199–203 (1993).
  CAS PubMed Google Scholar
• Annas, G. J. Testing poor pregnant patients for cocaine–physicians as police investigators. N. Engl. J. Med. 344, 1729–1732 (2001).
  CAS PubMed Google Scholar
• US Supreme Court Center. Ferguson et al. v. City of Charleston et al. 532 U.S. 67. Justia.com[online], (2001).
• The State of South Carolina in The Supreme Court. McKnight v. State of South Carolina, 26484. South Carolina Judicial Department [online], (2008).
• Rakic, P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18, 383–388 (1995).
  CAS PubMed Google Scholar
• Stanwood, G. D. & Levitt, P. in Handbook of Developmental Cognitive Neuroscience 2nd edn (eds Nelson, C. A. & Luciana, M.) 83–94 (MIT Press, 2008).
  Google Scholar