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01-05-2016 | Original Article

Impact of prenatal nicotine on the structure of midbrain dopamine regions in the rat

Authors: Natalia Omelchenko, Priya Roy, Judith Joyce Balcita-Pedicino, Samuel Poloyac, Susan R. Sesack

Published in: Brain Structure and Function | Issue 4/2016

Abstract

In utero exposure of rats to nicotine (NIC) provides a useful animal model for studying the impact of smoking during pregnancy on human offspring. Certain sequelae of prenatal NIC exposure suggest an impact on the development of the midbrain dopamine (DA) system, which receives a robust cholinergic innervation from the mesopontine tegmentum. We therefore investigated whether prenatal NIC induced structural changes in cells and synapses within the midbrain that persisted into adulthood. Osmotic minipumps delivering either sodium bitartrate (vehicle; VEH) or NIC bitartrate at 2 mg/kg/day were implanted into nine timed-pregnant dams at E4. At birth, rat pups were culled to litters of six males each, and the litters were cross-fostered. Plasma levels of NIC and cotinine from killed pups provided evidence of NIC exposure in utero. Pups separated from dams at weaning showed a trend toward reduced locomotor activity at this time point but not when tested again in adulthood. Adult rats were killed for anatomical studies. Estimates of brain size and volume did not vary with NIC treatment. Midbrain sections stained for Nissl or by immunoperoxidase for tyrosine hydroxylase and analyzed using unbiased stereology revealed no changes in volume or cell number in the substantia nigra compacta or ventral tegmental area as a result of NIC exposure. Within the ventral tegmental area, electron microscopic physical disector analysis showed no significant differences in the number of axon terminals or the number of asymmetric (putative excitatory) or symmetric (putative inhibitory) synapses. Although too infrequent to estimate by unbiased stereology, no obvious difference in the proportion of cholinergic axons was noted in NIC- versus VEH-treated animals. These data suggest that activation of nicotinic receptors during prenatal development induces no significant modifications in the structure of cells in the ventral midbrain when assessed in adulthood.

Abdel-Rahman A, Dechkovskaia AM, Sutton JM, Chen WC, Guan X, Khan WA, Abou-Donia MB (2005) Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty. Toxicology 209:245–261PubMedCrossRef

Abreu-Villaca Y, Seidler FJ, Tate CA, Slotkin TA (2003) Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations. Brain Res 979:114–128PubMedCrossRef

Abreu-Villaca Y, Seidler FJ, Slotkin TA (2004a) Does prenatal nicotine exposure sensitize the brain to nicotine-induced neurotoxicity in adolescence? Neuropsychopharmacology 29:1440–1450PubMedCrossRef

Abreu-Villaca Y, Seidler FJ, Tate CA, Cousins MM, Slotkin TA (2004b) Prenatal nicotine exposure alters the response to nicotine administration in adolescence: effects on cholinergic systems during exposure and withdrawal. Neuropsychopharmacology 29:879–890PubMedCrossRef

Adriani W, Macri S, Pacifici R, Laviola G (2002) Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 27:212–224PubMedCrossRef

Adriani W, Spijker S, Deroche-Gamonet V, Laviola G, Le Moal M, Smit AB, Piazza PV (2003) Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats. J Neurosci 23:4712–4716PubMed

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

Andres RL, Day MC (2000) Perinatal complications associated with maternal tobacco use. Semin Neonatol 5:231–241PubMedCrossRef

Atluri P, Fleck MW, Shen Q, Mah SJ, Stadfelt D, Barnes W, Goderie SK, Temple S, Schneider AS (2001) Functional nicotinic acetylcholine receptor expression in stem and progenitor cells of the early embryonic mouse cerebral cortex. Dev Biol 240:143–156PubMedCrossRef

Audesirk T, Cabell L (1999) Nanomolar concentrations of nicotine and cotinine alter the development of cultured hippocampal neurons via non-acetylcholine receptor-mediated mechanisms. Neurotoxicology 20:639–646PubMed

Bardy AH, Seppala T, Lillsunde P, Kataja JM, Koskela P, Pikkarainen J, Hiilesmaa VK (1993) Objectively measured tobacco exposure during pregnancy: neonatal effects and relation to maternal smoking. Br J Obstet Gynaecol 100:721–726PubMedCrossRef

Bayer SA, Altman J (2007) The human brain during the early first trimester. Taylor & Francis, USACrossRef

Bayer VE, Pickel VM (1990) Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and neuronal associations. J Neurosci 10:2996–3013PubMed

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 14:83–144PubMed

Benowitz NL (1996a) Biomarkers of cigarette smoking. The FTC cigarette test method for determining tar, nicotine, and carbon monoxide yields of U.S. cigarettes. U.S. Department of Health and Human Services, Public Health Service, National Institutes of Health, Bethesda, pp 93–111

Benowitz NL (1996b) Pharmacology of nicotine: addiction and therapeutics. Annu Rev Pharmacol Toxicol 36:597–613PubMedCrossRef

Berger F, Gage FH, Vijayaraghavan S (1998) Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J Neurosci 18:6871–6881PubMed

Buchmann AF, Zohsel K, Blomeyer D, Hohm E, Hohmann S, Jennen-Steinmetz C, Treutlein J, Becker K, Banaschewski T, Schmidt MH, Esser G, Brandeis D, Poustka L, Zimmermann US, Laucht M (2014) Interaction between prenatal stress and dopamine D4 receptor genotype in predicting aggression and cortisol levels in young adults. Psychopharmacology 231:3089–3097PubMedCrossRef

Buka SL, Shenassa ED, Niaura R (2003) Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am J Psychiatry 160:1978–1984PubMedCrossRef

Buznikov GA, Shmukler YB, Lauder JM (1996) From oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell Mol Neurobiol 16:537–559PubMedCrossRef

Calverley RK, Bedi KS, Jones DG (1988) Estimation of the numerical density of synapses in rat neocortex. Comparison of the ‘disector’ with an ‘unfolding’ method. J Neurosci Methods 23:195–205PubMedCrossRef

Carr DB, Sesack SR (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864–3873PubMed

Chen WJ, Edwards RB (2003) Prenatal nicotine exposure does not cause Purkinje cell loss in the developing rat cerebellar vermis. Neurotoxicol Teratol 25:633–637PubMedCrossRef

Chen WJ, Parnell SE, West JR (1999) Effects of alcohol and nicotine on developing olfactory bulb: loss of mitral cells and alterations in neurotransmitter levels. Alcohol Clin Exp Res 23:18–25PubMed

Chen WJ, Edwards RB, Romero RD, Parnell SE, Monk RJ (2003) Long-term nicotine exposure reduces Purkinje cell number in the adult rat cerebellar vermis. Neurotoxicol Teratol 25:329–334PubMedCrossRef

Choy KH, de Visser YP, van den Buuse M (2009) The effect of ‘two hit’ neonatal and young-adult stress on dopaminergic modulation of prepulse inhibition and dopamine receptor density. Br J Pharmacol 156:388–396PubMedPubMedCentralCrossRef

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

Crooks PA, Dwoskin LP (1997) Contribution of CNS nicotine metabolites to the neuropharmacological effects of nicotine and tobacco smoking. Biochem Pharmacol 54:743–753PubMedCrossRef

Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9:251–259PubMedCrossRef

De Groot DM (1988) Comparison of methods for the estimation of the thickness of ultrathin tissue sections. J Microsc 151:23–42PubMedCrossRef

Dempsey D, Jacob P 3rd, Benowitz NL (2000) Nicotine metabolism and elimination kinetics in newborns. Clin Pharmacol Ther 67:458–465PubMedCrossRef

DiFranza JR, Lew RA (1995) Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. J Fam Pract 40:385–394PubMed

Dorph-Petersen KA, Pierri JN, Perel JM, Sun Z, Sampson AR, Lewis DA (2005) The influence of chronic exposure to antipsychotic medications on brain size before and after tissue fixation: a comparison of haloperidol and olanzapine in macaque monkeys. Neuropsychopharmacology 30:1649–1661PubMedCrossRef

Dwoskin LP, Teng L, Buxton ST, Crooks PA (1999) (S)-(-)-Cotinine, the major brain metabolite of nicotine, stimulates nicotinic receptors to evoke [3H]dopamine release from rat striatal slices in a calcium-dependent manner. J Pharmacol Exp Ther 288:905–911PubMed

El Marroun H, Schmidt MN, Franken IH, Jaddoe VW, Hofman A, van der Lugt A, Verhulst FC, Tiemeier H, White T (2014) Prenatal tobacco exposure and brain morphology: a prospective study in young children. Neuropsychopharmacology 39:792–800PubMedPubMedCentralCrossRef

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

Eskenazi B, Castorina R (1999) Association of prenatal maternal or postnatal child environmental tobacco smoke exposure and neurodevelopmental and behavioral problems in children. Environ Health Perspect 107:991–1000PubMedPubMedCentralCrossRef

Francis HW, Rivas A, Lehar M, Saito Y, Mouton PR, Ryugo DK (2006) Efficient quantification of afferent cochlear ultrastructure using design-based stereology. J Neurosci Methods 150:150–158PubMedCrossRef

Fucile S, Renzi M, Lauro C, Limatola C, Ciotti T, Eusebi F (2004) Nicotinic cholinergic stimulation promotes survival and reduces motility of cultured rat cerebellar granule cells. Neuroscience 127:53–61PubMedCrossRef

Fung YK (1988) Postnatal behavioural effects of maternal nicotine exposure in rats. J Pharm Pharmacol 40:870–872PubMedCrossRef

Fung YK (1989) Postnatal effects of maternal nicotine exposure on the striatal dopaminergic system in rats. J Pharm Pharmacol 41:576–578PubMedCrossRef

Fung YK, Lau YS (1989) Effects of prenatal nicotine exposure on rat striatal dopaminergic and nicotinic systems. Pharmacol Biochem Behav 33:1–6PubMedCrossRef

Geinisman Y, Gundersen HJ, van der Zee E, West MJ (1996) Unbiased stereological estimation of the total number of synapses in a brain region. J Neurocytol 25:805–819PubMedCrossRef

German DC, Manaye KF, Wu D, Hersh LB, Zweig RM (1999) Mesopontine cholinergic and non-cholinergic neurons in schizophrenia. Neuroscience 94:33–38PubMedCrossRef

Ghosheh O, Dwoskin LP, Li WK, Crooks PA (1999) Residence times and half-lives of nicotine metabolites in rat brain after acute peripheral administration of [2′-(14)C]nicotine. Drug Metab Dispos 27:1448–1455PubMed

Godding V, Bonnier C, Fiasse L, Michel M, Longueville E, Lebecque P, Robert A, Galanti L (2004) Does in utero exposure to heavy maternal smoking induce nicotine withdrawal symptoms in neonates? Pediatr Res 55:645–651PubMedCrossRef

Greenberg ME, Ziff EB, Greene LA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 234:80–83PubMedCrossRef

Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B et al (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857–881PubMedCrossRef

Hohmann CF (2003) A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 27:351–363PubMedCrossRef

Ingham CA, Hood SH, Taggart P, Arbuthnott GW (1998) Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J Neurosci 18:4732–4743PubMed

Jacob P 3rd, Wilson M, Benowitz NL (1981) Improved gas chromatographic method for the determination of nicotine and cotinine in biologic fluids. J Chromatogr 222:61–70PubMedCrossRef

Jorenby DE (1998) New developments in approaches to smoking cessation. Curr Opin Pulm Med 4:103–106PubMedCrossRef

Joschko MA, Dreosti IE, Tulsi RS (1991) The teratogenic effects of nicotine in vitro in rats: a light and electron microscope study. Neurotoxicol Teratol 13:307–316PubMedCrossRef

Kandel DB, Wu P, Davies M (1994) Maternal smoking during pregnancy and smoking by adolescent daughters. Am J Public Health 84:1407–1413PubMedPubMedCentralCrossRef

Kane VB, Fu Y, Matta SG, Sharp BM (2004) Gestational nicotine exposure attenuates nicotine-stimulated dopamine release in the nucleus accumbens shell of adolescent Lewis rats. J Pharmacol Exp Ther 308:521–528PubMedCrossRef

King BA, Alam S, Promoff G, Arrazola R, Dube SR (2013) Awareness and ever-use of electronic cigarettes among U.S. adults, 2010–2011. Nicotine Tob Res 15:1623–1627PubMedPubMedCentralCrossRef

Koob GF (1996) Hedonic valence, dopamine and motivation. Mol Psychiatry 1:186–189PubMed

Kunzler J, Braun K, Bock J (2013) Early life stress and sex-specific sensitivity of the catecholaminergic systems in prefrontal and limbic regions of Octodon degus. Brain Struct Funct (Epub ahead of print)

Lambers DS, Clark KE (1996) The maternal and fetal physiologic effects of nicotine. Semin Perinatol 20:115–126PubMedCrossRef

Leranth C, Roth RH, Elsworth JD, Naftolin F, Horvath TL, Redmond DE Jr (2000) Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: implications for Parkinson’s disease and memory. J Neurosci 20:8604–8609PubMed

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 85:575–583PubMedPubMedCentralCrossRef

Lichtensteiger W, Ribary U, Schlumpf M, Odermatt B, Widmer HR (1988) Prenatal adverse effects of nicotine on the developing brain. Prog Brain Res 73:137–157PubMedCrossRef

Lv J, Mao C, Zhu L, Zhang H, Pengpeng H, Xu F, Liu Y, Zhang L, Xu Z (2008) The effect of prenatal nicotine on expression of nicotine receptor subunits in the fetal brain. Neurotoxicology 29:722–726PubMedPubMedCentralCrossRef

Mayhew TM (1992) A review of recent advances in stereology for quantifying neural structure. J Neurocytol 21:313–328PubMedCrossRef

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 58:223–229PubMedCrossRef

Messi ML, Renganathan M, Grigorenko E, Delbono O (1997) Activation of alpha7 nicotinic acetylcholine receptor promotes survival of spinal cord motoneurons. FEBS Lett 411:32–38PubMedCrossRef

Muhammad A, Mychasiuk R, Nakahashi A, Hossain SR, Gibb R, Kolb B (2012) Prenatal nicotine exposure alters neuroanatomical organization of the developing brain. Synapse 66:950–954PubMedCrossRef

Muneoka K, Ogawa T, Kamei K, Muraoka S, Tomiyoshi R, Mimura Y, Kato H, Suzuki MR, Takigawa M (1997) Prenatal nicotine exposure affects the development of the central serotonergic system as well as the dopaminergic system in rat offspring: involvement of route of drug administrations. Brain Res Dev Brain Res 102:117–126PubMedCrossRef

Muneoka K, Nakatsu T, Fuji J, Ogawa T, Takigawa M (1999) Prenatal administration of nicotine results in dopaminergic alterations in the neocortex. Neurotoxicol Teratol 21:603–609PubMedCrossRef

Mychasiuk R, Muhammad A, Carroll C, Kolb B (2013a) Does prenatal nicotine exposure alter the brain’s response to nicotine in adolescence? A neuroanatomical analysis. Eur J Neurosci 38:2491–2503PubMedCrossRef

Mychasiuk R, Muhammad A, Gibb R, Kolb B (2013b) Long-term alterations to dendritic morphology and spine density associated with prenatal exposure to nicotine. Brain Res 1499:53–60PubMedCrossRef

Naeff B, Schlumpf M, Lichtensteiger W (1992) Pre- and postnatal development of high-affinity [3H]nicotine binding sites in rat brain regions: an autoradiographic study. Dev Brain Res 68:163–174CrossRef

Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, Ungless MA (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 152:1024–1031PubMedPubMedCentralCrossRef

Navarro HA, Seidler FJ, Whitmore WL, Slotkin TA (1988) Prenatal exposure to nicotine via maternal infusions: effects on development of catecholamine systems. J Pharmacol Exp Ther 244:940–944PubMed

Newman MB, Shytle RD, Sanberg PR (1999) Locomotor behavioral effects of prenatal and postnatal nicotine exposure in rat offspring. Behav Pharmacol 10:699–706PubMedCrossRef

Nguyen L, Rigo JM, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 305:187–202PubMedCrossRef

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 10:16–29PubMedCrossRef

Omelchenko N, Sesack SR (2005) Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 483:217–235PubMedCrossRef

Omelchenko N, Sesack SR (2006) Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol 494:863–875PubMedPubMedCentralCrossRef

Omelchenko N, Sesack SR (2007) Glutamate synaptic inputs to ventral tegmental area neurons in the rat derive primarily from subcortical sources. Neuroscience 146:1259–1274PubMedPubMedCentralCrossRef

Omelchenko N, Bell R, Sesack SR (2009) Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30:1239–1250PubMedPubMedCentralCrossRef

Onal A, Uysal A, Ulker S, Delen Y, Yurtseven ME, Evinc A (2004) Alterations of brain tissue in fetal rats exposed to nicotine in utero: possible involvement of nitric oxide and catecholamines. Neurotoxicol Teratol 26:103–112PubMedCrossRef

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 22:329–337PubMedCrossRef

Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, New York

Peters A, Palay SL, Webster HF (1991) The fine structure of the nervous system. Neurons and their supporting cells. Oxford University Press, New York

Phillipson OT (1979) Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol 187:117–144PubMedCrossRef

Pichini S, Basagana XB, Pacifici R, Garcia O, Puig C, Vall O, Harris J, Zuccaro P, Segura J, Sunyer J (2000) Cord serum cotinine as a biomarker of fetal exposure to cigarette smoke at the end of pregnancy. Environ Health Perspect 108:1079–1083PubMedPubMedCentralCrossRef

Qiao D, Seidler FJ, Violin JD, Slotkin TA (2003) Nicotine is a developmental neurotoxicant and neuroprotectant: stage-selective inhibition of DNA synthesis coincident with shielding from effects of chlorpyrifos. Brain Res Dev Brain Res 147:183–190PubMedCrossRef

Redgrave P, Prescott TJ, Gurney K (1999) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22:146–151PubMedCrossRef

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 248:786–792PubMed

Richardson SA, Tizabi Y (1994) Hyperactivity in the offspring of nicotine-treated rats: role of the mesolimbic and nigrostriatal dopaminergic pathways. Pharmacol Biochem Behav 47:331–337PubMedCrossRef

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

Romijn HJ, Hofman MA, Gramsbergen A (1991) At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev 26:61–67PubMedCrossRef

Roy TS, Sabherwal U (1994) Effects of prenatal nicotine exposure on the morphogenesis of somatosensory cortex. Neurotoxicol Teratol 16:411–421PubMedCrossRef

Roy TS, Sabherwal U (1998) Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol 20:465–473PubMedCrossRef

Roy TS, Seidler FJ, Slotkin TA (2002) Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300:124–133PubMedCrossRef

Saal D, Dong Y, Bonci A, Malenka RC (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577–582PubMedCrossRef

Santiago SE, Huffman KJ (2012) Postnatal effects of prenatal nicotine exposure on body weight, brain size and cortical connectivity in mice. Neurosci Res 73:282–291PubMedCrossRef

Scalera A, Koren G (1998) Rationale for treating pregnant smokers with nicotine patches. Can Fam Phys 44:1601–1603

Schneider AS, Atluri P, Shen Q, Barnes W, Mah SJ, Stadfelt D, Goderie SK, Temple S, Fleck MW (2002) Functional nicotinic acetylcholine receptor expression on stem and progenitor cells of the early embryonic nervous system. Ann N Y Acad Sci 971:135–138PubMedCrossRef

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 36:1114–1125PubMedPubMedCentralCrossRef

Seidler FJ, Albright ES, Lappi SE, Slotkin TA (1994) In search of a mechanism for receptor-mediated neurobehavioral teratogenesis by nicotine: catecholamine release by nicotine in immature rat brain regions. Dev Brain Res 82:1–8CrossRef

Sesack SR, Grace AA (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35:27–47PubMedPubMedCentralCrossRef

Sesack SR, Snyder CL, Lewis DA (1995) Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J Comp Neurol 363:264–280PubMedCrossRef

Shenassa ED, McCaffery JM, Swan GE, Khroyan TV, Shakib S, Lerman C, Lyons M, Mouttapa M, Niaura RS, Buka SL, Leslie F, Santangelo SL (2003) Intergenerational transmission of tobacco use and dependence: a transdisciplinary perspective. Nicotine Tob Res 5(Suppl 1):S55–69PubMedCrossRef

Slotkin TA (1998) Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther 285:931–945PubMed

Slotkin TA, Cho H, Whitmore WL (1987) Effects of prenatal nicotine exposure on neuronal development: selective actions on central and peripheral catecholaminergic pathways. Brain Res Bull 18:601–611PubMedCrossRef

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 750:180–188PubMedCrossRef

Smith SJ (1994) Neurobiology. Just a chemical attraction. Nature 368:101–102PubMedCrossRef

Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321–353PubMedCrossRef

Thomas JD, Garrison ME, Slawecki CJ, Ehlers CL, Riley EP (2000) Nicotine exposure during the neonatal brain growth spurt produces hyperactivity in preweanling rats. Neurotoxicol Teratol 22:695–701PubMedCrossRef

Tizabi Y, Popke EJ, Rahman MA, Nespor SM, Grunberg NE (1997) Hyperactivity induced by prenatal nicotine exposure is associated with an increase in cortical nicotinic receptors. Pharmacol Biochem Behav 58:141–146PubMedCrossRef

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 66:495–500PubMedCrossRef

Trauth JA, Seidler FJ, McCook EC, Slotkin TA (1999) Persistent c-fos induction by nicotine in developing rat brain regions: interaction with hypoxia. Pediatr Res 45:38–45PubMedCrossRef

Trauth JA, Seidler FJ, Slotkin TA (2000) An animal model of adolescent nicotine exposure: effects on gene expression and macromolecular constituents in rat brain regions. Brain Res 867:29–39PubMedCrossRef

Tribollet E, Bertrand D, Marguerat A, Raggenbass M (2004) Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 124:405–420PubMedCrossRef

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 150:159–170PubMedCrossRef

West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14:275–285PubMedCrossRef

Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12:2549–2554PubMed

Zhang X, Liu C, Miao H, Gong ZH, Nordberg A (1998) Postnatal changes of nicotinic acetylcholine receptor alpha 2, alpha 3, alpha 4, alpha 7 and beta 2 subunits genes expression in rat brain. Int J Dev Neurosci 16:507–518PubMedCrossRef

Zoli M, Le Novere N, Hill JA Jr, Changeux JP (1995) Developmental regulation of nicotinic ACh receptor subunit mRNAs in the rat central and peripheral nervous systems. J Neurosci 15:1912–1939PubMed

Title: Impact of prenatal nicotine on the structure of midbrain dopamine regions in the rat
Authors: Natalia Omelchenko
Priya Roy
Judith Joyce Balcita-Pedicino
Samuel Poloyac
Susan R. Sesack
Publication date: 01-05-2016
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2016
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-015-1014-y

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Impact of prenatal nicotine on the structure of midbrain dopamine regions in the rat

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