Gestational Nicotine Exposure Attenuates Nicotine-Stimulated Dopamine Release in the Nucleus Accumbens Shell of Adolescent Lewis Rats

The effects of chronic gestational exposure to nicotine on the nucleus accumbens dopamine response to acute nicotine were determined during adolescence (postnatal day 29–36) in cross-fostered and noncross-fostered Lewis rats. In both males and females, gestational nicotine exposure diminished the adolescent nucleus accumbens dopamine response to 0.07 mg/kg nicotine i.v. (p < 0.05). However, dopamine responses to 0.105 mg/kg nicotine were unaffected by gestational nicotine treatment and were similar in both genders. Furthermore, in both female and male gestational nicotine and control groups, the dopamine response to nicotine (0.105) was the same as that observed to the lower dose of nicotine in gestational controls. Thus, in adolescent male and female Lewis rats, gestational nicotine exposure attenuated nucleus accumbens dopamine release to a maximally stimulative dose of nicotine. Unexpectedly, in female gestational controls cross-fostering per se reduced nucleus accumbens dopamine secretion to 0.07 mg/kg nicotine (p < 0.05). These investigations suggest that gestational nicotine exposure could modify the acute reinforcing effects of nicotine in adolescent rats, whereas early postnatal stressors, (e.g., cross-fostering) may affect nicotine-induced reinforcement in female but not male adolescents.

[1]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[2]  T. Slotkin,et al.  Effects of prenatal nicotine exposure on biochemical development of rat brain regions: maternal drug infusions via osmotic minipumps. , 1987, The Journal of pharmacology and experimental therapeutics.

[3]  T. Slotkin,et al.  Prenatal exposure to nicotine via maternal infusions: effects on development of catecholamine systems. , 1988, The Journal of pharmacology and experimental therapeutics.

[4]  R. Heidel,et al.  Reducing the Health Consequences of Smoking: 25 Years of Progress. A Report of the Surgeon General. , 1989 .

[5]  U. Ribary,et al.  Effects of acute and chronic prenatal nicotine treatment on central catecholamine systems of male and female rat fetuses and offspring. , 1989, The Journal of pharmacology and experimental therapeutics.

[6]  Ting-kai Li,et al.  Effects of D1 and D2 dopamine receptor agents on ethanol consumption in the high-alcohol-drinking (HAD) line of rats. , 1993, Alcohol.

[7]  G. Koob,et al.  Dopamine receptor agonists, partial agonists and psychostimulant addiction. , 1994, Trends in pharmacological sciences.

[8]  Yousef Tizabi,et al.  Hyperactivity in the offspring of nicotine-treated rats: Role of the mesolimbic and nigrostriatal dopaminergic pathways , 1994, Pharmacology Biochemistry and Behavior.

[9]  D. Kandel,et al.  Maternal smoking during pregnancy and smoking by adolescent daughters. , 1994, American journal of public health.

[10]  Terje Sagvolden,et al.  Altered dopaminergic function in the prefrontal cortex, nucleus accumbens and caudate-putamen of an animal model of attention-deficit hyperactivity disorder — the spontaneously hypertensive rat , 1995, Brain Research.

[11]  Thomas J. H. Chen,et al.  Dopamine D2 receptor gene variants: association and linkage studies in impulsive-addictive-compulsive behaviour. , 1995, Pharmacogenetics.

[12]  W. Mcbride,et al.  Association between low contents of dopamine and serotonin in the nucleus accumbens and high alcohol preference. , 1995, Alcoholism, clinical and experimental research.

[13]  R. O'donnell,et al.  A Survey of Adolescent Smoking Patterns , 1996, The Journal of the American Board of Family Medicine.

[14]  S. Faraone,et al.  Is maternal smoking during pregnancy a risk factor for attention deficit hyperactivity disorder in children , 1996 .

[15]  John G. Cull,et al.  REWARD DEFICIENCY SYNDROME , 1996 .

[16]  J. Amin,et al.  Sustained Nicotine Exposure Differentially Affects α3β2 and α4β2 Neuronal Nicotinic Receptors Expressed in Xenopus Oocytes , 1996 .

[17]  A. Amos,et al.  Women and smoking. , 1996, British medical bulletin.

[18]  C C Presson,et al.  The natural history of cigarette smoking from adolescence to adulthood: demographic predictors of continuity and change. , 1996, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[19]  S. Matta,et al.  Printed in U.S.A. Copyright © 1997 by The Endocrine Society Adrenocorticotropin Response and Nicotine-Induced Norepinephrine Secretion in the Rat Paraventricular Nucleus Are Mediated through Brainstem Receptors* , 2022 .

[20]  Martin H. Teicher,et al.  Sex differences in dopamine receptor overproduction and elimination , 1997, Neuroreport.

[21]  S. Ikemoto,et al.  GABAA Receptor Blockade in the Anterior Ventral Tegmental Area Increases Extracellular Levels of Dopamine in the Nucleus Accumbens of Rats , 1997, Journal of neurochemistry.

[22]  J. Sergeant,et al.  Differential distribution, affinity and plasticity of dopamine D-1 and D-2 receptors in the target sites of the mesolimbic system in an animal model of ADHD , 1998, Behavioural Brain Research.

[23]  T. Slotkin Fetal nicotine or cocaine exposure: which one is worse? , 1998, The Journal of pharmacology and experimental therapeutics.

[24]  E. Rodríguez-Echandía,et al.  Effects of prenatal exposure to a mild chronic variable stress on body weight, preweaning mortality and rat behavior. , 1999, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[25]  J. Elster Addiction : entries and exits , 1999 .

[26]  Eliot L. Gardner,et al.  The neurobiology and genetics of addiction: Implications of the "reward deficiency syndrome" for therapeutic strategies in chemical dependency. , 1999 .

[27]  G. Chiara Drug addiction as dopamine-dependent associative learning disorder , 1999 .

[28]  Martin H. Teicher,et al.  Sex differences in dopamine receptors and their relevance to ADHD , 2000, Neuroscience & Biobehavioral Reviews.

[29]  M. Nyirenda,et al.  Programming hyperglycaemia in the rat through prenatal exposure to glucocorticoids-fetal effect or maternal influence? , 2001, The Journal of endocrinology.

[30]  Michele Zoli,et al.  Molecular and Physiological Diversity of Nicotinic Acetylcholine Receptors in the Midbrain Dopaminergic Nuclei , 2001, The Journal of Neuroscience.

[31]  A. Nordberg,et al.  Nicotine-induced alterations in the expression of nicotinic receptors in primary cultures from human prenatal brain , 2001, Neuroscience.

[32]  P. Garris,et al.  Partial, graded losses of dopamine terminals in the rat caudate-putamen: an animal model for the study of compensatory adaptation in preclinical parkinsonism , 2001, Journal of Neuroscience Methods.

[33]  J. Auman,et al.  Perinatal exposure to environmental tobacco smoke upregulates nicotinic cholinergic receptors in monkey brain. , 2002, Brain research. Developmental brain research.

[34]  David Satcher,et al.  Women and smoking: a report of the Surgeon General. , 2002, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[35]  S. Matta,et al.  Rat strain differences in nicotine self-administration using an unlimited access paradigm , 2002, Brain Research.

[36]  S. Faraone,et al.  Current concepts on the neurobiology of Attention-Deficit/Hyperactivity Disorder , 2002, Journal of attention disorders.

[37]  N. Rigotti,et al.  Development of symptoms of tobacco dependence in youths: 30 month follow up data from the DANDY study , 2002, Tobacco control.

[38]  T. Kosten,et al.  HPA axis function and drug addictive behaviors: insights from studies with Lewis and Fischer 344 inbred rats , 2002, Psychoneuroendocrinology.

[39]  K. Chergui,et al.  GABAB receptor-mediated modulation of the firing pattern of ventral tegmental area dopamine neurons in vivo , 2002, Naunyn-Schmiedeberg's Archives of Pharmacology.

[40]  T. Svensson,et al.  Differential effects of acute and chronic nicotine on dopamine output in the core and shell of the rat nucleus accumbens , 2005, Journal of Neural Transmission.