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Prenatal Nicotine Exposure Mouse Model Showing Hyperactivity, Reduced Cingulate Cortex Volume, Reduced Dopamine Turnover, and Responsiveness to Oral Methylphenidate Treatment
Open accessAbstract
Cigarette smoking, nicotine replacement therapy, and smokeless tobacco use during pregnancy are associated with cognitive disabilities later in life in children exposed prenatally to nicotine. The disabilities include attention deficit hyperactivity disorder (ADHD) and conduct disorder. However, the structural and neurochemical bases of these cognitive deficits remain unclear. Using a mouse model we show that prenatal nicotine exposure produces hyperactivity, selective decreases in cingulate cortical volume, and radial thickness, as well as decreased dopamine turnover in the frontal cortex. The hyperactivity occurs in both male and female offspring and peaks during the "active" or dark phase of the light/dark cycle. These features of the mouse model closely parallel the human ADHD phenotype, whether or not the ADHD is associated with prenatal nicotine exposure. A single oral, but not intraperitoneal, administration of a therapeutic equivalent dose (0.75 mg/kg) of methylphenidate decreases the hyperactivity and increases the dopamine turnover in the frontal cortex of the prenatally nicotine exposed mice, once again paralleling the therapeutic effects of this compound in ADHD subjects. Collectively, our data suggest that the prenatal nicotine exposure mouse model has striking parallels to the ADHD phenotype not only in behavioral, neuroanatomical, and neurochemical features, but also with respect to responsiveness of the behavioral phenotype to methylphenidate treatment. The behavioral, neurochemical, and anatomical biomarkers in the mouse model could be valuable for evaluating new therapies for ADHD and mechanistic investigations into its etiology.
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“For example, a mouse model has demonstrated that fetal exposure to nicotine yields hyperactivity, reduces cingulate cortex volume, reduces dopamine turnover and responsiveness to methylphenidate and might thereby lead to the identification of new pharmacotherapies 58 .”
From Attention-deficit/hyperactivity disorder (2015) · cites this paper as [58]
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“Similarly, a study using a mouse model found that PNE produced hyperactivity that was associated with selective decreases in cingulate cortical volume and radial thickness and a decrease in drug-induced dopamine release in the frontal cortex”
From Prenatal nicotine exposure during pregnancy results in adverse neurodevelopmental alterations and neurobehavioral deficits (2023) · cites this paper as [36]
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“For example, a mouse model has demonstrated that fetal exposure to nicotine yields hyperactivity, reduces cingulate cortex volume, reduces dopamine turnover and responsiveness to methylphenidate and might thereby lead to the identification of new pharmacotherapies 58 .”
From Attention-deficit/hyperactivity disorder (2015) · cites this paper as [58]
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“For example, a mouse model has demonstrated that fetal exposure to nicotine yields hyperactivity, reduces cingulate cortex volume, reduces dopamine turnover and responsiveness to methylphenidate and might thereby lead to the identification of new pharmacotherapies 58 .”
From Attention-deficit/hyperactivity disorder (2015) · cites this paper as [58]
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“For example, a mouse model has demonstrated that fetal exposure to nicotine yields hyperactivity, reduces cingulate cortex volume, reduces dopamine turnover and responsiveness to methylphenidate and might thereby lead to the identification of new pharmacotherapies 58 .”
From Attention-deficit/hyperactivity disorder (2015) · cites this paper as [58]
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Citations
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
International Journal of Epidemiology
Rothman, N., Garcia-closas, M., & Hein, D. W. (1973) · Journal of Medical Genetics · doi:10.1136/jmg.10.1.100-a · Cited by 2,837
Metabolism and Disposition Kinetics of Nicotine
Hukkanen, J., Jacob, P., & Benowitz, N. L. (2005) · Pharmacological Reviews · doi:10.1124/pr.57.1.3 · Cited by 1,583
Bush, G., Frazier, J. A., Rauch, S. L., Seidman, L. J., Whalen, P. J., Jenike, M. A., Rosen, B. R., & Biederman, J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00083-9 · Cited by 866
Self-citationBehavioral and Neural Consequences of Prenatal Exposure to Nicotine
ERNST, M., MOOLCHAN, E. T., & ROBINSON, M. L. (2001) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-200106000-00007 · Cited by 590
Presynaptic regulation of neurotransmitter release in the brain: Facts and hypothesis
Chesselet, M.-F. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90058-7 · Cited by 577
Slotkin, T. A. (2004) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2003.06.001 · Cited by 544
Stimulants: Therapeutic Actions in ADHD
Arnsten, A. F. T. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301164 · Cited by 473
Makris, N., Biederman, J., Valera, E. M., Bush, G., Kaiser, J., Kennedy, D. N., Caviness, V. S., Faraone, S. V., & Seidman, L. J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl047 · Cited by 450
Self-citationRodent Models of Attention-Deficit/Hyperactivity Disorder
Sagvolden, T., Russell, V. A., Aase, H., Johansen, E. B., & Farshbaf, M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.02.002 · Cited by 448
Milberger, S., Biederman, J., Faraone, S. V., Chen, L., & Jones, J. T. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.9.1138 · Cited by 414
Self-citationVolkow, N. D., Wang, G.-J., Fowler, J. S., & Ding, Y.-S. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.11.006 · Cited by 368
Kuczenski, R., & Segal, D. S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07264.2002 · Cited by 316
Thapar, A., Rice, F., Hay, D., Boivin, J., Langley, K., van den Bree, M. V. D., Rutter, M., & Harold, G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.05.032 · Cited by 308
Cingulate, Frontal, and Parietal Cortical Dysfunction in Attention-Deficit/Hyperactivity Disorder
Bush, G. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.01.022 · Cited by 304
Circadian blood nicotine concentrations during cigarette smoking
Benowitz, N. L., Kuyt, F., & Jacob, P. (1982) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.1982.233 · Cited by 290
Kuczenski, R. T., & Segal, D. S. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38829-9 · Cited by 267
Bolaños, C. A., Barrot, M., Berton, O., Wallace-Black, D., & Nestler, E. J. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00570-5 · Cited by 266
Altered responsiveness to cocaine in rats exposed to methylphenidate during development
Andersen, S. L., Arvanitogiannis, A., Pliakas, A. M., LeBlanc, C., & Carlezon, W. A. (2002) · Nature Neuroscience · doi:10.1038/nn777 · Cited by 259
Effects of Nicotine During Pregnancy: Human and Experimental Evidence
Wickstrom, R. (2007) · Current Neuropharmacology · doi:10.2174/157015907781695955 · Cited by 256
Gerasimov, M. R., Franceschi, M., Volkow, N. D., Gifford, A. J., Gatley, S. J., Marsteller, D. A., Molina, P. E., & Dewey, S. L. (2000) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38868-8 · Cited by 253
Enduring behavioral effects of early exposure to methylphenidate in rats
Carlezon, W. A., Mague, S. D., & Andersen, S. L. (2003) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.020 · Cited by 248
Animal models of attention-deficit hyperactivity disorder
Russell, V. A., Sagvolden, T., & Johansen, E. B. (2005) · Behavioral and Brain Functions · doi:10.1186/1744-9081-1-9 · Cited by 248
Milberger, S., Biederman, J., Faraone, S. V., & Jones, J. (1998) · Journal of Clinical Child Psychology · doi:10.1207/s15374424jccp2703_11 · Cited by 211
Self-citationDevelopmental consequences of prenatal tobacco exposure
Cornelius, M. D., & Day, N. L. (2009) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328326f6dc · Cited by 209
Sparks, J. A., & Pauly, J. R. (1999) · Psychopharmacology · doi:10.1007/s002130050818 · Cited by 188
Vaglenova, J., Birru, S., Pandiella, N. M., & Breese, C. R. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.07.005 · Cited by 180
Fried, P. A., & Watkinson, B. (2001) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(01)00160-x · Cited by 173
Navarro, H. A., Seidler, F. J., Schwartz, R. D., Baker, F. E., Dobbins, S. S., & Slotkin, T. A. (1989) · Brain Research Bulletin · doi:10.1016/0361-9230(89)90146-9 · Cited by 171
Crandall, J. E., McCarthy, D. M., Araki, K. Y., Sims, J. R., Ren, J.-Q., & Bhide, P. G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5124-06.2007 · Cited by 134
Self-citationPatrick, K. S., & Markowitz, J. S. (1997) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/(sici)1099-1077(199711/12)12:6 · Cited by 132
Seeman, P. M., & Madras, B. K. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00435-1 · Cited by 125
Slotkin, T. A., Cho, H., & Whitmore, W. L. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90130-4 · Cited by 124
Kuczenski, R. T., & Segal, D. S. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.036 · Cited by 121
Obel, C., Olsen, J. H., Henriksen, T. B., Rodriguez, A., Järvelin, M., Moilanen, I., Parner, E. T., Línnet, K., Taanila, A. M., Ebeling, H., et al. (2010) · International Journal of Epidemiology · doi:10.1093/ije/dyq185 · Cited by 118
Pauly, J. R., Sparks, J. A., Hauser, K. F., & Pauly, T. H. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.05.009 · Cited by 113
Muhammad, A., & Kolb, B. E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.015 · Cited by 110
Richardson, S. A., & Tizabi, Y. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90018-3 · Cited by 106
Behavioral Teratogenicity Induced by Nonforced Maternal Nicotine Consumption
Paz, R., Barsness, B., Martenson, T., Tanner, D., & Allan, A. M. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301066 · Cited by 105
Repeated methylphenidate treatment in adolescent rats alters gene regulation in the striatum
Brandon, C. L., & Steiner, H. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02892.x · Cited by 105
Schneider, T., Ilott, N., Brolese, G., Bizarro, L., Asherson, P. J. E., & Stolerman, I. P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.249 · Cited by 97
Behavioral and Brain Functions. A new journal
Sagvolden, T. (2005) · Behavioral and Brain Functions · doi:10.1186/1744-9081-1-1 · Cited by 89
Oral administration of nicotine: Its uptake and distribution after chronic administration to mice
Rowell, P. P., Hurst, H. E., Marlowe, C., & Bennett, B. D. (1983) · Journal of Pharmacological Methods · doi:10.1016/0160-5402(83)90064-5 · Cited by 81
Muhammad, A., & Kolb, B. E. (2011) · Developmental Neuroscience · doi:10.1159/000324744 · Cited by 73
Cocaine Alters BDNF Expression and Neuronal Migration in the Embryonic Mouse Forebrain
McCarthy, D. M., Zhang, X., Darnell, S. B., Sangrey, G. R., Yanagawa, Y., Sadri‐Vakili, G., & Bhide, P. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2944-11.2011 · Cited by 65
Self-citationBhide, P. G. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.01.006 · Cited by 60
Self-citationBalcioglu, A., Ren, J.-Q., McCarthy, D., Spencer, T. J., Biederman, J., & Bhide, P. G. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.07.025 · Cited by 60
Self-citationAnterior Cingulate Volumetric Alterations in Treatment-Naïve Adults With ADHD: A Pilot Study
Makris, N., Seidman, L. J., Valera, E. M., Biederman, J., Monuteaux, M. C., Kennedy, D. N., Caviness, V. S., Bush, G., Crum, K., Brown, A. B., et al. (2010) · Journal of Attention Disorders · doi:10.1177/1087054709351671 · Cited by 60
Self-citationRobbins, T. W. (2002) · Nature Medicine · doi:10.1038/nm0102-24 · Cited by 49
McCarthy, D. M., Lueras, P., & Bhide, P. G. (2007) · Brain Research · doi:10.1016/j.brainres.2007.08.088 · Cited by 47
Self-citationAugustyniak, P. N., Kourrich, S., Rezazadeh, S. M., Stewart, J., & Arvanitogiannis, A. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.09.014 · Cited by 37
Biederman, J., Petty, C. R., Bhide, P. G., Woodworth, K. Y., & Faraone, S. V. (2011) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.562243 · Cited by 22
Self-citationRen, J., Jiang, Y., Wang, Z., McCarthy, D. M., Rajadhyaksha, A. M., Tropea, T. F., Kosofsky, B. E., & Bhide, P. G. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.09.012 · Cited by 12
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Self-citationDevelopmental Consequences of Fetal Exposure to Drugs: What We Know and What We Still Must Learn
Ross, E. J., Graham, D. L., Money, K. M., & Stanwood, G. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.147 · Cited by 515
Human brain organoid-on-a-chip to model prenatal nicotine exposure
Wang, Y., Wang, L., Zhu, Y., & Qin, J. (2018) · Lab on a Chip · doi:10.1039/c7lc01084b · Cited by 330
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Karama, S., Ducharme, S., Corley, J., Chouinard-Decorte, F., Starr, J. M., Wardlaw, J. M., Bastin, M. E., & Deary, I. J. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.187 · Cited by 185
Maternal Smoking and Attention-Deficit/Hyperactivity Disorder in Offspring: A Meta-analysis
Huang, L., Wang, Y., Zhang, L., Zheng, Z., Zhu, T., Qu, Y., & Mu, D. (2018) · Pediatrics · doi:10.1542/peds.2017-2465 · Cited by 179
Metadata
- Authors
- Zhu, J., Zhang, X., Xu, Y., Spencer, T. J., Biederman, J., & Bhide, P. G.
- Affiliations
- Florida State University (US)
- Harvard University (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-07-04
- Volume
- 32
- Issue
- 27
- Pages
- 9410-9418
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3417040
- OpenAlex
- W2027221598
- Cited by
- 125
- References
- 53
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 5 · 2023: 10 · 2022: 15 · 2021: 7 · 2020: 10 · 2019: 11 · 2018: 10 · 2017: 10 · 2016: 8 · 2015: 10 · 2014: 8 · 2013: 7 · 2012: 1
- FWCI
- 7.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institute on Drug Abuse (R21DA027358, R01DA020796)
- National Institute of Neurological Disorders and Stroke (P30NS045776)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- prenatal nicotine exposure, attention deficit hyperactivity disorder, methylphenidate, dopamine turnover, cingulate cortex, cortical thickness, hyperactivity, frontal cortex, mouse model, maternal smoking, sex differences
- MeSH terms
- Animals, Attention Deficit Disorder with Hyperactivity, Disease Models, Animal, Dopamine, Female, Gyrus Cinguli, Male, Methylphenidate, Mice, Inbred C57BL, Models, Neurological, Nicotine, Pregnancy, Prenatal Exposure Delayed Effects, Smoking, Mice
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