Evidence for enhanced neurobehavioral vulnerability to nicotine during periadolescence in rats
Open accessAbstract
Epidemiological studies indicate that there is an increased likelihood for the development of nicotine addiction when cigarette smoking starts early during adolescence. These observations suggest that adolescence could be a “critical” ontogenetic period, during which drugs of abuse have distinct effects responsible for the development of dependence later in life. We compared the long-term behavioral and molecular effects of repeated nicotine treatment during either periadolescence or postadolescence in rats. It was found that exposure to nicotine during periadolescence, but not a similar exposure in the postadolescent period, increased the intravenous self-administration of nicotine and the expression of distinct subunits of the ligand-gated acetylcholine receptor in adult animals. Both these changes indicated an increased sensitivity to the addictive properties of nicotine. In conclusion, adolescence seems to be a critical developmental period, characterized by enhanced neurobehavioral vulnerability to nicotine.
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Adolescent nicotine exposure increases later nicotine reward and reduces nicotine aversion in adult animals.
“Adolescent nicotine treatment increases subsequent nicotine reward and decreases aversion in adults”
From Unique, long-term effects of nicotine on adolescent brain. (2020) · cites this paper as Adriani et al., 2003
The Results report that nicotine pretreatment during periadolescence increased nicotine self-administration in adult rats, and the Discussion interprets this as greater sensitivity to nicotine’s reinforcing effects. Our copy does not report reduced nicotine aversion; searches for aversion and aversive effects did not find support for that part of the claim. No page numbers were available in the indexed passages. (LLM, conf=0.86)
Experimental — accuracy not yet measuredNicotine administration during adolescence, but not after, has long-lasting effects on cognitive, addictive, and emotional behavior in rats.
“Nicotine administration during, but not following, adolescence has long-lasting effects on cognitive, addictive, and emotional behavior in rats (Adriani et al. 2003; Iniguez et al. 2008; Counotte et al. 2009, 2011).”
From Short- and Long-Term Consequences of Nicotine Exposure during Adolescence for Prefrontal Cortex Neuronal Network Function (2012) · cites this paper as Adriani et al. 2003
The Results (page unavailable) report that nicotine pretreatment during periadolescence, but not postadolescence, increased nicotine self-administration in adult rats, supporting a lasting effect on addiction-related behavior. The paper does not report lasting effects on cognitive or emotional behavior from that treatment. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAdolescent rats are more susceptible than adult rats to nicotine's lasting effects on cognitive, addictive, and emotional behaviors.
“Adolescents are more vulnerable than adults to nicotine’s long-term effects on addictive and cognitive behavior.”
From Adolescent nicotine exposure transiently increases high-affinity nicotinic receptors and modulates inhibitory synaptic transmission in rat medial prefrontal cortex (2012) · cites this paper as [16]
The Results report that nicotine exposure during periadolescence, but not postadolescence, increased nicotine self-administration and motivation to obtain nicotine in adult rats. That supports a lasting difference in addiction-related behavior, but the paper does not establish lasting effects on cognitive behavior or the emotional behavior mentioned in the supplied paraphrase. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn rats, nicotine given during adolescence but not afterward has lasting effects on cognitive, addictive, and emotional behavior.
“Nicotine administration during, but not following, adolescence has long-lasting effects on cognitive, addictive, and emotional behavior in rats (16–19).”
From Adolescent nicotine exposure transiently increases high-affinity nicotinic receptors and modulates inhibitory synaptic transmission in rat medial prefrontal cortex (2012) · cites this paper as [16]
The Results report that nicotine pretreatment during periadolescence, but not postadolescence, increased nicotine self-administration in adult rats, supporting a lasting effect on addiction-related behavior. The paper does not report lasting effects on cognitive or emotional behavior. (LLM, conf=0.88)
Experimental — accuracy not yet measuredα4β2 and α7 nAchR expression and binding are higher in adolescents than adults.
“α4β2 and α7 nAchR expression and binding are higher in adolescents than adults [187, 188].”
From Consequences of adolescent drug use (2023) · cites this paper as [187]
The Discussion (page unavailable) says nAChRs are overexpressed in rat brains during adolescence relative to later life. It does not establish higher α4β2 or α7 expression or binding specifically. The reported β2 increase was measured in adults previously exposed to nicotine during periadolescence, not in adolescents compared with adults. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Mid-adolescent nicotine exposure (PND 34-43) increases expression of α5, α6, β2, and β3 nAChR subunits in the adult VTA, whereas the same exposure during adulthood only increases the β3 subunit.
“A similar mid-adolescent exposure regimen (PND 34–43) lead to an increased expression of α5, α6, β2, and β3 nAChR subunits in the adult VTA –– while the same exposure, given instead during adulthood, only increased the β3 subunit [117].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [117]
The nAChR gene expression section reports increased α5, α6, and β2 expression after periadolescent nicotine exposure, and increased β3 expression after exposure in either age group. However, the Methods describe the comparison group as postadolescent (P60–P69), rather than adult, and say the sampled tissue contained mainly VTA plus a small portion of substantia nigra; the finding is not strictly VTA-specific. (LLM, conf=0.85)
Experimental — accuracy not yet measuredLaboratory animals also show a difference in nicotine sensitivity between adolescents and adults.
“The difference in sensitivity to nicotine between adolescents and adults is also reported for laboratory animals (Slotkin 2002; Adriani et al. 2003).”
From Short- and Long-Term Consequences of Nicotine Exposure during Adolescence for Prefrontal Cortex Neuronal Network Function (2012) · cites this paper as Adriani et al. 2003
There are alterations in both right dorsal and left ventral frontostriatal tracts in young adult male smokers, which corresponded with poorer performance in cognitive tasks.
“there are alterations in both right dorsal and left ventral frontostriatal tracts in young adult male smokers, which corresponded with poorer performance in cognitive tasks [187, 188].”
From Consequences of adolescent drug use (2023) · cites this paper as [187]
The Statistical analyses and Discussion sections concern nicotine exposure, behavior, and receptor changes in rats. Searches for right dorsal and left ventral frontostriatal tracts and cognitive performance in young adult male smokers found no passage addressing those findings. The rat results do not contradict the human claim, but they cannot verify it. (LLM, conf=0.78)
Experimental — accuracy not yet measured
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Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
The neural basis of drug craving: An incentive-sensitization theory of addiction
Robinson, T. (1993) · Brain Research Reviews · doi:10.1016/0165-0173(93)90013-p · Cited by 7,346 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs.
Pontieri, F. E., Tanda, G., Orzi, F., & Chiara, G. D. (1996) · Nature · doi:10.1038/382255a0 · Cited by 1,073 · see citing works
Breslau, N., & Peterson, E. L. (1996) · American Journal of Public Health · doi:10.2105/ajph.86.2.214 · Cited by 682 · see citing works
Klink, R., d'Exaerde, A. D. K., Zoli, M., & Changeux, J.-P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01452.2001 · Cited by 674 · see citing works
Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain
Picciotto, M. R., Zoli, M., Léna, C., Bessis, A., Lallemand, Y., LeNovère, N., Vincent, P., Pich, E. M., Brûlet, P., & Changeux, J.-P. (1995) · Nature · doi:10.1038/374065a0 · Cited by 668 · see citing works
Laviola, G., Macrı̀, S., Morley-Fletcher, S., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00006-x · Cited by 621 · see citing works
Self-citationPiazza, P. V., Deminiere, J. M., le Moal, M., & Simon, H. (1990) · Brain Research · doi:10.1016/0006-8993(90)90431-a · Cited by 565 · see citing works
Self-citationPeriadolescence: age-dependent behavior and psychopharmacological responsivity in rats
Spear, L. P., & Brake, S. C. (1983) · Developmental Psychobiology · doi:10.1002/dev.420160203 · Cited by 539 · see citing works
Teicher, M. H., Andersen, S. L., & Hostetter, J. C. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(95)00109-q · Cited by 505 · see citing works
Loizou, L. A. (1972) · Brain Research · doi:10.1016/0006-8993(72)90142-4 · Cited by 394 · see citing works
Tirelli, E., Laviola, G., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00018-6 · Cited by 362 · see citing works
Self-citationPiazza, P. V., Deroche-Gamonent, V., Rougé‐Pont, F., & Moal, M. L. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04226.2000 · Cited by 353 · see citing works
Self-citationLaviola, G., Adriani, W., Terranova, M. L., & Gerra, G. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00032-9 · Cited by 345 · see citing works
Self-citationSex differences in dopamine receptor overproduction and elimination
Andersen, S. L., Rutstein, M. D., Benzo, J., Hostetter, J. C., & Teicher, M. H. (1997) · Neuroreport · doi:10.1097/00001756-199704140-00034 · Cited by 316 · see citing works
Effect of the Age at Which Smoking Begins on Frequency of Smoking in Adulthood
Taioli, E., & Wynder, E. L. (1991) · New England Journal of Medicine · doi:10.1056/nejm199109263251318 · Cited by 301 · see citing works
Extent of smoking and nicotine dependence in the United States: 19911993
Chen, D. B. K. (2000) · Nicotine & Tobacco Research · doi:10.1080/14622200050147538 · Cited by 261 · cited 1× · see citing works
“Several epidemiological studies indicate that there is an increased likelihood for the development of nicotine addiction when cigarette smoking starts early during adolescence (Taioli and Wynder, 1991; Breslau and Peterson, 1996; Kandel and Chen, 2000).”
BackgroundBehavioural neuroscience : a practical approach
Sahgal, A. (1993) · IRL Press eBooks · Cited by 242 · see citing works
Gerzanich, V., Wang, F., Kuryatov, A., & Lindstrom, J. M. (1998) · PubMed · Cited by 242 · see citing works
Nicotine self-administration in rats: strain and nicotine pre-exposure effects on acquisition
Shoaib, M., Schindler, C. W., & Goldberg, S. R. (1997) · Psychopharmacology · doi:10.1007/s002130050159 · Cited by 233 · see citing works
Trauth, J. A., Seidler, F. J., McCook, E. C., & Slotkin, T. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01994-0 · Cited by 230 · see citing works
Human α6 AChR subtypes: subunit composition, assembly, and pharmacological responses
Kuryatov, A., Olale, F., Cooper, J., Choi, C. H., & Lindstrom, J. M. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00144-1 · Cited by 223 · see citing works
Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence
Adriani, W. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00295-6 · Cited by 214 · see citing works
Self-citationPierre, P. J., & Vezina, P. (1997) · Psychopharmacology · doi:10.1007/s002130050191 · Cited by 197 · see citing works
The neurobiology of tobacco addiction
Stolerman, I. P., & Shoaib, M. C. (1991) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(91)90638-9 · Cited by 195 · see citing works
Cocaine sensitization in periadolescent and adult rats.
Giovanni Laviola, A., Wood, R. D., Kuhn, C. M., Francis, R., & SPEAR, L. P. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12056-9 · Cited by 195 · see citing works
Cocaine self‐administration increases the incentive motivational properties of the drug in rats
Deroche‐Gamonet, V., Moal, M. L., & Piazza, P. V. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00696.x · Cited by 178 · see citing works
Self-citationRisner, M. E., & Goldberg, S. R. (1983) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)33473-7 · Cited by 168 · see citing works
Trauth, J. A., Seidler, F. J., Ali, S. F., & Slotkin, T. A. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03227-3 · Cited by 150 · see citing works
Gerzanich, V., Wang, F., Kuryatov, A., & Lindstrom, J. M. (1998) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37589-5 · Cited by 129 · see citing works
Sensitization and Tolerance in Psychostimulant Self-Administration
Schenk, S., & Partridge, B. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00447-9 · Cited by 123 · see citing works
Naeff, B., Schlumpf, M., & LICHTENSTEIGER, W. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90058-5 · Cited by 115 · see citing works
Development and Ageing of the Rat Nigrostriatal Dopamine System Studied with Fast Cyclic Voltammetry
Stamford, J. A. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb09212.x · Cited by 102 · see citing works
Single channel properties of human α3 AChRs: impact of β2, β4 and α5 subunits
Nelson, M. E., & Lindstrom, J. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0657u.x · Cited by 92 · see citing works
Novère, N. G. L., Zoli, M., Léna, C., Ferrari, R., Picciotto, M. R., Merlo‐Pich, E., & Changeux, J. (1999) · Neuroreport · doi:10.1097/00001756-199908200-00012 · Cited by 86 · see citing works
Development of the nigrostriatal dopamine neuron and the pathways in the basal ganglia
Segawa, M. (2000) · Brain and Development · doi:10.1016/s0387-7604(00)00149-2 · Cited by 54 · see citing works
Léna, C., & Changeux, J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb11333.x · Cited by 28 · see citing works
Risner, M. E., & Cone, E. J. (1986) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(86)90041-4 · Cited by 25 · see citing works
Giordano, L. A., Bickel, W. K., Shahan, T. A., & Badger, G. J. (2001) · Behavioural Pharmacology · doi:10.1097/00008877-200109000-00005 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
How can drug addiction help us understand obesity?
Volkow, N. D., & Wise, R. A. (2005) · Nature Neuroscience · doi:10.1038/nn1452 · Cited by 1,089 · see citing works
Guidelines on nicotine dose selection for in vivo research
Matta, S. G., Balfour, D. J., Benowitz, N. L., Boyd, R. T., Buccafusco, J. J., Caggiula, A. R., Craig, C. R., Collins, A. C., Damaj, M. I., Donny, E. C., et al. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0441-0 · Cited by 824 · see citing works
Drug addiction: the neurobiology of behaviour gone awry
Volkow, N. D., & Li, T. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1539 · Cited by 620 · see citing works
<scp>N</scp> icotine and the adolescent brain
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 582 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · see citing works
Nicotine addiction and comorbidity with alcohol abuse and mental illness
Dani, J. A., & Harris, R. A. (2005) · Nature Neuroscience · doi:10.1038/nn1580 · Cited by 382 · see citing works
McCormick, C. M., & Zovkic, I. B. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.012 · Cited by 373 · see citing works
Piasecki, T. M. (2006) · Clinical Psychology Review · doi:10.1016/j.cpr.2005.11.007 · Cited by 370 · see citing works
Public Health Implications of Raising the Minimum Age of Legal Access to Tobacco Products
Board on Population Health and Public Health Practice (2015) · National Academies Press eBooks · doi:10.17226/18997 · Cited by 347 · see citing works
Risk Taking and Novelty Seeking in Adolescence: Introduction to Part I
KELLEY, A. E., SCHOCHET, T., & LANDRY, C. F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.003 · Cited by 325 · see citing works
Goriounova, N. A., & Mansvelder, H. D. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012120 · Cited by 307 · see citing works
“Nicotine administration during, but not following, adolescence has long-lasting effects on cognitive, addictive, and emotional behavior in rats (Adriani et al. 2003; Iniguez et al. 2008; Counotte et al. 2009, 2011).”
BackgroundDrugs as instruments: A new framework for non-addictive psychoactive drug use
Müller, C. P., & Schumann, G. (2011) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11000057 · Cited by 286 · see citing works
Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats
Belluzzi, J., Lee, A., Oliff, H., & Leslie, F. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1758-6 · Cited by 280 · see citing works
Weiss, R. B., Baker, T. B., Cannon, D. S., von Niederhausern, A., Dunn, D. M., Matsunami, N., Singh, N. A., Baird, L., Coon, H., McMahon, W. M., et al. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000125 · Cited by 271 · see citing works
Implications of CYP2A6 Genetic Variation for Smoking Behaviors and Nicotine Dependence*
Malaiyandi, V., Sellers, E. M., & Tyndale, R. F. (2005) · Clinical Pharmacology & Therapeutics · doi:10.1016/j.clpt.2004.10.011 · Cited by 268 · see citing works
Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model
Adriani, W., & Laviola, G. (2004) · Behavioural Pharmacology · doi:10.1097/00008877-200409000-00005 · Cited by 267 · see citing works
Self-citationAcetaldehyde Enhances Acquisition of Nicotine Self-Administration in Adolescent Rats
Belluzzi, J. D., Wang, R., & Leslie, F. M. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300586 · Cited by 245 · see citing works
Monique Ernst, D., Romeo, R. D., & Andersen, S. L. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.12.013 · Cited by 236 · see citing works
Consequences of adolescent drug use
Steinfeld, M. R., & Torregrossa, M. M. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02590-4 · Cited by 237 · see citing works
“For example, α4β2 and α7 nAchR expression and binding are higher in adolescents than adults [187, 188].”
BackgroundThe reality of comorbidity: Depression and drug abuse
Volkow, N. D. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.07.007 · Cited by 213 · see citing works
Slotkin, T. A. (2008) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2007.09.002 · Cited by 206 · see citing works
Nicotine dependence and reward differ between adolescent and adult male mice
Kota, D., Martin, B. R., Robinson, S. E., & Damaj, M. I. (2007) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.121616 · Cited by 202 · see citing works
SPEAR, L. P., & Swartzwelder, H. S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.04.012 · Cited by 202 · see citing works
Pistis, M., Perra, S., Pillolla, G., Melis, M., Muntoni, A. L., & Gessa, G. L. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.05.006 · Cited by 194 · see citing works
Shram, M. J., Funk, D., Li, Z., & Lê, A. D. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0373-8 · Cited by 192 · see citing works
Effects of Nicotine in Experimental Animals and Humans: An Update on Addictive Properties
Foll, B. L., & Goldberg, S. R. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-69248-5_12 · Cited by 194 · see citing works
England, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Unique, long-term effects of nicotine on adolescent brain.
Leslie, F. M. (2020) · Pharmacology, Biochemistry, and Behavior · doi:10.1016/j.pbb.2020.173010 · Cited by 178 · see citing works
“Adolescent nicotine treatment increases subsequent nicotine reward and decreases aversion in adults (Adriani et al., 2003; Torres et al., 2008; Kallupi et al., 2019).”
BackgroundNicotine Gateway Effects on Adolescent Substance Use
Ren, M., & Lotfipour, S. (2019) · Western Journal of Emergency Medicine · doi:10.5811/westjem.2019.7.41661 · Cited by 166 · see citing works
Long-Lasting Cognitive Deficits Resulting from Adolescent Nicotine Exposure in Rats
Counotte, D. S., Spijker, S., Van de Burgwal, L. H., Hogenboom, F., Schoffelmeer, A. N. M., De Vries, T. J., Smit, A. B., & Pattij, T. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.96 · Cited by 163 · see citing works
Self-citationSpontaneously hypertensive rats do not predict symptoms of attention-deficit hyperactivity disorder
van den Bergh, F. S., Bloemarts, E., Chan, J. S. W., Groenink, L., Olivier, B., & Oosting, R. S. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.02.018 · Cited by 164 · see citing works
Behavioral and Neurochemical Vulnerability During Adolescence in Mice: Studies with Nicotine
Adriani, W., Granstrem, O., Macrı̀, S., Izykenova, G. A., Dambinova, S. A., & Giovanni Laviola, A. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300366 · Cited by 164 · see citing works
Self-citationNicotine exposure during adolescence induces a depression-like state in adulthood
Iñiguez, S. D., Warren, B. L., Parise, E. M., Alcantara, L. F., Schuh, B., Maffeo, M. L., Manojlovic, Z., & Bolaños-Guzmán, C. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.220 · Cited by 157 · see citing works
Consequences of adolescent use of alcohol and other drugs: Studies using rodent models
SPEAR, L. P. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.026 · Cited by 154 · see citing works
Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction
O’Dell, L. E., Bruijnzeel, A. W., Smith, R. T., Parsons, L. H., Merves, M. L., Goldberger, B. A., Richardson, H. N., Koob, G. F., & Markou, A. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0383-6 · Cited by 153 · see citing works
Mechanisms of Action and Persistent Neuroplasticity by Drugs of Abuse
Korpi, E. R., den Hollander, B., Farooq, U., Vashchinkina, E., Rajkumar, R., Nutt, D. J., Hyytiä, P., & Dawe, G. S. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.010967 · Cited by 148 · see citing works
Levin, E. D., Lawrence, S. S., Petro, A., Horton, K., Rezvani, A. H., Seidler, F. J., & Slotkin, T. A. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2007.02.002 · Cited by 147 · see citing works
Role of acetaldehyde in tobacco smoke addiction
Talhout, R., Opperhuizen, A., & van Amsterdam, J. (2007) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2007.02.013 · Cited by 145 · see citing works
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144 · see citing works
Developmental regulation of nicotinic acetylcholine receptors within midbrain dopamine neurons
Azam, L., Chen, Y., & Leslie, F. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.011 · Cited by 138 · see citing works
Adolescent brain maturation and smoking: What we know and where we’re headed
Lydon‐Staley, D. M., Wilson, S. J., Child, A. E., & Geier, C. F. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.003 · Cited by 133 · see citing works
Nicotine as a typical drug of abuse in experimental animals and humans
Foll, B. L., & Goldberg, S. R. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0155-8 · Cited by 131 · see citing works
Synergistic interaction between nicotine and social rewards in adolescent male rats
Thiel, K. J., Sanabria, F., & Neisewander, J. L. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1470-2 · Cited by 131 · see citing works
Doura, M. B., Gold, A. B., Keller, A. B., & Perry, D. C. (2008) · Brain Research · doi:10.1016/j.brainres.2008.03.056 · Cited by 129 · see citing works
Lynch, W. J. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.07.004 · Cited by 122 · see citing works
Adolescent nicotine induces persisting changes in development of neural connectivity.
Smith, R. F., McDonald, C. G., Bergstrom, H. C., Ehlinger, D. G., & Brielmaier, J. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.019 · Cited by 120 · see citing works
Baker, T. B., Weiss, R. B., Bolt, D. M., von Niederhausern, A. C., Fiore, M. C., Dunn, D. M., Piper, M. E., Matsunami, N., Smith, S. S., Coon, H. H., et al. (2009) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntp064 · Cited by 120 · see citing works
Molecules and circuits involved in nicotine addiction: The many faces of smoking
Picciotto, M. R., & Mineur, Y. S. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.028 · Cited by 117 · see citing works
Low dose nicotine treatment during early adolescence increases subsequent cocaine reward
McQuown, S. C., Belluzzi, J. D., & Leslie, F. M. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.10.012 · Cited by 117 · see citing works
Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory
Carroll, M. E., Anker, J. J., & Perry, J. L. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2008.11.011 · Cited by 116 · see citing works
Shram, M. J., Funk, D. R., Li, Z., & Lê, A. D. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301454 · Cited by 109 · see citing works
Abreu‐Villaça, Y., Seidler, F. J., Tate, C. A., Cousins, M. M., & Slotkin, T. A. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300401 · Cited by 107 · see citing works
Assessment of adolescent neurotoxicity: Rationale and methodological considerations
SPEAR, L. P. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.11.006 · Cited by 104 · see citing works
Adolescent and adult female rats differ in sensitivity to nicotine's activity effects
ELLIOTT, B., Faraday, M. M., PHILLIPS, J., & Grunberg, N. E. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.019 · Cited by 102 · see citing works
Foll, B. L., & Goldberg, S. R. (2005) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2005.04.005 · Cited by 98 · see citing works
Adolescent neurodevelopment and substance use: receptor expression and behavioral consequences
Thorpe, H. H. A., Hamidullah, S., Jenkins, B. W., & Khokhar, J. Y. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107431 · Cited by 97 · see citing works
Neurobiological Processes in Adolescent Addictive Disorders
Schepis, T. S., Adinoff, B. H., & Rao, U. (2008) · American Journal on Addictions · doi:10.1080/10550490701756146 · Cited by 95 · see citing works
Klein, L. C., Stine, M. M., Vandenbergh, D. J., Whetzel, C. A., & Kamens, H. M. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.01.005 · Cited by 95 · see citing works
Influence of Neuronal Nicotinic Receptors over Nicotine Addiction and Withdrawal
De Biasi, M., & Salas, R. (2008) · Experimental Biology and Medicine · doi:10.3181/0712-mr-355 · Cited by 95 · see citing works
Schochet, T. L., Kelley, A. E., & Landry, C. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.057 · Cited by 93 · see citing works
Smoking impacts on prefrontal attentional network function in young adult brains
Musso, F., Bettermann, F., Vucurevic, G., Stoeter, P., Konrad, A., & Winterer, G. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0499-8 · Cited by 93 · see citing works
Reichelt, A. C. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00189 · Cited by 93 · see citing works
Brielmaier, J. M., McDonald, C. G., & Smith, R. F. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.09.023 · Cited by 90 · see citing works
Secondhand smoke and nicotine exposure: A brief review
Okoli, C. T. C., Kelly, T. H., & Hahn, E. J. (2007) · Addictive Behaviors · doi:10.1016/j.addbeh.2006.12.024 · Cited by 88 · see citing works
Slotkin, T. A., Tate, C. A., Cousins, M. M., & Seidler, F. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300988 · Cited by 88 · see citing works
Role of central amygdala neuronal ensembles in incubation of nicotine craving
Funk, D., Coen, K., Tamadon, S., Hope, B. T., Shaham, Y., & Lê, A. D. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1505-16.2016 · Cited by 87 · see citing works
Adriani, W., Deroche-Gamonet, V., Le Moal, M., Laviola, G., & Piazza, P. V. V. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0125-1 · Cited by 86 · see citing works
Self-citationBEHAVIORAL MECHANISMS UNDERLYING NICOTINE REINFORCEMENT
Rupprecht, L. E., Smith, T. T., Schassburger, R. L., Buffalari, D., Sved, A., & Donny, E. C. (2015) · Current topics in behavioral neurosciences · doi:10.1007/978-3-319-13482-6_2 · Cited by 78 · see citing works
O’Dell, L. E., Torres, O. V., Natividad, L. A., & Tejeda, H. A. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.11.003 · Cited by 84 · see citing works
Smoking kills (alcoholics)! shouldn't we do something about it?
Littleton, J., Barron, S., Prendergast, M., & Nixon, S. J. (2007) · Alcohol and Alcoholism · doi:10.1093/alcalc/agm019 · Cited by 82 · see citing works
A psychobiological framework of the substrates that mediate nicotine use during adolescence
O'Dell, L. E. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.039 · Cited by 81 · see citing works
Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning
Portugal, G. S., Wilkinson, D. S., Turner, J. R., Blendy, J. A., & Gould, T. J. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.04.003 · Cited by 79 · see citing works
Diergaarde, L., de Vries, W., Raasø, H. S., Schoffelmeer, A. N. M., & Vries, T. J. D. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.003 · Cited by 80 · see citing works
Nicotine alters limbic function in adolescent rat by a 5-HT1A receptor mechanism
Dao, J. M., McQuown, S. C., Loughlin, S. E., Belluzzi, J. D., & Leslie, F. M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.8 · Cited by 79 · see citing works
Doyon, W. M., Thomas, A. M., Ostroumov, A., Dong, Y., & Dani, J. A. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.007 · Cited by 77 · see citing works
Counotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Self-citationAn animal model of social instability stress in adolescence and risk for drugs of abuse
McCormick, C. M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.01.014 · Cited by 76 · see citing works
Increased Genetic Vulnerability to Smoking at CHRNA5 in Early-Onset Smokers
Hartz, S. M., Short, S. E., Saccone, N. L., Culverhouse, R., Chen, L., Schwantes-An, T.-H., Coon, H., Han, Y., Stephens, S. H., Sun, J., et al. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2012.124 · Cited by 75 · see citing works
Holliday, E. D., & Gould, T. J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.003 · Cited by 75 · see citing works
Hogle, J. M., Kaye, J. T., & Curtin, J. J. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.003 · Cited by 72 · see citing works
SMITH, L., MCDONALD, C., BERGSTROM, H., BRIELMAIER, J., EPPOLITO, A., WHEELER, T., FALCO, A., & SMITH, R. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.014 · Cited by 70 · see citing works
Cholinergic modulation of dopamine pathways through nicotinic acetylcholine receptors
de Kloet, S. F., Mansvelder, H. D., & De Vries, T. J. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.07.014 · Cited by 69 · see citing works
Cohen, A., & George, O. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00041 · Cited by 67 · see citing works
Periadolescent nicotine exposure causes heterologous sensitization to cocaine reinforcement
McMillen, B. A., Davis, B. J., Williams, H. L., & Soderstrom, K. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.01.002 · Cited by 66 · see citing works
Goriounova, N. A., & Mansvelder, H. D. (2012) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2012.00003 · Cited by 65 · see citing works
Obesity and food addiction: Similarities to drug addiction
Campana, B., Brasiel, P. G. D. A., de Aguiar, A. S., & Dutra, S. C. P. L. (2019) · Obesity Medicine · doi:10.1016/j.obmed.2019.100136 · Cited by 63 · see citing works
Neurochemical alterations produced by daily nicotine exposure in periadolescent vs. adult male rats
Collins, S. L., Wade, D., Ledon, J., & Izenwasser, S. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.08.039 · Cited by 62 · see citing works
Individual differences in oral nicotine intake in rats
Nesil, T., Kanıt, L., Collins, A. C., & Pöğün, Ş. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.03.027 · Cited by 62 · see citing works
Age dependent nicotinic influences over dopamine neuron synaptic plasticity
Placzek, A. N., Zhang, T. A., & Dani, J. A. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.05.014 · Cited by 61 · see citing works
Vorhees, C. V., Reed, T. M., Morford, L. L., Fukumura, M., Wood, S. L., Brown, C. A., Skelton, M. R., McCrea, A. E., Rock, S. L., & Williams, M. T. (2004) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2004.09.005 · Cited by 61 · see citing works
Bergstrom, H. C., McDonald, C. G., French, H. T., & Smith, R. F. (2008) · Synapse · doi:10.1002/syn.20467 · Cited by 60 · see citing works
Abou-Donia, M. B., Khan, W. A., Dechkovskaia, A. M., Goldstein, L. B., Bullman, S. L., & Abdel-Rahman, A. A. (2006) · Archives of Toxicology · doi:10.1007/s00204-006-0077-1 · Cited by 60 · see citing works
Enhanced nicotine reward in adulthood after exposure to nicotine during early adolescence in mice
Kota, D., Robinson, S. E., & Imad Damaj, M. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.06.099 · Cited by 59 · see citing works
Conditioned Place Preference Induced by Licit Drugs: Establishment, Extinction, and Reinstatement
Liu, Y., Foll, B. L., Liu, Y., Wang, X. L., & Lü, L. (2008) · The Scientific World JOURNAL · doi:10.1100/tsw.2008.154 · Cited by 57 · see citing works
Mahajan, S. D., Homish, G. G., & Quisenberry, A. J. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.664748 · Cited by 64 · see citing works
Nicotinic acetylcholine receptors: upregulation, age‐related effects and associations with drug use
Melroy-Greif, W. E., Stitzel, J. A., & Ehringer, M. A. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12251 · Cited by 54 · see citing works
Manhães, A. C., Guthierrez, M. C. S., Filgueiras, C. C., & Abreu‐Villaça, Y. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.05.018 · Cited by 54 · see citing works
Adolescence, schizophrenia and drug abuse: a window of vulnerability
Nimwegen, L., Haan, L., Beveren, N., Brink, W., & Linszen, D. (2005) · Acta Psychiatrica Scandinavica Supplementum · doi:10.1111/j.1600-0447.2005.00543.x · Cited by 45 · see citing works
Abdel-Rahman, A. A., Dechkovskaia, A. M., Sutton, J. M., Chen, W., Guan, X., Khan, W. A., & Abou-Donia, M. B. (2005) · Toxicology · doi:10.1016/j.tox.2004.12.037 · Cited by 53 · see citing works
- Authors
- Adriani, W., Spijker, S., Deroche-Gamonet, V., Laviola, G., Le Moal, M., Smit, A. B., & Piazza, P. V.
- Affiliations
- Inserm (FR)
- Vrije Universiteit Amsterdam (NL)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-06-01
- Volume
- 23
- Issue
- 11
- Pages
- 4712-4716
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6740776
- OpenAlex
- W2159655610
- Cited by
- 257
- References
- 41
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 1 · 2023: 4 · 2022: 9 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 6 · 2017: 6 · 2016: 11 · 2015: 16 · 2014: 15 · 2013: 18 · 2012: 14
- FWCI
- 10.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- nicotine, adolescence, periadolescence, nicotine dependence, nicotine self-administration, acetylcholine receptor subunits, ligand-gated receptors, developmental vulnerability
- MeSH terms
- Animals, Behavior, Animal, Critical Period, Psychological, Injections, Intravenous, Male, Mesencephalon, Motor Activity, Nervous System, Nicotine, Receptors, Nicotinic, Reinforcement, Psychology, RNA, Messenger, Self Administration, Sexual Maturation, Substantia Nigra, Time, Tobacco Use Disorder, Gene Expression, Rats, Sprague-Dawley, Ventral Tegmental Area, Protein Subunits, Rats
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