Age- and sex-dependent nicotine pretreatment effects on the enhancement of methamphetamine self-administration in Sprague-Dawley rats
Open accessAbstract
INTRODUCTION: Initiation of tobacco products typically occurs in adolescence. Adolescence is a critical period in development where the maturation of brain neurocircuitry is vulnerable to nicotine. Nicotine-containing products and psychostimulants, such as methamphetamine (METH), are often coabused. Rodent studies have shown that nicotine exposure in early adolescence increases subsequent drug intake and reward. Given the exponential increase in e-cigarette use among adolescents, there is a pressing need to understand whether adolescent nicotine exposure impacts concurrent increased METH use. The objective of this study is to evaluate age, sex, and longitudinal effects of nicotine pretreatment on METH reinforcement. AIMS AND METHODS: Male and female Sprague-Dawley rats were pretreated with a subchronic, low-dose nicotine (2×, 30 µg/kg/0.1 mL, intravenous) or saline during early adolescence (postnatal days [PN] 28-31) or adulthood (PN 86-89). Following nicotine pretreatment, on PN 32 or PN 90, animals underwent operant intravenous self-administration for METH (20 µg/kg/inf) over a 2-hour period for five consecutive days. RESULTS: Early adolescent nicotine exposure enhances intravenous METH self-administration in male, but not female adolescents. Male adult rats self-administer METH over the 5-day testing period, independent of nicotine exposure. In contrast, nicotine exposure increases METH self-administration in female adults during the later sessions of the 5-day testing period. CONCLUSIONS: Taken together, our data highlight age- and sex-dependent effects of low dose, subchronic nicotine pretreatment on subsequent intravenous METH self-administration. IMPLICATIONS: A majority of polysubstance users begin smoking before the age of 18. Mounting evidence highlights adolescent susceptibility to nicotine exposure on brain and behavior. With the escalation in nicotine-containing products and stimulant use among adolescents, it is important to identify the consequences from adolescent nicotine use, including polysubstance use. Our study provides evidence that adolescent nicotine exposure enhances subsequent METH use, with important sex- and age-dependent effects.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Brief pretreatment of early adolescent rats (P28-31) with a low dose of nicotine that models smoking initiation significantly increases self-administration of cocaine, ethanol, fentanyl, and methamphetamine when compared to adults.
“Brief pretreatment of early adolescent rats (postnatal days (P) 28–31) with a low dose of nicotine that models smoking initiation significantly increases self-administration of cocaine, ethanol, fentanyl, and methamphetamine when compared to adults [146–151].”
From Nicotine on the developing brain. (2023) · cites this paper as [151]
The Introduction describes the P28–31 nicotine pretreatment as a model of smoking initiation, and the Discussion reports prior age-dependent findings for cocaine, ethanol, fentanyl, and methamphetamine. But the paper’s own methamphetamine results show increased intake after nicotine pretreatment in adolescent males, not adolescent females; adult females also showed an increase. The Results report greater methamphetamine intake in adults overall, so the claim that adolescent self-administration was significantly higher than adults’ is not supported. Page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
Stages in adolescent involvement in drug use
Kandel, D. B. (1975) · Science · doi:10.1126/science.1188374 · Cited by 1,099 · 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
Methamphetamine use behaviors and gender differences
Brecht, M., O’Brien, A., von Mayrhauser, C., & Anglin, M. D. (2003) · Addictive Behaviors · doi:10.1016/s0306-4603(03)00082-0 · Cited by 444 · see citing works
Sex 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
Acetaldehyde 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
Amphetamine and methamphetamine differentially affect dopamine transporters in vitro and in vivo.
Goodwin, J. S., Larson, G. A., Swant, J., Sen, N., Javitch, J. A., Zahniser, N. R., De Felice, L. J., & Khoshbouei, H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m805298200 · Cited by 203 · 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
Nicotine 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
Self-citationStress is a principal factor that promotes tobacco use in females
Torres, O. V., & O'Dell, L. E. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.04.005 · Cited by 164 · see citing works
Sex differences in methamphetamine seeking in rats: Impact of oxytocin
Cox, B. M., Young, A. B., See, R. E., & Reichel, C. M. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.005 · Cited by 159 · see citing works
Hypothalamic–Pituitary–Adrenocortical responses to psychological stress and risk for smoking relapse
Al’Absi, M. (2006) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.10.010 · Cited by 156 · see citing works
Collins, S. L., & Izenwasser, S. (2003) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.09.024 · Cited by 154 · see citing works
Reichel, C. M., Chan, C. H., Ghee, S. M., & See, R. E. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2727-8 · Cited by 153 · see citing works
Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction
Andersen, S. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00069-5 · Cited by 152 · 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
Ethanol consumption inhibits TFH cell responses and the development of autoimmune arthritis
Azizov, V., Dietel, K., Steffen, F., Dürholz, K., Meidenbauer, J., Lucas, S., Frech, M., Omata, Y., Tajik, N., Knipfer, L., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15855-z · Cited by 133 · 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
Nicotine Receptor Inactivation Decreases Sensitivity to Cocaine
Zachariou, V. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00224-4 · Cited by 115 · see citing works
Torres, O. V., Natividad, L. A., Tejeda, H. A., Van Weelden, S. A., & O’Dell, L. E. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1607-3 · Cited by 110 · see citing works
Risk factors for methamphetamine use in youth: a systematic review
Russell, K. F., Dryden, D. M., Liang, Y., Friesen, C., O'Gorman, K., Durec, T., Wild, T. C., & Klassen, T. P. (2008) · BMC Pediatrics · doi:10.1186/1471-2431-8-48 · Cited by 106 · see citing works
Sex‐dependent effects of nicotine on the developing brain
Cross, S. J., Linker, K. E., & Leslie, F. M. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23878 · Cited by 104 · see citing works
Mechanisms and genetic factors underlying co-use of nicotine and alcohol or other drugs of abuse
Cross, S. J., Lotfipour, S., & Leslie, F. M. (2016) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2016.1209512 · Cited by 101 · see citing works
Self-citationInteractions between nicotine and drugs of abuse: a review of preclinical findings
Kohut, S. J. (2016) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2016.1209513 · Cited by 89 · see citing works
Kučerová, J., Amchová, P., Babinská, Z., Dušek, L., Micale, V., & Šulcová, A. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00091 · Cited by 87 · see citing works
Substance use pathways to methamphetamine use among treated users
Brecht, M., Greenwell, L., & Anglin, M. D. (2006) · Addictive Behaviors · doi:10.1016/j.addbeh.2006.03.017 · Cited by 83 · 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
Microglial activation increases cocaine self-administration following adolescent nicotine exposure
Linker, K. E., Gad, M., Tawadrous, P., Cano, M., Green, K. N., Wood, M. A., & Leslie, F. M. (2020) · Nature Communications · doi:10.1038/s41467-019-14173-3 · Cited by 77 · see citing works
Levin, E. D., Mead, T., Rezvani, A. H., Rose, J. E., Gallivan, C., & Gross, R. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00382-6 · Cited by 75 · see citing works
Age- and sex-dependent amphetamine self-administration in rats
Shahbazi, M., Moffett, A. M., Williams, B. F., & Frantz, K. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0933-6 · Cited by 74 · see citing works
Influence of gender and sex hormones on nicotine acute pharmacological effects in mice.
Damaj, M. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29673-7 · Cited by 72 · see citing works
Collins, S. L., Montano, R. E., & Izenwasser, S. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.08.004 · Cited by 71 · 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
Adolescent Maturation of Cocaine-Sensitive Neural Mechanisms
Cao, J., Lotfipour, S., Loughlin, S. E., & Leslie, F. M. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301349 · Cited by 55 · see citing works
Self-citationElectronic cigarettes (e‐cigarettes)
(2014) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21228 · Cited by 54 · see citing works
Escalation of methamphetamine self-administration in adolescent and adult rats
Anker, J. J., Baron, T. R., Zlebnik, N. E., & Carroll, M. E. (2012) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.01.004 · Cited by 52 · see citing works
Locomotor and stress responses to nicotine differ in adolescent and adult rats
Cao, J., Belluzzi, J. D., Loughlin, S. E., Dao, J. M., Chen, Y., & Leslie, F. M. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.04.010 · Cited by 47 · see citing works
McQuown, S. C., Dao, J. M., Belluzzi, J. D., & Leslie, F. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1642-0 · Cited by 39 · see citing works
Early adolescent nicotine exposure affects later-life cocaine reward in mice
Alajaji, M., Lazenka, M. F., Kota, D., Wise, L. E., Younis, R. M., Carroll, F. I., Levine, A., Selley, D. E., Sim-Selley, L. J., & Damaj, M. I. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.01.032 · Cited by 39 · see citing works
Opioids and methamphetamine: a tale of two crises
Lancet, T. (2018) · The Lancet · doi:10.1016/s0140-6736(18)30319-2 · Cited by 39 · see citing works
dos Santos, G. C., Marin, M. T., Cruz, F. C., DeLucia, R., & Planeta, C. S. (2009) · Addiction Biology · doi:10.1111/j.1369-1600.2009.00153.x · Cited by 35 · see citing works
Nicotine elicits methamphetamine-seeking in rats previously administered nicotine
Neugebauer, N. M., Harrod, S. B., & Bardo, M. T. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.07.018 · Cited by 24 · see citing works
Pipkin, J. A., Kaplan, G. J., Plant, C. P., Eaton, S. E., Gil, S. M., Zavala, A. R., & Crawford, C. A. (2014) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2014.06.029 · Cited by 21 · see citing works
Cardenas, A., Martinez, M., Saenz Mejia, A., & Lotfipour, S. (2021) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000593 · Cited by 21 · see citing works
Self-citationHarmony, Z. R., Alderson, E. M., Garcia-Carachure, I., Bituin, L. D., & Crawford, C. A. (2020) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2020.107927 · Cited by 12 · see citing works
Chronic Nicotine Exposure Attenuates Methamphetamine-Induced Dopaminergic Deficits
Vieira‐Brock, P. L., McFadden, L. M., Nielsen, S. M., Ellis, J. D., Walters, E. T., Stout, K. A., McIntosh, J. M., Wilkins, D. G., Hanson, G. R., & Fleckenstein, A. E. (2015) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.221945 · Cited by 10 · see citing works
Nicotine- and cocaine-triggered methamphetamine reinstatement in female and male Sprague-Dawley rats
Pittenger, S. T., Chou, S., Barrett, S. T., Catalano, I., Lydiatt, M. F., & Bevins, R. A. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.07.003 · Cited by 7 · see citing works
Effects of nicotine conditioning history on alcohol and methamphetamine self-administration in rats
Randall, P. A., Fortino, B., Huynh, Y. W., Thompson, B. M., Larsen, C. E., Callen, M. P., Barrett, S. T., Murray, J. E., Bevins, R. A., & Besheer, J. (2019) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2019.01.005 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Yuan M, Cross SJ, Loughlin SE, Leslie FM. Nicotine and the adolescent brain. J Physiol. 2015;593(16):3397-3412.
Cited by
Sorted by citations
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
“ANE also increases the likelihood of continued nicotine use [178], cannabis use [179], and alcohol use in humans [180], as well as other drugs in rodents such as methamphetamine [181], alcohol [182], cocaine [183, 184], and fentanyl [183].”
BackgroundNicotine on the developing brain.
Castro, E. M., Lotfipour, S., & Leslie, F. M. (2023) · Pharmacological research · doi:10.1016/j.phrs.2023.106716 · Cited by 140 · see citing works
Self-citation
- Authors
- Cardenas, A., & Lotfipour, S.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- Lotfipour, Shahrdad
- Venue
- Nicotine & Tobacco Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-10-20
- Volume
- 24
- Issue
- 8
- Pages
- 1186-1192
- ISSN
- 1462-2203 (ISSN-L)
- 1469-994X
- PMC
- PMC9653006
- OpenAlex
- W3206611930
- Cited by
- 16
- References
- 49
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 3 · 2023: 6 · 2022: 3
- FWCI
- 1.89
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Nicotine & Tobacco Research (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Tobacco-Related Disease Research Program Project (T31IP1427, 22RT-0103)
- UCI Institute for Clinical and Translational Sciences
- Pilot Studies Program
- UCI Department of Emergency Medicine Prestige Funds
- Brain and Behavior Research (21517)
- UCI School of Medicine Start Up funds
- Ford Foundation Fellowship and the UC President’s Pre-Professoriate Fellowship
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- nicotine, methamphetamine, adolescent nicotine exposure, self-administration, sex differences, age-dependent effects, polydrug use, electronic cigarettes, adolescent brain development
- MeSH terms
- Central Nervous System Stimulants, Animals, Conditioning, Operant, Male, Methamphetamine, Nicotine, Self Administration, Rats, Sprague-Dawley, Rats, Electronic Nicotine Delivery Systems
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
