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Lifetime caffeine and adolescent nicotine exposure in mice: effects on anxiety-like behavior and reward

Published online by Cambridge University Press:  03 April 2023

Ana Carolina Dutra-Tavares*
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
Anderson Ribeiro-Carvalho
Affiliation:
Departamento de Ciências, Faculdade de Formação de Professores da Universidade do Estado do Rio de Janeiro, São Gonçalo, RJ, 24435-005, Brasil
Fernanda Nunes
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
Ulisses Cesar Araújo
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
Vitor Bruno
Affiliation:
Departamento de Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Av. Prof. Lineu Prestes, 580, Bl. 13B, 05508-000, São Paulo, SP, Brasil
Tania Marcourakis
Affiliation:
Departamento de Análises Clínicas e Toxicológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Av. Prof. Lineu Prestes, 580, Bl. 13B, 05508-000, São Paulo, SP, Brasil
Claudio C. Filgueiras
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
Alex C. Manhães
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
Yael Abreu-Villaça
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, Brasil
*
Address for correspondence: Ana Carolina Dutra-Tavares, Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro (UERJ), Av. Prof. Manuel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brasil. Email: dutratavaresana@gmail.com

Abstract

Caffeine consumption occurs throughout life, while nicotine use typically begins during adolescence, the period when caffeine-nicotine epidemiological association begins in earnest. Despite that, few studies in animal models parallel the pattern of coexposure that occurs in humans. Therefore, the neurobehavioral consequences of the association between these drugs remain unclear. Here, we exposed Swiss mice to lifetime caffeine. Caffeine solutions of 0.1 g/L (CAF0.1), 0.3 g/L (CAF0.3), or water (CTRL) were used as the sole liquid source, being offered to progenitors until weaning and, after that, directly to the offspring until the last day of adolescent behavioral evaluation. The open field test was used to evaluate acute effects of nicotine, of lifetime caffeine and of their interaction on locomotion and anxiety-like behavior, while the conditioned place preference test was used to assess the impact of caffeine on nicotine (0.5 mg/Kg, i.p.) reward. Frontal cerebral cortex dopamine content, dopamine turnover, and norepinephrine levels, as well as hippocampal serotonin 1A receptor expression were assessed. CAF0.3 mice exhibited an increase in anxiety-like behavior when compared to CAF0.1 and CTRL ones, but nicotine coexposure mitigated the anxiogenic-like caffeine-induced effect. Distinctively, caffeine had no effect on locomotion and failed to interfere with both nicotine-induced hyperactivity and place preference. There were no significant effects on dopaminergic and serotonergic markers. In conclusion, although caffeine did not affect nicotine reward, considering the strong association between anxiety disorders and tobacco consumption, caffeine-induced anxiety-like behavior advises limiting its consumption during development, including adolescence, as caffeine could be a risk factor to nicotine use.

Type
Original Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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Footnotes

Ana Carolina Dutra-Tavares and Anderson Ribeiro-Carvalho contributed equally to this work.

References

Frary, CD, Johnson, RK, Wang, MQ. Food sources and intakes of caffeine in the diets of persons in the United States. J Am Diet Assoc. 2005; 105(1), 110113.CrossRefGoogle ScholarPubMed
Calvaresi, V, Escuder, D, Minutillo, A, et al. Transfer of nicotine, cotinine and caffeine into breast milk in a smoker mother consuming caffeinated drinks. J Anal Toxicol. 2016; 40(6), 473477.CrossRefGoogle Scholar
Ruiz, LD, Scherr, RE. Risk of energy drink consumption to adolescent health. Am J Lifestyle Med. 2019; 13(1), 2225.CrossRefGoogle ScholarPubMed
Ahluwalia, N, Herrick, K. Caffeine intake from food and beverage sources and trends among children and adolescents in the United States: review of national quantitative studies from 1999 to 2011. Adv Nutr. 2015; 6(1), 102111.CrossRefGoogle ScholarPubMed
Glatter, KA, Myers, R, Chiamvimonvat, N. Recommendations regarding dietary intake and caffeine and alcohol consumption in patients with cardiac arrhythmias: what do you tell your patients to do or not to do? Curr Treat Options Cardiovasc Med. 2012; 14(5), 529535.CrossRefGoogle ScholarPubMed
Pennington, N, Johnson, M, Delaney, E, Blankenship, MB. Energy drinks: a new health hazard for adolescents. J Sch Nurs. 2010; 26(5), 352359.CrossRefGoogle ScholarPubMed
Temple, JL. Review: trends, safety, and recommendations for caffeine use in children and adolescents. J Am Acad Child Adolesc Psychiatry. 2019; 58(1), 3645.CrossRefGoogle ScholarPubMed
Li, Y, Zhang, W, Shi, R, et al. Prenatal caffeine damaged learning and memory in rat offspring mediated by ARs/PKA/CREB/BDNF pathway. Physiol Res. 2018; 67(6), 975983.CrossRefGoogle ScholarPubMed
Laureano-Melo, R, da Silveira, ALB, de Azevedo Cruz Seara, F, et al. Behavioral profile assessment in offspring of Swiss mice treated during pregnancy and lactation with caffeine. Metab Brain Dis. 2016; 31(5), 10711080.CrossRefGoogle ScholarPubMed
Silva, CG, Métin, C, Fazeli, W, et al. Adenosine receptor antagonists including caffeine alter fetal brain development in mice. Sci Transl Med. 2013; 5(197).CrossRefGoogle ScholarPubMed
Anderson, NL, Hughes, RN. Increased emotional reactivity in rats following exposure to caffeine during adolescence. Neurotoxicol Teratol. 2008; 30(3), 195201.CrossRefGoogle ScholarPubMed
Ardais, AP, Borges, MF, Rocha, AS, Sallaberry, C, Cunha, RA, Porciúncula, LO. Caffeine triggers behavioral and neurochemical alterations in adolescent rats. Neuroscience. 2014; 270, 2739.CrossRefGoogle ScholarPubMed
Hinton, DJ, Andres-Beck, LG, Nett, KE, et al. Chronic caffeine exposure in adolescence promotes diurnal, biphasic mood-cycling and enhanced motivation for reward in adult mice. Behav Brain Res. 2019; 370, 111943.CrossRefGoogle ScholarPubMed
da Silva Gonçalves, B, Leal-Rocha, PH, Manhães, AC, Filgueiras, CC, Abreu-Villaça, Y, Ribeiro-Carvalho, A. Lifelong exposure to caffeine increases anxiety-like behavior in adult mice exposed to tobacco smoke during adolescence. Neurosci Lett. 2019; 696, 146150.CrossRefGoogle ScholarPubMed
Seifert, SM, Schaechter, JL, Hershorin, ER, Lipshultz, SE. Health effects of energy drinks on children, adolescents, and young adults. Pediatrics. 2011; 127(3), 511528.CrossRefGoogle ScholarPubMed
Richards, G, Smith, A. Caffeine consumption and self-assessed stress, anxiety, and depression in secondary school children. J Psychopharmacol. 2015; 29(12), 12361247.CrossRefGoogle ScholarPubMed
Marmorstein, NR. Energy drink and coffee consumption and psychopathology symptoms among early adolescents: cross-sectional and longitudinal associations. J Caffeine Res. 2016; 6(2), 6472.CrossRefGoogle ScholarPubMed
Leal, WE, Jackson, DB. Energy drinks and escalation in drug use severity: an emergent hazard to adolescent health. Prev Med (Baltim). 2018; 111, 391396.CrossRefGoogle ScholarPubMed
Cotter, BV, Jackson, DAE, Merchant, RC, et al. Energy drink and other substance use among adolescent and young adult emergency department patients. Pediatr Emerg Care. 2013; 29(10), 10911097.CrossRefGoogle ScholarPubMed
Terry-McElrath, YM, O’Malley, PM, Johnston, LD. Energy drinks, soft drinks, and substance use among united states secondary school students. J Addict Med. 2014; 8(1), 613.CrossRefGoogle ScholarPubMed
Swanson, JA, Lee, JW, Hopp, JW. Caffeine and nicotine: a review of their joint use and possible interactive effects in tobacco withdrawal. Addict Behav. 1994; 19(3), 229256.CrossRefGoogle ScholarPubMed
Brody, AL, Hubert, R, Mamoun, MS, et al. Smokers : effect of heavy caffeine or marijuana use, 2017; 233(17), 32493257.CrossRefGoogle Scholar
Liu, X, Jernigan, C. Effects of caffeine on persistence and reinstatement of nicotine-seeking behavior in rats: interaction with nicotine-associated cues. Psychopharmacology (Berl). 2012; 220(3), 541550.CrossRefGoogle ScholarPubMed
Celik, E, Uzbay, IT, Karakas, S. Caffeine and amphetamine produce cross-sensitization to nicotine-induced locomotor activity in mice. Prog Neuro-Psychopharmacol Biol Psychiatry. 2006; 30(1), 5055.CrossRefGoogle ScholarPubMed
Gasior, M, Jaszyna, M, Peters, J, Goldberg, SR. Changes in the ambulatory activity and discriminative stimulus effects of psychostimulant drugs in rats chronically exposed to caffeine: effect of caffeine dose. J Pharmacol Exp Ther. 2000; 295(3), 11011111.Google ScholarPubMed
Justinova, Z, Ferré, S, Barnes, C, et al. Effects of chronic caffeine exposure on adenosinergic modulation of the discriminative-stimulus effects of nicotine, methamphetamine and cocaine in rats. Psychopharmacology (Berl). 2010; 203(2), 355367.CrossRefGoogle Scholar
Kayir, H, Uzbay, IT. Nicotine antagonizes caffeine- but not pentylenetetrazole-induced anxiogenic effect in mice. Psychopharmacology (Berl). 2006; 184(3-4), 464469.CrossRefGoogle Scholar
Lawrence, D, Considine, J, Mitrou, F, Zubrick, SR. Anxiety disorders and cigarette smoking: results from the Australian Survey of Mental Health and Wellbeing. Aust N Z J Psychiatry. 2010; 44(6), 520527.Google ScholarPubMed
Tobias, AM, Templeton, R, Collings, S, Tobias, M, Templeton, R, Collings, S. How much do mental disorders contribute to New Zealand’s tobacco epidemic? Tob Control. 2014; 17(5), 347350.CrossRefGoogle Scholar
Cullen, KA, Gentzke, AS, Sawdey, MD, et al. e-Cigarette use among youth in the United States, 2019. JAMA - J Am Med Assoc. 2019; 322(21), 20952103.CrossRefGoogle Scholar
Cullen, KA, Liu, ST, Bernat, JK, et al. Flavored tobacco product use among middle and high school students — United States, 2014-2018. MMWR Morb Mortal Wkly Rep. 2019; 68(39), 839844.CrossRefGoogle ScholarPubMed
Miech, R, Leventhal, A, Johnston, L, O’Malley, PM, Patrick, ME, Barrington-Trimis, J. Trends in use and perceptions of nicotine vaping among US youth from 2017 to 2020. JAMA Pediatr. 2021; 175(2), 185190.CrossRefGoogle ScholarPubMed
Govind, AP, Vezina, P. Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Clin Lymphoma. 2010; 9(1), 1922.Google Scholar
Gotti, C, Guiducci, S, Tedesco, V, et al. Nicotinic acetylcholine receptors in the mesolimbic pathway: primary role of ventral tegmental area α6β2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement. J Neurosci. 2010; 30(15), 53115325.CrossRefGoogle ScholarPubMed
Jobson, CLM, Renard, J, Szkudlarek, H, et al. Adolescent nicotine exposure induces dysregulation of mesocorticolimbic activity states and depressive and anxiety-like prefrontal cortical molecular phenotypes persisting into adulthood. Cereb Cortex. 2019; 29(7), 31403153.CrossRefGoogle ScholarPubMed
McGranahan, TM, Patzlaff, NE, Grady, SR, Heinemann, SF, Booker, TK. α4β2 Nicotinic acetylcholine receptors on dopaminergic neurons mediate nicotine reward and anxiety relief. J Neurosci. 2011; 31(30), 1089110902.CrossRefGoogle ScholarPubMed
Pandolfo, P, Machado, NJ, Kofalvi, A, Takahashia, RN, Cunhab, RA. Caffeine regulates frontocorticostriatal dopamine transporter density and improves attention and cognitive deficits in an animal model of attention deficit hyperactivity disorder. Eur Neuropsychopharmacol. 2013; 23(4), 317328.CrossRefGoogle Scholar
Ceceli, AO, Bradberry, CW, Goldstein, RZ. The neurobiology of drug addiction: cross-species insights into the dysfunction and recovery of the prefrontal cortex. Neuropsychopharmacology. 2022; 47(1), 276291.CrossRefGoogle ScholarPubMed
Gottschalk, MG, Domschke, K. Genetics of generalized anxiety disorder and related traits. Dialogues Clin Neurosci. 2017; 19(2), 159168.CrossRefGoogle ScholarPubMed
Hale, M, Shekhar, A, Lowry, C. Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell Mol Neurobiol. 2012; 32(5), 695708.CrossRefGoogle ScholarPubMed
Asan, E, Steinke, M, Lesch, KP. Serotonergic innervation of the amygdala: targets, receptors, and implications for stress and anxiety. Histochem Cell Biol. 2013; 139(6), 785813.CrossRefGoogle ScholarPubMed
Mah, L, Szabuniewicz, C, Fiocco, AJ. Can anxiety damage the brain? Curr Opin Psychiatry. 2016; 29(1), 5663.CrossRefGoogle ScholarPubMed
Okada, M, Kawata, Y, Murakami, T, et al. Differential effects of adenosine receptor subtypes on release and reuptake of hippocampal serotonin. Eur J Neurosci. 1999; 11(1), 19.CrossRefGoogle ScholarPubMed
Gross, C, Zhuang, X, Stark, K, et al. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature. 2002; 416(6879), 396400.CrossRefGoogle ScholarPubMed
Gordon, JA, Hen, R. The serotonergic system and anxiety. NeuroMolecular Med. 2004; 5(1), 2740.CrossRefGoogle ScholarPubMed
Fredholm, BB, Bättig, K, Holmén, J, Nehlig, A, Zvartau, EE. Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol Rev. 1999; 51(1), 83133.Google ScholarPubMed
Seibenhener, ML, Wooten, MC. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp. 2015; 96, 16.Google Scholar
Kraeuter, AK, Guest, P, Sarnyai, Z. The open field test for measuring locomotor activity and anxiety-like behavior. Pre-Clin Model Tech Protoc Methods Mol Biol. 1916, 99103.Google Scholar
Prut, L, Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol. 2003; 463(1-3), 333.CrossRefGoogle Scholar
Brielmaier, JM, McDonald, CG, Smith, RF. Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicol Teratol. 2007; 29(1), 7480.CrossRefGoogle ScholarPubMed
Pistillo, F, Clementi, F, Zoli, M, Gotti, C. Nicotinic, glutamatergic and dopaminergic synaptic transmission and plasticity in the mesocorticolimbic system: focus on nicotine effects. Prog Neurobiol. 2015; 124, 127.CrossRefGoogle ScholarPubMed
Panagis, G, Nisell, M, Nomikos, GG, Chergui, K, Svensson, TH. Nicotine injections into the ventral tegmental area increase locomotion and Fos-like immunoreactivity in the nucleus accumbens of the rat. Brain Res. 1996; 730(1-2), 133142.CrossRefGoogle ScholarPubMed
Ferrari, R, Le Novère, N, Picciotto, MR, Changeux, JP, Zoli, M. Acute and long-term changes in the mesolimbic dopamine pathway after systemic or local single nicotine injections. Eur J Neurosci. 2002; 15(11), 18101818.CrossRefGoogle ScholarPubMed
Morissette, SB, Tull, MT, Gulliver, SB, Kamholz, BW, Zimering, RT. Anxiety, anxiety disorders, tobacco use, and nicotine : a critical review of interrelationships. Psychol Bull. 2007; 133(2), 245272.CrossRefGoogle ScholarPubMed
Picciotto, MR, Brunzell, DH, Caldarone, BJ. Effect of nicotine and nicotinic receptors on anxiety and depression. Neuroreport. 2002; 13(9), 10971106.CrossRefGoogle ScholarPubMed
Liu, Y, Le Foll, B, Liu, Y, Wang, X, Lu, L. Conditioned place preference induced by licit drugs: establishment, extinction, and reinstatement. ScientificWorldJournal. 2008; 8, 12281245.CrossRefGoogle ScholarPubMed
O’Dell, LE, Khroyan, TV. Rodent models of nicotine reward: what do they tell us about tobacco abuse in humans? Pharmacol Biochem Behav. 2009; 91(4), 481488.CrossRefGoogle ScholarPubMed
Tzschentke, TM. Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol. 2007; 12(3-4), 227462.CrossRefGoogle ScholarPubMed
Dutra-Tavares, AC, Silva, JO, Nunes-Freitas, AL, et al. Maternal undernutrition during lactation alters nicotine reward and DOPAC/dopamine ratio in cerebral cortex in adolescent mice, but does not affect nicotine-induced nAChRs upregulation. Int J Dev Neurosci. 2018; 65(1), 4553.CrossRefGoogle Scholar
Nunes-Freitas, AL, Manhães, AC, Dutra-Tavares, AC, et al. Sex- and age-dependent differences in nicotine susceptibility evoked by developmental exposure to tobacco smoke and/or ethanol in mice. J Dev Orig Health Dis. 2021; 12(6), 940951.CrossRefGoogle ScholarPubMed
Abreu-Villaça, Y, Correa-Santos, M, Dutra-Tavares, AC, et al. A ten fold reduction of nicotine yield in tobacco smoke does not spare the central cholinergic system in adolescent mice. Int J Dev Neurosci. 2016; 52(1), 93103.CrossRefGoogle Scholar
Seth, P, Cheeta, S, Tucci, S, File, SE. Nicotinic-serotonergic interactions in brain and behaviour. Pharmacol Biochem Behav. 2002; 71(4), 795805.CrossRefGoogle ScholarPubMed
Pistillo, F, Fasoli, F, Moretti, M, et al. Chronic nicotine and withdrawal affect glutamatergic but not nicotinic receptor expression in the mesocorticolimbic pathway in a region-specific manner. Pharmacol Res. 2016; 103, 167176.CrossRefGoogle ScholarPubMed
Yoshitake, T, Kehr, J, Todoroki, K, Nohta, H, Yamaguchi, M. Derivatization chemistries for determination of serotonin, norepinephrine and dopamine in brain microdialysis samples by liquid chromatography with fluorescence detection. Biomed Chromatogr. 2006; 20(3), 267281.CrossRefGoogle ScholarPubMed
Yoshitake, T, Kehr, J, Yoshitake, S, Fujino, K, Nohta, H, Yamaguchi, M. Determination of serotonin, noradrenaline, dopamine and their metabolites in rat brain extracts and microdialysis samples by column liquid chromatography with fluorescence detection following derivatization with benzylamine and 1,2-diphenylethylenediamine. J Chromatogr B Anal Technol Biomed Life Sci. 2004; 807(2), 177183.CrossRefGoogle ScholarPubMed
Ohkura, Y, Kai, M, Nohta, H. Fluorogenic reactions for biomedical chromatography. J Chromatogr B Biomed Sci Appl. 1994; 659(1-2), 85107.CrossRefGoogle ScholarPubMed
Kendler, KS, Myers, J, Prescott, CA. Specificity of genetic and environmental risk factors for symptoms of cannabis, cocaine, alcohol, caffeine, and nicotine dependence. Arch Gen Psychiatry. 2007; 64(11), 13131320.CrossRefGoogle ScholarPubMed
Martin, CA, Cook, C, Woodring, JH, et al. Caffeine use: association with nicotine use, aggression, and other psychopathology in psychiatric and pediatric outpatient adolescents. ScientificWorldJournal. 2008; 8, 512516.CrossRefGoogle ScholarPubMed
Ibrahim, MK, Kamal, M, Tikamdas, R, Nouh, RA, Tian, J, Sayed, M. Effects of chronic caffeine administration on behavioral and molecular adaptations to sensory contact model induced stress in adolescent male mice. Behav Genet. 2020; 50(5), 374383.CrossRefGoogle ScholarPubMed
Poole, R, Braak, D, Gould, T. Concentration- and age-dependent effects of chronic caffeine on contextual fear conditioning in C57BL/6J mice. Behav Brain Res. 2016; 298(Pt A), 6977.CrossRefGoogle ScholarPubMed
Arnold, M, Williams, P, McArthur, J, et al. Effects of chronic caffeine exposure during adolescence and subsequent acute caffeine challenge during adulthood on rat brain serotonergic systems. Neuropharmacology. 2019; 148, 257271.CrossRefGoogle ScholarPubMed
Krahe, TE, Filgueiras, CC, Quaresma, S, et al. Energy drink enhances the behavioral effects of alcohol in adolescent mice. Neurosci Lett. 2017; 651, 102108.CrossRefGoogle ScholarPubMed
Temple, JL. Caffeine use in children: what we know, what we have left to learn, and why we should worry. Neurosci Biobehav Rev. 2009; 33(6), 793806.CrossRefGoogle ScholarPubMed
James, JE. Maternal caffeine consumption and pregnancy outcomes: a narrative review with implications for advice to mothers and mothers-to-be. BMJ Evidence-Based Med. 2021; 26(3), 114115.CrossRefGoogle ScholarPubMed
Björklund, O, Kahlström, J, Salmi, P, Fredholm, BB. Perinatal caffeine, acting on maternal adenosine A1 receptors, causes long-lasting behavioral changes in mouse offspring. PLoS One. 2008;; 3(12), e3977.CrossRefGoogle ScholarPubMed
Sallaberry, C, Paula, A, Rocha, A, et al. Sex differences in the effects of pre- and postnatal caffeine exposure on behavior and synaptic proteins in pubescent rats.. Prog Neuropsychopharmacol Biol Ppsychiatry. 2018; 81, 416425.CrossRefGoogle ScholarPubMed
El, Yacoubi M, Ledent, C, Ois, JF, et al. The stimulant effects of caffeine on locomotor behaviour in mice are mediated through its blockade of adenosine A(2A) receptors. Br J Pharmacol. 2000; 129(7), 14651473.Google Scholar
Neill, CEO, Newsom, RJ, Stafford, J, et al. Adolescent caffeine consumption increases adulthood anxiety- related behavior and modifies neuroendocrine signaling. Psychoneuroendocrinology. 2016; 67, 4050.Google Scholar
Bressan, RA, Pilowsky, LS. Hipótese glutamatérgica da esquizofrenia glutamatergic hypothesis of schizophrenia. Rev Bras Psiquiatr. 2003; 25(3), 177183.CrossRefGoogle ScholarPubMed
Matovu, D, Alele, PE. Seizure vulnerability and anxiety responses following chronic co-administration and acute withdrawal of caffeine and ethanol in a rat model. J Basic Clin Physiol Pharmacol. 2018; 29(1), 110.CrossRefGoogle ScholarPubMed
Wilar, G, Shinoda, Y, Sasaoka, T, Fukunaga, K. Crucial role of dopamine D2 receptor signaling in nicotine-induced conditioned place preference. Mol Neurobiol. 2019; 56(12), 79117928.CrossRefGoogle ScholarPubMed
Cohen, B, Mackey, E, Grady, S, et al. Nicotinic cholinergic mechanisms causing elevated dopamine release and abnormal locomotor behavior. Neuroscience. 2012; 200, 3141.CrossRefGoogle ScholarPubMed
Dutra-Tavares, AC, Manhães, AC, Silva, JO, et al. Locomotor response to acute nicotine in adolescent mice is altered by maternal undernutrition during lactation. Int J Dev Neurosci. 2015; 7(Pt B), 278285.CrossRefGoogle Scholar
Taura, J, Sahlholm, K, Craenenbroeck, MWK Van, Ciruela, SFF. Behavioral control by striatal adenosine A 2A -dopamine D 2 receptor heteromers 2018, 111.CrossRefGoogle Scholar
Franco, R, Lluis, C, Canela, E, et al. Receptor – receptor interactions involving adenosine A 1 or dopamine D 1 receptors and accessory proteins. J Neural Transm. 2007; 114(1), 93104.CrossRefGoogle ScholarPubMed
Ferré, S. Mechanisms of the psychostimulant effects of caffeine: implications for substance use disorders. Psychopharmacology (Berl). 2016; 233(10), 19631979.CrossRefGoogle ScholarPubMed
Filip, M, Zaniewska, M, Frankowska, M, Wydra, K, Fuxe, K. The importance of the adenosine a 2A receptor-dopamine D2 receptor interaction in drug addiction. Curr Med Chem. 2012; 19(3), 317355.CrossRefGoogle ScholarPubMed
Metaxas, A, Al-hasani, R, Farshim, P, et al. Genetic deletion of the adenosine A 2A receptor prevents nicotine-induced upregulation of a 7, but not a 4 b 2 * nicotinic acetylcholine receptor binding in the brain. Neuropharmacology. 2013; 71, 228236.CrossRefGoogle Scholar
Garção, P, Szabó, EC, Wopereis, S, Castro, AA, Tomé, Â.R. Functional interaction between pre-synaptic α 6 β 2-containing nicotinic and adenosine A 2A receptors in the control of dopamine release in the rat striatum. Br J Pharmacol. 2013; 169(7), 16001611.CrossRefGoogle Scholar
Porciúncula, LO, Sallaberry, C, Mioranzza, S, Henrique, P, Botton, S, Rosemberg, DB. The Janus face of caffeine. Neurochem Int. 2013; 63(6), 594609.CrossRefGoogle ScholarPubMed
Karcz-kubicha, M, Antoniou, K, Terasmaa, A, et al. Involvement of adenosine A 1 and a 2A receptors in the motor effects of caffeine after its acute and chronic administration. Neuropsychopharmacology. 2003; 28(7), 12811291.CrossRefGoogle Scholar
Quarta, D, Ferre, S, Solinas, M, bing, You Z, Goldberg, SR. Opposite modulatory roles for adenosine A 1 and A 2A receptors on glutamate and dopamine release in the shell of the nucleus accumbens. Effects of chronic caffeine exposure. J Neurochem. 2004; 88(5), 11511158.CrossRefGoogle Scholar
Rezvani, AH, Sexton, HG, Johnson, J, Wells, C, Gordon, K, Levin, ED. Effects of caffeine on alcohol consumption and nicotine self- administration in rats. Alcohol Clin Exp Res. 2013; 37(9), 16091617.CrossRefGoogle ScholarPubMed
Porru, S, López-Cruz, L, Carratalá-Ros, C, Salamone, JD, Acquas, E, Correa, M. Impact of caffeine on ethanol-induced stimulation and sensitization: changes in ERK and DARPP-32 phosphorylation in nucleus accumbens. Alcohol Clin Exp Res. 2021; 45(3), 608619.CrossRefGoogle ScholarPubMed
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