Neurochemical and Behavioral Consequences of Ethanol and/or Caffeine
Exposure: Effects in Zebrafish and Rodents

Carly    L.    Clayman; Victoria    P.    Connaughton
doi:10.2174/1570159X19666211111142027
Abstract

Zebrafish are increasingly being utilized to model the behavioral and neurochemical effects of pharmaceuticals and, more recently, pharmaceutical interactions. Zebrafish models of stress establish that both caffeine and ethanol influence anxiety, though few studies have implemented coadministration to assess the interaction of anxiety and reward-seeking. Caffeine exposure in zebrafish is teratogenic, causing developmental abnormalities in the cardiovascular, neuromuscular, and nervous systems of embryos and larvae. Ethanol is also a teratogen and, as an anxiolytic substance, may be able to offset the anxiogenic effects of caffeine. Co-exposure to caffeine and alcohol impacts neuroanatomy and behavior in adolescent animal models, suggesting stimulant substances may moderate the impact of alcohol on neural circuit development. Here, we review the literature describing neuropharmacological and behavioral consequences of caffeine and/or alcohol exposure in the zebrafish model, focusing on neurochemistry, locomotor effects, and behavioral assessments of stress/anxiety as reported in adolescent/juvenile and adult animals. The purpose of this review is twofold: (1) describe the work in zebrafish documenting the effects of ethanol and/or caffeine exposure and (2) compare these zebrafish studies with comparable experiments in rodents. We focus on specific neurochemical pathways (dopamine, serotonin, adenosine, GABA), anxiety-type behaviors (assessed with a novel tank, thigmotaxis, shoaling), and locomotor changes resulting from both individual and co-exposure. We compare findings in zebrafish with those in rodent models, revealing similarities across species and identifying conservation of mechanisms that potentially reinforce coaddiction.
Keywords: Danio rerio, ethanol, caffeine, anxiety, adenosine, novel tank, scototaxis, shoaling.
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[1] 
Correa, M.; Lopez-Cruz, L.; Porru, S.; Salamone, J. The impact of ethanol plus caffeine exposure on cognitive, emotional, and motivational effects related to social functioning. Neuroscience of Alcohol; Elsevier, 2019, pp. 545-554.
[2] 
Tran, S. Acute and chronic alcohol effects in zebrafish. Behavioral and Neural Genetics of Zebrafish; Elsevier, 2020, pp. 325-341.
[http://dx.doi.org/10.1016/B978-0-12-817528-6.00020-6] 
[3] 
Abozaid, A.; Trzuskot, L.; Najmi, Z.; Paul, I.; Tsang, B.; Gerlai, R. Developmental stage and genotype dependent behavioral effects of embryonic alcohol exposure in zebrafish larvae. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 97 ,109774
[http://dx.doi.org/10.1016/j.pnpbp.2019.109774] [PMID:  31655157] 
[4] 
Fernandes, Y.; Buckley, D.M.; Eberhart, J.K. Diving into the world of alcohol teratogenesis: a review of zebrafish models of fetal alcohol spectrum disorder. Biochem. Cell Biol.,  2018, 96(2), 88-97.
[http://dx.doi.org/10.1139/bcb-2017-0122] [PMID:  28817785] 
[5] 
Lovely, C.B.; Fernandes, Y.; Eberhart, J.K. Fishing for fetal alcohol spectrum disorders: zebrafish as a model for ethanol teratogenesis. Zebrafish,  2016, 13(5), 391-398.
[http://dx.doi.org/10.1089/zeb.2016.1270] [PMID:  27186793] 
[6] 
Pinheiro-da-Silva, J.; Luchiari, A.C. Embryonic ethanol exposure on zebrafish early development. Brain Behav.,  2021, 11(6) ,e02062
[http://dx.doi.org/10.1002/brb3.2062] [PMID:  33939334] 
[7] 
Parichy, D.M.; Elizondo, M.R.; Mills, M.G.; Gordon, T.N.; Engeszer, R.E. Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev. Dyn.,  2009, 238(12), 2975-3015.
[http://dx.doi.org/10.1002/dvdy.22113] [PMID:  19891001] 
[8] 
Westphal, R.E.; O’Malley, D.M. Fusion of locomotor maneuvers, and improving sensory capabilities, give rise to the flexible homing strikes of juvenile zebrafish. Front. Neural Circuits,  2013, 7, 108.
[http://dx.doi.org/10.3389/fncir.2013.00108] [PMID:  23761739] 
[9] 
O’Neill, C.E.; Levis, S.C.; Schreiner, D.C.; Amat, J.; Maier, S.F.; Bachtell, R.K. Effects of adolescent caffeine consumption on cocaine sensitivity. Neuropsychopharmacology,  2015, 40(4), 813-821.
[http://dx.doi.org/10.1038/npp.2014.278] [PMID:  25328052] 
[10] 
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. Periadolescent rats (P41-50) exhibit increased susceptibility to D-methamphetamine-induced long-term spatial and sequential learning deficits compared to juvenile (P21-30 or P31-40) or adult rats (P51-60). Neurotoxicol. Teratol.,  2005, 27(1), 117-134.
[http://dx.doi.org/10.1016/j.ntt.2004.09.005] [PMID:  15681126] 
[11] 
Robins, M.T.; Lu, J.; van Rijn, R.M. Unique behavioral and neurochemical effects induced by repeated adolescent consumption of caffeine-mixed alcohol in C57B/6 mice. PLoS One,  2016, 11(7) ,e0158189
[http://dx.doi.org/10.1371/journal.pone.0158189] [PMID:  27380261] 
[12] 
Arain, M.; Haque, M.; Johal, L.; Mathur, P.; Nel, W.; Rais, A.; Sandhu, R.; Sharma, S. Maturation of the adolescent brain. Neuropsychiatr. Dis. Treat.,  2013, 9, 449-461.
[PMID:  23579318] 
[13] 
Casey, B.J.; Getz, S.; Galvan, A. The adolescent brain. Dev. Rev.,  2008, 28(1), 62-77.
[http://dx.doi.org/10.1016/j.dr.2007.08.003] [PMID:  18688292] 
[14] 
Smith, R.F. Animal models of periadolescent substance abuse. Neurotoxicol. Teratol.,  2003, 25(3), 291-301.
[http://dx.doi.org/10.1016/S0892-0362(02)00349-5] [PMID:  12757826] 
[15] 
Crews, F.T.; Vetreno, R.P.; Broadwater, M.A.; Robinson, D.L. Adolescent alcohol exposure persistently impacts adult neurobiology and behavior. Pharmacol. Rev.,  2016, 68(4), 1074-1109.
[http://dx.doi.org/10.1124/pr.115.012138] [PMID:  27677720] 
[16] 
Cole, G.J.; Zhang, C.; Ojiaku, P.; Bell, V.; Devkota, S.; Mukhopadhyay, S. Effects of ethanol exposure on nervous system development in zebrafish. Int. Rev. Cell Mol. Biol.,  2012, 299, 255-315.
[http://dx.doi.org/10.1016/B978-0-12-394310-1.00007-2] [PMID:  22959306] 
[17] 
De Bellis, M.D.; Van Voorhees, E.; Hooper, S.R.; Gibler, N.; Nelson, L.; Hege, S.G.; Payne, M.E.; MacFall, J. Diffusion tensor measures of the corpus callosum in adolescents with adolescent onset alcohol use disorders. Alcohol. Clin. Exp. Res.,  2008, 32(3), 395-404.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00603.x] [PMID:  18241319] 
[18] 
Silveri, M.M.; Rohan, M.L.; Pimentel, P.J.; Gruber, S.A.; Rosso, I.M.; Yurgelun-Todd, D.A. Sex differences in the relationship between white matter microstructure and impulsivity in adolescents. Magn. Reson. Imaging,  2006, 24(7), 833-841.
[http://dx.doi.org/10.1016/j.mri.2006.03.012] [PMID:  16916700] 
[19] 
Spear, L. Modeling adolescent development and alcohol use in animals. Alcohol Res. Health,  2000, 24(2), 115-123.
[PMID:  11199278] 
[20] 
Spear, L.P.; Swartzwelder, H.S. Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci. Biobehav. Rev.,  2014, 45, 1-8.
[http://dx.doi.org/10.1016/j.neubiorev.2014.04.012] [PMID:  24813805] 
[21] 
Séguret, A.; Collignon, B.; Halloy, J. Strain differences in the collective behaviour of zebrafish (Danio rerio) in heterogeneous environment. R. Soc. Open Sci.,  2016, 3(10) ,160451
[http://dx.doi.org/10.1098/rsos.160451] [PMID:  27853558] 
[22] 
Spinello, C.; Macrì, S.; Porfiri, M. Acute ethanol administration affects zebrafish preference for a biologically inspired robot. Alcohol,  2013, 47(5), 391-398.
[http://dx.doi.org/10.1016/j.alcohol.2013.04.003] [PMID:  23725654] 
[23] 
Vignet, C.; Bégout, M-L.; Péan, S.; Lyphout, L.; Leguay, D.; Cousin, X. Systematic screening of behavioral responses in two zebrafish strains. Zebrafish,  2013, 10(3), 365-375.
[http://dx.doi.org/10.1089/zeb.2013.0871] [PMID:  23738739] 
[24] 
Holden, L.A.; Brown, K.H. Baseline mRNA expression differs widely between common laboratory strains of zebrafish. Sci. Rep.,  2018, 8(1), 4780.
[http://dx.doi.org/10.1038/s41598-018-23129-4] [PMID:  29555936] 
[25] 
Pan, Y.; Chatterjee, D.; Gerlai, R. Strain dependent gene expression and neurochemical levels in the brain of zebrafish: focus on a few alcohol related targets. Physiol. Behav.,  2012, 107(5), 773-780.
[http://dx.doi.org/10.1016/j.physbeh.2012.01.017] [PMID:  22313674] 
[26] 
van den Bos, R.; Mes, W.; Galligani, P.; Heil, A.; Zethof, J.; Flik, G.; Gorissen, M. Further characterisation of differences between TL and AB zebrafish (Danio rerio): Gene expression, physiology and behaviour at day 5 of the larval stage. PLoS One,  2017, 12(4) ,e0175420
[http://dx.doi.org/10.1371/journal.pone.0175420] [PMID:  28419104] 
[27] 
Guryev, V.; Koudijs, M.J.; Berezikov, E.; Johnson, S.L.; Plasterk, R.H.; van Eeden, F.J.; Cuppen, E. Genetic variation in the zebrafish. Genome Res.,  2006, 16(4), 491-497.
[http://dx.doi.org/10.1101/gr.4791006] [PMID:  16533913] 
[28] 
van den Bos, R.; Althuizen, J.; Tschigg, K.; Bomert, M.; Zethof, J.; Filk, G.; Gorissen, M. .Early life exposure to cortisol in zebrafish (Danio rerio): similarities and differences in behaviour and physiology between larvae of the AB and TL strains. Behav. Pharmacol.,  2019, 30(2 and 3-Spec Issue), 260-271.
[http://dx.doi.org/10.1097/FBP.0000000000000470] [PMID:  30724799] 
[29] 
Chatterjee, D.; Shams, S.; Gerlai, R. Chronic and acute alcohol administration induced neurochemical changes in the brain: comparison of distinct zebrafish populations. Amino Acids,  2014, 46(4), 921-930.
[http://dx.doi.org/10.1007/s00726-013-1658-y] [PMID:  24381007] 
[30] 
Tran, S.; Fulcher, N.; Nowicki, M.; Desai, P.; Tsang, B.; Facciol, A.; Chow, H.; Gerlai, R. Time-dependent interacting effects of caffeine, diazepam, and ethanol on zebrafish behaviour. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2017, 75, 16-27. b
[http://dx.doi.org/10.1016/j.pnpbp.2016.12.004] [PMID: 28025019] 
[31] 
Rosa, L.V.; Ardais, A.P.; Costa, F.V.; Fontana, B.D.; Quadros, V.A.; Porciúncula, L.O.; Rosemberg, D.B. Different effects of caffeine on behavioral neurophenotypes of two zebrafish populations. Pharmacol. Biochem. Behav.,  2018, 165, 1-8.
[http://dx.doi.org/10.1016/j.pbb.2017.12.002] [PMID:  29241648] 
[32] 
Das, S.K.; Vasudevan, D.M. Alcohol-induced oxidative stress. Life Sci.,  2007, 81(3), 177-187.
[http://dx.doi.org/10.1016/j.lfs.2007.05.005] [PMID:  17570440] 
[33] 
Zima, T.; Fialová, L.; Mestek, O.; Janebová, M.; Crkovská, J.; Malbohan, I.; Stípek, S.; Mikulíková, L.; Popov, P. Oxidative stress, metabolism of ethanol and alcohol-related diseases. J. Biomed. Sci.,  2001, 8(1), 59-70.
[http://dx.doi.org/10.1007/BF02255972] [PMID:  11173977] 
[34] 
Comporti, M.; Signorini, C.; Leoncini, S.; Gardi, C.; Ciccoli, L.; Giardini, A.; Vecchio, D.; Arezzini, B. Ethanol-induced oxidative stress: basic knowledge. Genes Nutr.,  2010, 5(2), 101-109.
[http://dx.doi.org/10.1007/s12263-009-0159-9] [PMID:  20606811] 
[35] 
Krystal, J.; Tabakoff, B. Ethanol abuse, dependence, and withdrawal: neurobiology and clinical implications. Psychopharmacol A Fifth Gener Progress; Lippincott Williams & Wilkins: Philadelphia, PA, 2002, pp. 1425-1443.
[36] 
Walter, H.J.; Messing, R.O. Regulation of neuronal voltage-gated calcium channels by ethanol. Neurochem. Int.,  1999, 35(2), 95-101.
[http://dx.doi.org/10.1016/S0197-0186(99)00050-9] [PMID:  10405992] 
[37] 
Facciol, A.; Bailleul, C.; Nguyen, S.; Chatterjee, D.; Gerlai, R. Developmental stage-dependent deficits induced by embryonic ethanol exposure in zebrafish: A neurochemical analysis. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 99 ,109859
[http://dx.doi.org/10.1016/j.pnpbp.2020.109859] [PMID:  31917146] 
[38] 
Gerlai, R.; Chatterjee, D.; Pereira, T.; Sawashima, T.; Krishnannair, R. Acute and chronic alcohol dose: population differences in behavior and neurochemistry of zebrafish. Genes Brain Behav.,  2009, 8(6), 586-599.
[http://dx.doi.org/10.1111/j.1601-183X.2009.00488.x] [PMID:  19243447] 
[39] 
Mahabir, S.; Chatterjee, D.; Gerlai, R. Strain dependent neurochemical changes induced by embryonic alcohol exposure in zebrafish. Neurotoxicol. Teratol.,  2014, 41, 1-7.
[http://dx.doi.org/10.1016/j.ntt.2013.11.001] [PMID:  24225385] 
[40] 
Mahabir, S.; Chatterjee, D.; Gerlai, R. Short exposure to low concentrations of alcohol during embryonic development has only subtle and strain- dependent effect on the levels of five amino acid neurotransmitters in zebrafish. Neurotoxicol. Teratol.,  2018, 68, 91-96.
[http://dx.doi.org/10.1016/j.ntt.2018.05.005] [PMID:  29886245] 
[41] 
Maximino, C.; Herculano, A.M. A review of monoaminergic neuropsychopharmacology in zebrafish. Zebrafish,  2010, 7(4), 359-378.
[http://dx.doi.org/10.1089/zeb.2010.0669] [PMID:  21158565] 
[42] 
Renier, C.; Faraco, J.H.; Bourgin, P.; Motley, T.; Bonaventure, P.; Rosa, F.; Mignot, E. Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet. Genomics,  2007, 17(4), 237-253.
[http://dx.doi.org/10.1097/FPC.0b013e3280119d62] [PMID:  17496723] 
[43] 
Schweitzer, J.; Driever, W. Development of the dopamine systems in zebrafish. Adv. Exp. Med. Biol.,  2009, 651, 1-14.
[http://dx.doi.org/10.1007/978-1-4419-0322-8_1] [PMID:  19731546] 
[44] 
Dlugos, C.A.; Rabin, R.A. Ethanol effects on three strains of zebrafish: model system for genetic investigations. Pharmacol. Biochem. Behav.,  2003, 74(2), 471-480.
[http://dx.doi.org/10.1016/S0091-3057(02)01026-2] [PMID:  12479969] 
[45] 
Lin, J-N.; Chang, L-L.; Lai, C-H.; Lin, K-J.; Lin, M-F.; Yang, C-H.; Lin, H.H.; Chen, Y.H. Development of an animal model for alcoholic liver disease in zebrafish. Zebrafish,  2015, 12(4), 271-280.
[http://dx.doi.org/10.1089/zeb.2014.1054] [PMID:  25923904] 
[46] 
Crews, F.T.; Braun, C.J.; Hoplight, B.; Switzer, R.C., III; Knapp, D.J. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol. Clin. Exp. Res.,  2000, 24(11), 1712-1723.
[http://dx.doi.org/10.1111/j.1530-0277.2000.tb01973.x] [PMID:  11104119] 
[47] 
Ehlers, C.L.; Criado, J.R. Adolescent ethanol exposure: does it produce long-lasting electrophysiological effects? Alcohol,  2010, 44(1), 27-37.
[http://dx.doi.org/10.1016/j.alcohol.2009.09.033] [PMID:  20113872] 
[48] 
Maldonado-Devincci, A.M.; Badanich, K.A.; Kirstein, C.L. Alcohol during adolescence selectively alters immediate and long-term behavior and neurochemistry. Alcohol,  2010, 44(1), 57-66.
[http://dx.doi.org/10.1016/j.alcohol.2009.09.035] [PMID:  20113874] 
[49] 
Nagel, B.J.; Schweinsburg, A.D.; Phan, V.; Tapert, S.F. Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res.,  2005, 139(3), 181-190.
[http://dx.doi.org/10.1016/j.pscychresns.2005.05.008] [PMID:  16054344] 
[50] 
Witt, E.D. Research on alcohol and adolescent brain development: opportunities and future directions. Alcohol,  2010, 44(1), 119-124.
[http://dx.doi.org/10.1016/j.alcohol.2009.08.011] [PMID:  20113880] 
[51] 
Arias-Carrión, O.; Stamelou, M.; Murillo-Rodríguez, E.; Menéndez-González, M.; Pöppel, E. Dopaminergic reward system: a short integrative review. Int. Arch. Med.,  2010, 3, 24.
[http://dx.doi.org/10.1186/1755-7682-3-24] [PMID:  20925949] 
[52] 
Ayano, G. Dopamine: receptors, functions, synthesis, pathways, locations and mental disorders: review of literatures. J Ment Disord Treat.,  2016, 2 ,10000120
[http://dx.doi.org/10.4172/2471-271X.1000120] 
[53] 
Ma, H.; Zhu, G. The dopamine system and alcohol dependence. Shanghai Jingshen Yixue,  2014, 26(2), 61-68.
[PMID:  25092951] 
[54] 
Carrara-Nascimento, P.F.; Hoffmann, L.B.; Flório, J.C.; Planeta, C.S.; Camarini, R. Effects of ethanol exposure during adolescence or adulthood on locomotor sensitization and dopamine levels in the reward system. Front. Behav. Neurosci.,  2020, 14, 31.
[http://dx.doi.org/10.3389/fnbeh.2020.00031] [PMID:  32210774] 
[55] 
Ramachandra, V.; Phuc, S.; Franco, A.C.; Gonzales, R.A. Ethanol preference is inversely correlated with ethanol-induced dopamine release in 2 substrains of C57BL/6 mice. Alcohol. Clin. Exp. Res.,  2007, 31(10), 1669-1676.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00463.x] [PMID:  17651469] 
[56] 
Tang, A.; George, M.A.; Randall, J.A.; Gonzales, R.A. Ethanol increases extracellular dopamine concentration in the ventral striatum in C57BL/6 mice. Alcohol. Clin. Exp. Res.,  2003, 27(7), 1083-1089.
[http://dx.doi.org/10.1097/01.ALC.0000075825.14331.65] [PMID:  12878914] 
[57] 
Bassareo, V.; Cucca, F.; Frau, R.; Di Chiara, G. Changes in dopamine transmission in the nucleus accumbens shell and core during ethanol and sucrose self-administration. Front. Behav. Neurosci.,  2017, 11, 71.
[http://dx.doi.org/10.3389/fnbeh.2017.00071] [PMID:  28507512] 
[58] 
Weiss, F.; Lorang, M.T.; Bloom, F.E.; Koob, G.F. Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J. Pharmacol. Exp. Ther.,  1993, 267(1), 250-258.
[PMID:  8229752] 
[59] 
Rink, E.; Wullimann, M.F. The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res.,  2001, 889(1-2), 316-330.
[http://dx.doi.org/10.1016/S0006-8993(00)03174-7] [PMID:  11166725] 
[60] 
Alexandre, M.C.M.; Mendes, N.V.; Torres, C.A.; Baldin, S.L.; Bernardo, H.T.; Scussel, R.; Baggio, S.; Mussulini, B.H.M.; Zenki, K.C.; da Rosa, M.I.; Rico, E.P. Weekly ethanol exposure alters dopaminergic parameters in zebrafish brain. Neurotoxicol. Teratol.,  2019, 75 ,106822
[http://dx.doi.org/10.1016/j.ntt.2019.106822] [PMID:  31421226] 
[61] 
Nowicki, M.; Tran, S.; Chatterjee, D.; Gerlai, R. Inhibition of phosphorylated tyrosine hydroxylase attenuates ethanol-induced hyperactivity in adult zebrafish (Danio rerio). Pharmacol. Biochem. Behav.,  2015, 138, 32-39.
[http://dx.doi.org/10.1016/j.pbb.2015.09.008] [PMID:  26366782] 
[62] 
Rosemberg, D.B.; Braga, M.M.; Rico, E.P.; Loss, C.M.; Córdova, S.D.; Mussulini, B.H.; Blaser, R.E.; Leite, C.E.; Campos, M.M.; Dias, R.D.; Calcagnotto, M.E.; de Oliveira, D.L.; Souza, D.O. Behavioral effects of taurine pretreatment in zebrafish acutely exposed to ethanol. Neuropharmacology,  2012, 63(4), 613-623.
[http://dx.doi.org/10.1016/j.neuropharm.2012.05.009] [PMID:  22634362] 
[63] 
Weiner, N.; Molinoff, P. .Catecholamines.Basic Neurochemistry,	5th ed; Siegel, G.; Agranoff, B.; Albers, R.; Molinoff, P., Eds.; RavenPress: New York, , 1994; pp. 261-281.
[64] 
Acevedo, J.; Santana-Almansa, A.; Matos-Vergara, N.; Marrero-Cordero, L.R.; Cabezas-Bou, E.; Díaz-Ríos, M. Caffeine stimulates locomotor activity in the mammalian spinal cord via adenosine A1 receptor-dopamine D1 receptor interaction and PKA-dependent mechanisms. Neuropharmacology,  2016, 101, 490-505.
[http://dx.doi.org/10.1016/j.neuropharm.2015.10.020] [PMID:  26493631] 
[65] 
Navarrete, F.; Rubio, G.; Manzanares, J. Effects of naltrexone plus topiramate on ethanol self-administration and tyrosine hydroxylase gene expression changes. Addict. Biol.,  2014, 19(5), 862-873.
[http://dx.doi.org/10.1111/adb.12058] [PMID:  23573810] 
[66] 
Li, X.; Li, X.; Li, Y-X.; Zhang, Y.; Chen, D.; Sun, M-Z.; Zhao, X.; Chen, D.Y.; Feng, X.Z. The difference between anxiolytic and anxiogenic effects induced by acute and chronic alcohol exposure and changes in associative learning and memory based on color preference and the cause of Parkinson-like behaviors in zebrafish. PLoS One,  2015, 10(11) ,e0141134
[http://dx.doi.org/10.1371/journal.pone.0141134] [PMID:  26558894] 
[67] 
Tran, S.; Gerlai, R. Time-course of behavioural changes induced by ethanol in zebrafish (Danio rerio). Behav. Brain Res.,  2013, 252, 204-213.
[http://dx.doi.org/10.1016/j.bbr.2013.05.065] [PMID:  23756142] 
[68] 
Paiva, I.M.; Sartori, B.M.; Castro, T.F.D.; Lunkes, L.C.; Virote, B.D.C.R.; Murgas, L.D.S.; de Souza, R.P.; Brunialti-Godard, A.L. Behavioral plasticity and gene regulation in the brain during an intermittent ethanol exposure in adult zebrafish population. Pharmacol. Biochem. Behav.,  2020, 192 ,172909
[http://dx.doi.org/10.1016/j.pbb.2020.172909] [PMID:  32194086] 
[69] 
Frazer, A.; Hensler, J. Serotonin.Basic Neurochemistry, 5th ed;
	Siegel, G.; Agranoff, B.; Albers, R.; Molinoff, P., Eds.; Raven
	Press: New York, , 1994; pp. 283-308.
[70] 
Herculano, A.M.; Maximino, C. Serotonergic modulation of zebrafish behavior: towards a paradox. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2014, 55, 50-66.
[http://dx.doi.org/10.1016/j.pnpbp.2014.03.008] [PMID:  24681196] 
[71] 
Maximino, C.; Lima, M.; Araujo, J.; Oliveira, K.; Herculano, A.; Stewart, A. The serotonergic system of zebrafish: genomics, neuroanatomy, and neuropharmacology. Serotonin Biosynthesis, Regul Heal Implic. New York, NY. Nova Sci.,  2013, 53-67.
[72] 
Chatterjee, D.; Gerlai, R. High precision liquid chromatography analysis of dopaminergic and serotoninergic responses to acute alcohol exposure in zebrafish. Behav. Brain Res.,  2009, 200(1), 208-213.
[http://dx.doi.org/10.1016/j.bbr.2009.01.016] [PMID:  19378384] 
[73] 
Langen, B.; Dietze, S.; Fink, H. Acute effect of ethanol on anxiety and 5-HT in the prefrontal cortex of rats. Alcohol,  2002, 27(2), 135-141.
[http://dx.doi.org/10.1016/S0741-8329(02)00219-7] [PMID:  12106833] 
[74] 
Thielen, R.J.; Bare, D.J.; McBride, W.J.; Lumeng, L.; Li, T.K. Ethanol-stimulated serotonin release in the ventral hippocampus: an absence of rapid tolerance for the alcohol-preferring P rat and insensitivity in the alcohol-nonpreferring NP rat. Pharmacol. Biochem. Behav.,  2002, 71(1-2), 111-117.
[http://dx.doi.org/10.1016/S0091-3057(01)00633-5] [PMID:  11812514] 
[75] 
Yan, Q.S. Extracellular dopamine and serotonin after ethanol monitored with 5-minute microdialysis. Alcohol,  1999, 19(1), 1-7.
[http://dx.doi.org/10.1016/S0741-8329(99)00006-3] [PMID:  10487381] 
[76] 
Lovinger, D.M. Serotonin’s role in alcohol’s effects on the brain. Alcohol Health Res. World,  1997, 21(2), 114-120.
[PMID:  15704346] 
[77] 
Tabakoff, B.; Boggan, W.O. Effects of ethanol on serotonin metabolism in brain. J. Neurochem.,  1974, 22(5), 759-764.
[http://dx.doi.org/10.1111/j.1471-4159.1974.tb04291.x] [PMID:  4407097] 
[78] 
LeMarquand, D.; Pihl, R.O.; Benkelfat, C. Serotonin and alcohol intake, abuse, and dependence: findings of animal studies. Biol.Psychiatry,  1994, 36(6), 395-421. b
[http://dx.doi.org/10.1016/0006-3223(94)91215-7] [PMID:  7803601] 
[79] 
Naito, A.; Muchhala, K.H.; Asatryan, L.; Trudell, J.R.; Homanics, G.E.; Perkins, D.I.; Davies, D.L.; Alkana, R.L. Glycine and GABA(A) ultra-sensitive ethanol receptors as novel tools for alcohol and brain research. Mol. Pharmacol.,  2014, 86(6), 635-646.
[http://dx.doi.org/10.1124/mol.114.093773] [PMID:  25245406] 
[80] 
Wu, G.; Liu, H.; Jin, J.; Hong, L.; Lan, Y.; Chu, C.P.; Qiu, D.L. Ethanol attenuates sensory stimulus-evoked responses in cerebellar granule cells via activation of GABA(A) receptors in vivo in mice. Neurosci. Lett.,  2014, 561, 107-111.
[http://dx.doi.org/10.1016/j.neulet.2013.12.049] [PMID:  24388841] 
[81] 
Paul, S.M. Alcohol-sensitive GABA receptors and alcohol antagonists. Proc. Natl. Acad. Sci. USA,  2006, 103(22), 8307-8308.
[http://dx.doi.org/10.1073/pnas.0602862103] [PMID:  16717187] 
[82] 
Roberto, M.; Madamba, S.G.; Moore, S.D.; Tallent, M.K.; Siggins, G.R. Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc. Natl. Acad. Sci. USA,  2003, 100(4), 2053-2058.
[http://dx.doi.org/10.1073/pnas.0437926100] [PMID:  12566570] 
[83] 
Goodman, A.C.; Wong, R.Y. Differential effects of ethanol on behavior and GABAA receptor expression in adult zebrafish (Danio rerio) with alternative stress coping styles. Sci. Rep.,  2020, 10(1), 13076.
[http://dx.doi.org/10.1038/s41598-020-69980-2] [PMID:  32753576] 
[84] 
Roberto, M.; Madamba, S.G.; Stouffer, D.G.; Parsons, L.H.; Siggins, G.R. Increased GABA release in the central amygdala of ethanol-dependent rats. J. Neurosci.,  2004, 24(45), 10159-10166.
[http://dx.doi.org/10.1523/JNEUROSCI.3004-04.2004] [PMID:  15537886] 
[85] 
Sundstrom-Poromaa, I.; Smith, D.H.; Gong, Q.H.; Sabado, T.N.; Li, X.; Light, A.; Wiedmann, M.; Williams, K.; Smith, S.S. Hormonally regulated alpha(4)beta(2)delta GABA(A) receptors are a target for alcohol. Nat. Neurosci.,  2002, 5(8), 721-722.
[http://dx.doi.org/10.1038/nn888] [PMID:  12118257] 
[86] 
Borghese, C.M. Stórustovu, Sí.; Ebert, B.; Herd, M.B.; Belelli, D.; Lambert, J.J.; Marshall, G.; Wafford, K.A.; Harris, R.A. The delta subunit of gamma-aminobutyric acid type A receptors does not confer sensitivity to low concentrations of ethanol. J. Pharmacol. Exp. Ther.,  2006, 316(3), 1360-1368.
[http://dx.doi.org/10.1124/jpet.105.092452] [PMID:  16272217] 
[87] 
Carvan, M.J., III; Loucks, E.; Weber, D.N.; Williams, F.E. Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol. Teratol.,  2004, 26(6), 757-768.
[http://dx.doi.org/10.1016/j.ntt.2004.06.016] [PMID:  15451040] 
[88] 
Zhang, C.; Ojiaku, P.; Cole, G.J. Forebrain and hindbrain development in zebrafish is sensitive to ethanol exposure involving agrin, Fgf, and sonic hedgehog function. Birth Defects Res. A Clin. Mol. Teratol.,  2013, 97(1), 8-27. [Part A
[http://dx.doi.org/10.1002/bdra.23099] [PMID:  23184466] 
[89] 
Mathur, P.; Berberoglu, M.A.; Guo, S. Preference for ethanol in zebrafish following a single exposure. Brain Behav Res.,  2011, 217(1), 128-133.
[http://dx.doi.org/10.1016/j.bbr.2010.10.015] [PMID:  20974186] 
[90] 
Blaser, R.E.; Rosemberg, D.B. Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. PLoS One,  2012, 7(5) ,e36931
[http://dx.doi.org/10.1371/journal.pone.0036931] [PMID:  22615849] 
[91] 
Araujo-Silva, H.; Pinheiro-da-Silva, J.; Silva, P.F.; Luchiari, A.C. Individual differences in response to alcohol exposure in zebrafish (Danio rerio). PLoS One,  2018, 13(6) ,e0198856
[http://dx.doi.org/10.1371/journal.pone.0198856] [PMID:  29879208] 
[92] 
Gerlai, R.; Lahav, M.; Guo, S.; Rosenthal, A. Drinks like a fish: zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol. Biochem. Behav.,  2000, 67(4), 773-782.
[http://dx.doi.org/10.1016/S0091-3057(00)00422-6] [PMID:  11166068] 
[93] 
Gerlai, R.; Ahmad, F.; Prajapati, S. Differences in acute alcohol-induced behavioral responses among zebrafish populations. Alcohol. Clin. Exp. Res.,  2008, 32(10), 1763-1773.
[http://dx.doi.org/10.1111/j.1530-0277.2008.00761.x] [PMID:  18652595] 
[94] 
Gerlai, R.; Lee, V.; Blaser, R. Effects of acute and chronic ethanol exposure on the behavior of adult zebrafish (Danio rerio). Pharmacol. Biochem. Behav.,  2006, 85(4), 752-761.
[http://dx.doi.org/10.1016/j.pbb.2006.11.010] [PMID:  17196640] 
[95] 
de Esch, C.; van der Linde, H.; Slieker, R.; Willemsen, R.; Wolterbeek, A.; Woutersen, R.; De Groot, D. Locomotor activity assay in zebrafish larvae: influence of age, strain and ethanol. Neurotoxicol. Teratol.,  2012, 34(4), 425-433.
[http://dx.doi.org/10.1016/j.ntt.2012.03.002] [PMID:  22484456] 
[96] 
Acevedo, M.B.; Nizhnikov, M.E.; Molina, J.C.; Pautassi, R.M. Relationship between ethanol-induced activity and anxiolysis in the open field, elevated plus maze, light-dark box, and ethanol intake in adolescent rats. Behav. Brain Res.,  2014, 265, 203-215.
[http://dx.doi.org/10.1016/j.bbr.2014.02.032] [PMID:  24583190] 
[97] 
Correa, M.; Arizzi, M.N.; Betz, A.; Mingote, S.; Salamone, J.D. Open field locomotor effects in rats after intraventricular injections of ethanol and the ethanol metabolites acetaldehyde and acetate. Brain Res. Bull.,  2003, 62(3), 197-202.
[http://dx.doi.org/10.1016/j.brainresbull.2003.09.013] [PMID:  14698353] 
[98] 
Nadal, R.; Armario, A.; Janak, P.H. Positive relationship between activity in a novel environment and operant ethanol self-administration in rats. Psychopharmacology (Berl.),  2002, 162(3), 333-338.
[http://dx.doi.org/10.1007/s00213-002-1091-5] [PMID:  12122492] 
[99] 
Griffin, W.C., III; Novak, A.J.; Middaugh, L.D.; Patrick, K.S. The interactive effects of methylphenidate and ethanol on ethanol consumption and locomotor activity in mice. Pharmacol. Biochem. Behav.,  2010, 95(3), 267-272.
[http://dx.doi.org/10.1016/j.pbb.2010.01.009] [PMID:  20122954] 
[100] 
Hilbert, M.L.; May, C.E.; Griffin, W.C., III Conditioned reinforcement and locomotor activating effects of caffeine and ethanol combinations in mice. Pharmacol. Biochem. Behav.,  2013, 110, 168-173.
[http://dx.doi.org/10.1016/j.pbb.2013.07.008] [PMID:  23872371] 
[101] 
Jerlhag, E. The antipsychotic aripiprazole antagonizes the ethanol- and amphetamine-induced locomotor stimulation in mice. Alcohol,  2008, 42(2), 123-127.
[http://dx.doi.org/10.1016/j.alcohol.2007.11.004] [PMID:  18358991] 
[102] 
Middaugh, L.D.; Bao, K.; Shepherd, C.L. Comparative effects of ethanol on motor activity and operant behavior. Pharmacol. Biochem. Behav.,  1992, 43(2), 625-629.
[http://dx.doi.org/10.1016/0091-3057(92)90202-Q] [PMID:  1438501] 
[103] 
Correa, M.; Sanchis-Segura, C.; Pastor, R.; Aragon, C.M. Ethanol intake and motor sensitization: the role of brain catalase activity in mice with different genotypes. Physiol. Behav.,  2004, 82(2-3), 231-240.
[http://dx.doi.org/10.1016/j.physbeh.2004.03.033] [PMID:  15276784] 
[104] 
Phillips, T.J.; Shen, E.H.; Shent, E. Neurochemical bases of locomotion and ethanol stimulant effects. Int. Rev. Neurobiol.,  1996, 39, 243-282.
[http://dx.doi.org/10.1016/S0074-7742(08)60669-8] [PMID:  8894850] 
[105] 
Frye, G.D.; Breese, G.R. An evaluation of the locomotor stimulating action of ethanol in rats and mice. Psychopharmacology (Berl.),  1981, 75(4), 372-379.
[http://dx.doi.org/10.1007/BF00435856] [PMID:  6803283] 
[106] 
Cachat, J.; Canavello, P.; Elegante, M.; Bartels, B.; Elkhayat, S.; Hart, P. Modeling stress and anxiety in zebrafish. Zebrafish Models of Neurobehavioral Research; Humana Press, 2011, pp. 211-222.
[107] 
Cachat, J.; Stewart, A.; Grossman, L.; Gaikwad, S.; Kadri, F.; Chung, K.M.; Wu, N.; Wong, K.; Roy, S.; Suciu, C.; Goodspeed, J.; Elegante, M.; Bartels, B.; Elkhayat, S.; Tien, D.; Tan, J.; Denmark, A.; Gilder, T.; Kyzar, E.; Dileo, J.; Frank, K.; Chang, K.; Utterback, E.; Hart, P.; Kalueff, A.V. Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat. Protoc.,  2010, 5(11), 1786-1799.
[http://dx.doi.org/10.1038/nprot.2010.140] [PMID:  21030954] 
[108] 
Egan, R.J.; Bergner, C.L.; Hart, P.C.; Cachat, J.M.; Canavello, P.R.; Elegante, M.F.; Elkhayat, S.I.; Bartels, B.K.; Tien, A.K.; Tien, D.H.; Mohnot, S.; Beeson, E.; Glasgow, E.; Amri, H.; Zukowska, Z.; Kalueff, A.V. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav. Brain Res.,  2009, 205(1), 38-44.
[http://dx.doi.org/10.1016/j.bbr.2009.06.022] [PMID:  19540270] 
[109] 
Sackerman, J.; Donegan, J.J.; Cunningham, C.S.; Nguyen, N.N.; Lawless, K.; Long, A.; Benno, R.H.; Gould, G.G. Zebrafish behavior in novel environments: effects of acute exposure to anxiolytic compounds and choice of Danio rerio line. Int. J. Comp. Psychol.,  2010, 23(1), 43-61.
[PMID:  20523756] 
[110] 
Mathur, P.; Guo, S. Differences of acute versus chronic ethanol exposure on anxiety-like behavioral responses in zebrafish. Behav. Brain Res.,  2011, 219(2), 234-239.
[http://dx.doi.org/10.1016/j.bbr.2011.01.019] [PMID:  21255611] 
[111] 
Boa-Amponsem, O.; Zhang, C.; Burton, D.; Williams, K.P.; Cole, G.J. Ethanol and cannabinoids regulate zebrafish GABAergic neuron development and behavior in a sonic hedgehog and fibroblast growth factor-dependent mechanism. Alcohol. Clin. Exp. Res.,  2020, 44(7), 1366-1377.
[http://dx.doi.org/10.1111/acer.14383] [PMID:  32472575] 
[112] 
Baiamonte, M.; Parker, M.O.; Vinson, G.P.; Brennan, C.H. Sustained effects of developmental exposure to ethanol on zebrafish anxiety-like behavior. PLoS One,  2016, 11(2) ,e0148425
[http://dx.doi.org/10.1371/journal.pone.0148425] [PMID:  26862749] 
[113] 
da Silva Chaves, S.N.; Dutra Costa, B.P.; Vidal, G.G.C.; Lima-Maximino, M.; Pacheco, R.E.; Maximino, C. NOS-2 participates in the behavioral effects of ethanol withdrawal in zebrafish. Neurosci. Lett.,  2020, 728 ,134952
[http://dx.doi.org/10.1016/j.neulet.2020.134952] [PMID:  32283112] 
[114] 
Clayman, C.L.; Malloy, E.J.; Kearns, D.N.; Connaughton, V.P. Differential behavioral effects of ethanol pre-exposure in male and female zebrafish (Danio rerio). Behav. Brain Res.,  2017, 335, 174-184.
[http://dx.doi.org/10.1016/j.bbr.2017.08.007] [PMID:  28797598] 
[115] 
Wong, K.; Elegante, M.; Bartels, B.; Elkhayat, S.; Tien, D.; Roy, S.; Goodspeed, J.; Suciu, C.; Tan, J.; Grimes, C.; Chung, A.; Rosenberg, M.; Gaikwad, S.; Denmark, A.; Jackson, A.; Kadri, F.; Chung, K.M.; Stewart, A.; Gilder, T.; Beeson, E.; Zapolsky, I.; Wu, N.; Cachat, J.; Kalueff, A.V. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav. Brain Res.,  2010, 208(2), 450-457.
[http://dx.doi.org/10.1016/j.bbr.2009.12.023] [PMID:  20035794] 
[116] 
Novier, A.; Ornelas, L.C.; Diaz-Granados, J.L.; Matthews, D.B. Differences in behavioral responding in adult and aged rats following chronic ethanol exposure. Alcohol. Clin. Exp. Res.,  2016, 40(7), 1462-1472.
[http://dx.doi.org/10.1111/acer.13098] [PMID:  27218698] 
[117] 
Younis, R.M.; Wolstenholme, J.T.; Bagdas, D.; Bettinger, J.C.; Miles, M.F.; Damaj, M.I. Adolescent but not adult ethanol binge drinking modulates ethanol behavioral effects in mice later in life. Pharmacol. Biochem. Behav.,  2019, 184 ,172740
[http://dx.doi.org/10.1016/j.pbb.2019.172740] [PMID:  31326461] 
[118] 
Blaser, R.E.; Chadwick, L.; McGinnis, G.C. Behavioral measures of anxiety in zebrafish (Danio rerio). Behav. Brain Res.,  2010, 208(1), 56-62.
[http://dx.doi.org/10.1016/j.bbr.2009.11.009] [PMID:  19896505] 
[119] 
Maximino, C.; Marques de Brito, T.; Dias, C.A.; Gouveia, A., Jr; Morato, S. Scototaxis as anxiety-like behavior in fish. Nat. Protoc.,  2010, 5(2), 209-216.
[http://dx.doi.org/10.1038/nprot.2009.225] [PMID:  20134420] 
[120] 
Maximino, C.; da Silva, A.W.; Gouveia, A., Jr; Herculano, A.M. Pharmacological analysis of zebrafish (Danio rerio) scototaxis. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2011, 35(2), 624-631.
[http://dx.doi.org/10.1016/j.pnpbp.2011.01.006] [PMID:  21237231] 
[121] 
Holcombe, A.; Howorko, A.; Powell, R.A.; Schalomon, M.; Hamilton, T.J. Reversed scototaxis during withdrawal after daily-moderate, but not weekly-binge, administration of ethanol in zebrafish. PLoS One,  2013, 8(5) ,e63319
[http://dx.doi.org/10.1371/journal.pone.0063319] [PMID:  23675478] 
[122] 
Desikan, A.; Wills, D.N.; Ehlers, C.L. Ontogeny and adolescent alcohol exposure in Wistar rats: open field conflict, light/dark box and forced swim test. Pharmacol. Biochem. Behav.,  2014, 122, 279-285.
[http://dx.doi.org/10.1016/j.pbb.2014.04.011] [PMID:  24785000] 
[123] 
Fleming, W.; Jones, Q.; Chandra, U.; Saini, A.; Walker, D.; Francis, R.; Ocampo, G.; Kuhn, C. Withdrawal from brief repeated alcohol treatment in adolescent and adult male and female rats. Alcohol. Clin. Exp. Res.,  2019, 43(2), 204-211.
[http://dx.doi.org/10.1111/acer.13936] [PMID:  30566247] 
[124] 
Echevarria, D.; Jammack, C.; Pratt, D.; Hosemann, J. A novel behavioral test battery to assess global drug effects using the zebrafish. Int. J. Comp. Psychol.,  2008, 21, 19-34.
[125] 
Maaswinkel, H.; Le, X.; He, L.; Zhu, L.; Weng, W. Dissociating the effects of habituation, black walls, buspirone and ethanol on anxiety-like behavioral responses in shoaling zebrafish. A 3D approach to social behavior. Pharmacol. Biochem. Behav.,  2013, 108, 16-27.
[http://dx.doi.org/10.1016/j.pbb.2013.04.009] [PMID:  23603028] 
[126] 
Hughes, R.N.; Hancock, N.J. Strain-dependent effects of acute caffeine on anxiety-related behavior in PVG/c, Long-Evans and Wistar rats. Pharmacol. Biochem. Behav.,  2016, 140, 51-61.
[http://dx.doi.org/10.1016/j.pbb.2015.11.005] [PMID:  26577750] 
[127] 
Anderson, N.L.; Hughes, R.N. Increased emotional reactivity in rats following exposure to caffeine during adolescence. Neurotoxicol. Teratol.,  2008, 30(3), 195-201.
[http://dx.doi.org/10.1016/j.ntt.2008.02.002] [PMID:  18378115] 
[128] 
Santucci, A.C.; Cortes, C.; Bettica, A.; Cortes, F. Chronic ethanol consumption in rats produces residual increases in anxiety 4 months after withdrawal. Behav. Brain Res.,  2008, 188(1), 24-31.
[http://dx.doi.org/10.1016/j.bbr.2007.10.009] [PMID:  18061285] 
[129] 
Saverino, C.; Gerlai, R. The social zebrafish: behavioral responses to conspecific, heterospecific, and computer animated fish. Behav. Brain Res.,  2008, 191(1), 77-87.
[http://dx.doi.org/10.1016/j.bbr.2008.03.013] [PMID:  18423643] 
[130] 
Al-Imari, L.; Gerlai, R. Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio). Behav. Brain Res.,  2008, 189(1), 216-219.
[http://dx.doi.org/10.1016/j.bbr.2007.12.007] [PMID:  18243353] 
[131] 
Kurta, A.; Palestis, B.G. Effects of ethanol on the shoaling behavior of zebrafish (Danio rerio). Dose Response,  2010, 8(4), 527-533.
[http://dx.doi.org/10.2203/dose-response.10-008.Palestis] [PMID:  21191489] 
[132] 
Miller, N.; Greene, K.; Dydinski, A.; Gerlai, R. Effects of nicotine and alcohol on zebrafish (Danio rerio) shoaling. Behav. Brain Res.,  2013, 240, 192-196.
[http://dx.doi.org/10.1016/j.bbr.2012.11.033] [PMID:  23219966] 
[133] 
Gerlai, R. Zebra fish: an uncharted behavior genetic model. Behav. Genet.,  2003, 33(5), 461-468.
[http://dx.doi.org/10.1023/A:1025762314250] [PMID:  14574124] 
[134] 
Ariyasiri, K.; Choi, T-I.; Kim, O-H.; Hong, T.I.; Gerlai, R.; Kim, C-H. Pharmacological (ethanol) and mutation (sam2 KO) induced impairment of novelty preference in zebrafish quantified using a new three-chamber social choice task. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2019, 88, 53-65.
[http://dx.doi.org/10.1016/j.pnpbp.2018.06.009] [PMID:  29958859] 
[135] 
Gregson, J.; Burt De Perera, T. Shoaling in eyed and blind morphs of the characin Astyanax fasciatus under light and dark conditions. J. Fish Biol.,  2007, 70, 1615-1619.
[http://dx.doi.org/10.1111/j.1095-8649.2007.01430.x] 
[136] 
Partridge, B.; Pitcher, T. The sensory basis of fish schools: relative roles of lateral line and vision. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol.,  1980, 135, 315-325.
[http://dx.doi.org/10.1007/BF00657647] 
[137] 
Gerlai, R. Antipredatory behavior of zebrafish: adaptive function and a tool for translational research. Evol. Psychol.,  2013, 11(3), 591-605.
[http://dx.doi.org/10.1177/147470491301100308] [PMID:  23864295] 
[138] 
Fernandes, Y.; Gerlai, R. Long-term behavioral changes in response to early developmental exposure to ethanol in zebrafish. Alcohol. Clin. Exp. Res.,  2009, 33(4), 601-609.
[http://dx.doi.org/10.1111/j.1530-0277.2008.00874.x] [PMID:  19183139] 
[139] 
Buske, C.; Gerlai, R. Early embryonic ethanol exposure impairs shoaling and the dopaminergic and serotoninergic systems in adult zebrafish. Neurotoxicol. Teratol.,  2011, 33(6), 698-707.
[http://dx.doi.org/10.1016/j.ntt.2011.05.009] [PMID:  21658445] 
[140] 
Varlinskaya, E.I.; Hosová, D.; Towner, T.; Werner, D.F.; Spear, L.P. Effects of chronic intermittent ethanol exposure during early and late adolescence on anxiety-like behaviors and behavioral flexibility in adulthood. Behav. Brain Res.,  2020, 378 ,112292
[http://dx.doi.org/10.1016/j.bbr.2019.112292] [PMID:  31626849] 
[141] 
Varlinskaya, E.I.; Spear, L.P. Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol. Clin. Exp. Res.,  2002, 26(10), 1502-1511.
[http://dx.doi.org/10.1111/j.1530-0277.2002.tb02449.x] [PMID:  12394283] 
[142] 
Ferré, S. Mechanisms of the psychostimulant effects of caffeine: implications for substance use disorders. Psychopharmacology (Berl.),  2016, 233(10), 1963-1979.
[http://dx.doi.org/10.1007/s00213-016-4212-2] [PMID:  26786412] 
[143] 
Gutiérrez, H.C.; Vacca, I.; Schoenmacker, G.; Cleal, M.; Tochwin, A.; O’Connor, B.; Young, A.M.J.; Vasquez, A.A.; Winter, M.J.; Parker, M.O.; Norton, W.H.J. Screening for drugs to reduce zebrafish aggression identifies caffeine and sildenafil. Eur. Neuropsychopharmacol.,  2020, 30, 17-29.
[http://dx.doi.org/10.1016/j.euroneuro.2019.10.005] [PMID:  31679888] 
[144] 
Boehmler, W.; Petko, J.; Woll, M.; Frey, C.; Thisse, B.; Thisse, C.; Canfield, V.A.; Levenson, R. Identification of zebrafish A2 adenosine receptors and expression in developing embryos. Gene Expr. Patterns,  2009, 9(3), 144-151.
[http://dx.doi.org/10.1016/j.gep.2008.11.006] [PMID:  19070682] 
[145] 
Nikodijević, O.; Jacobson, K.A.; Daly, J.W. Locomotor activity in mice during chronic treatment with caffeine and withdrawal.Pharmacol. Biochem. Behav.,  1993, 44(1), 199-216. a
[http://dx.doi.org/10.1016/0091-3057(93)90299-9] [PMID: 7679219] 
[146] 
Daly, J.W.; Shi, D.; Wong, V.; Nikodijevic, O. Chronic effects of ethanol on central adenosine function of mice. Brain Res.,  1994, 650(1), 153-156.
[http://dx.doi.org/10.1016/0006-8993(94)90219-4] [PMID:  7953667] 
[147] 
Fredholm, B.B.; Bättig, K.; Holmén, J.; Nehlig, A.; Zvartau, E.E. Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol. Rev.,  1999, 51(1), 83-133.
[PMID:  10049999] 
[148] 
Jain, N.S.; Hirani, K.; Chopde, C.T. Reversal of caffeine-induced anxiety by neurosteroid 3-alpha-hydroxy-5-alpha-pregnane-20-one in rats. Neuropharmacology,  2005, 48(5), 627-638.
[http://dx.doi.org/10.1016/j.neuropharm.2004.11.016] [PMID:  15814098] 
[149] 
Gupta, P.; Khobragade, S.; Shingatgeri, V.; Rajaram, S. Assessment of locomotion behavior in adult zebrafish after acute exposure to different pharmacological reference compounds. Drug Develop Ther.,  2014, 5, 127.
[http://dx.doi.org/10.4103/2394-2002.139626] 
[150] 
Ladu, F.; Mwaffo, V.; Li, J.; Macrì, S.; Porfiri, M. Acute caffeine administration affects zebrafish response to a robotic stimulus. Behav. Brain Res.,  2015, 289, 48-54.
[http://dx.doi.org/10.1016/j.bbr.2015.04.020] [PMID:  25907748] 
[151] 
Richendrfer, H.; Pelkowski, S.D.; Colwill, R.M.; Creton, R. On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav. Brain Res.,  2012, 228(1), 99-106.
[http://dx.doi.org/10.1016/j.bbr.2011.11.041] [PMID:  22155488] 
[152] 
de Carvalho, T.S.; Cardoso, P.B.; Santos-Silva, M.; Lima-Bastos, S.; Luz, W.L.; Assad, N.; Kauffmann, N.; Passos, A.; Brasil, A.; Bahia, C.P.; Moraes, S.; Gouveia, A., Jr; de Jesus Oliveira, B.E.; Oliveira, K.R.M.H.; Herculano, A.M. Oxidative stress mediates anxiety-like behavior induced by high caffeine intake in zebrafish: protective effect of alpha-tocopherol. Oxid. Med. Cell. Longev.,  2019, 2019 ,8419810
[http://dx.doi.org/10.1155/2019/8419810] [PMID:  31772712] 
[153] 
Pohanka, M.; Dobes, P. Caffeine inhibits acetylcholinesterase, but not butyrylcholinesterase. Int. J. Mol. Sci.,  2013, 14(5), 9873-9882.
[http://dx.doi.org/10.3390/ijms14059873] [PMID:  23698772] 
[154] 
Ferré, S. An update on the mechanisms of the psychostimulant effects of caffeine. J. Neurochem.,  2008, 105(4), 1067-1079.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05196.x] [PMID:  18088379] 
[155] 
Ferré, S.; O’Brien, M.C. Alcohol and caffeine: the perfect storm. J. Caffeine Res.,  2011, 1(3), 153-162.
[http://dx.doi.org/10.1089/jcr.2011.0017] [PMID:  24761263] 
[156] 
Acquas, E.; Tanda, G.; Di Chiara, G. Differential effects of caffeine on dopamine and acetylcholine transmission in brain areas of drug-naive and caffeine-pretreated rats. Neuropsychopharmacology,  2002, 27(2), 182-193.
[http://dx.doi.org/10.1016/S0893-133X(02)00290-7] [PMID:  12093592] 
[157] 
Santos, L.; Ruiz-Oliveira, J.; Silva, P.; Luchiari, A. Caffeine dose-response relationship and behavioral screening in zebrafish.In: The Question of Caffeine,; , 2017. 
[http://dx.doi.org/10.5772/intechopen.68341] 
[158] 
Vada, S.; Goli, D.; Sharma, U.; Bose, A.; Mandal, S. Thorough investigation of epileptic behavioral characterization of caffeine in adult zebrafishes in correlation with drug brain concentration. Acta Ethol.,  2017, 20, 95-105.
[http://dx.doi.org/10.1007/s10211-017-0250-y] 
[159] 
Ruiz-Oliveira, J.; Silva, P.F.; Luchiari, A.C. Coffee time: Low caffeine dose promotes attention and focus in zebrafish. Learn. Behav.,  2019, 47(3), 227-233.
[http://dx.doi.org/10.3758/s13420-018-0369-3] [PMID:  30623296] 
[160] 
Angelucci, M.E.; Cesário, C.; Hiroi, R.H.; Rosalen, P.L.; Da Cunha, C. Effects of caffeine on learning and memory in rats tested in the Morris water maze. Braz. J. Med. Biol. Res.,  2002, 35(10), 1201-1208.
[http://dx.doi.org/10.1590/S0100-879X2002001000013] [PMID:  12424493] 
[161] 
Baldwin, H.A.; File, S.E. Caffeine-induced anxiogenesis: the role of adenosine, benzodiazepine and noradrenergic receptors. Pharmacol. Biochem. Behav.,  1989, 32(1), 181-186.
[http://dx.doi.org/10.1016/0091-3057(89)90230-X] [PMID:  2543990] 
[162] 
Alia, A.O.; Petrunich-Rutherford, M.L. Anxiety-like behavior and whole-body cortisol responses to components of energy drinks in zebrafish (Danio rerio). PeerJ,  2019, 7 ,e7546
[http://dx.doi.org/10.7717/peerj.7546] [PMID:  31497403] 
[163] 
Cauli, O.; Morelli, M. Caffeine and the dopaminergic system. Behav. Pharmacol.,  2005, 16(2), 63-77.
[http://dx.doi.org/10.1097/00008877-200503000-00001] [PMID:  15767841] 
[164] 
Solinas, M.; Ferré, S.; You, Z.B.; Karcz-Kubicha, M.; Popoli, P.; Goldberg, S.R. Caffeine induces dopamine and glutamate release in the shell of the nucleus accumbens. J. Neurosci.,  2002, 22(15), 6321-6324.
[http://dx.doi.org/10.1523/JNEUROSCI.22-15-06321.2002] [PMID:  12151508] 
[165] 
Hughes, R.N.; Hancock, N.J.; Henwood, G.A.; Rapley, S.A. Evidence for anxiolytic effects of acute caffeine on anxiety-related behavior in male and female rats tested with and without bright light. Behav. Brain Res.,  2014, 271, 7-15.
[http://dx.doi.org/10.1016/j.bbr.2014.05.038] [PMID:  24875772] 
[166] 
Burbano-L, D.A.; Porfiri, M. Data-driven modeling of zebrafish behavioral response to acute caffeine administration. J. Theor. Biol.,  2020, 485 ,110054
[http://dx.doi.org/10.1016/j.jtbi.2019.110054] [PMID:  31634449] 
[167] 
Chen, Y.H.; Huang, Y.H.; Wen, C.C.; Wang, Y.H.; Chen, W.L.; Chen, L.C.; Tsay, H.J. Movement disorder and neuromuscular change in zebrafish embryos after exposure to caffeine. Neurotoxicol. Teratol.,  2008, 30(5), 440-447.
[http://dx.doi.org/10.1016/j.ntt.2008.04.003] [PMID:  18508234] 
[168] 
El Yacoubi, M.; Ledent, C.; Ménard, J-F.; Parmentier, M.; Costentin, J.; Vaugeois, J-M. 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), 1465-1473. a
[http://dx.doi.org/10.1038/sj.bjp.0703170] [PMID: 10742303] 
[169] 
Zhang, Q.; Yu, Y.P.; Ye, Y.L.; Zhang, J.T.; Zhang, W.P.; Wei, E.Q. Spatiotemporal properties of locomotor activity after administration of central nervous stimulants and sedatives in mice. Pharmacol. Biochem. Behav.,  2011, 97(3), 577-585.
[http://dx.doi.org/10.1016/j.pbb.2010.09.011] [PMID:  20863845] 
[170] 
Buckholtz, N.S.; Middaugh, L.D. Effects of caffeine and L-phenylisopropyladenosine on locomotor activity of mice. Pharmacol. Biochem. Behav.,  1987, 28(2), 179-185.
[http://dx.doi.org/10.1016/0091-3057(87)90211-5] [PMID:  3685054] 
[171] 
Hsu, C.W.; Chen, C.Y.; Wang, C.S.; Chiu, T.H. Caffeine and a selective adenosine A2A receptor antagonist induce reward and sensitization behavior associated with increased phospho-Thr75-DARPP-32 in mice. Psychopharmacology (Berl.),  2009, 204(2), 313-325.
[http://dx.doi.org/10.1007/s00213-009-1461-3] [PMID:  19169672] 
[172] 
Kaplan, G.B.; Greenblatt, D.J.; Leduc, B.W.; Thompson, M.L.; Shader, R.I. Relationship of plasma and brain concentrations of caffeine and metabolites to benzodiazepine receptor binding and locomotor activity. J. Pharmacol. Exp. Ther.,  1989, 248(3), 1078-1083.
[PMID:  2539455] 
[173] 
Marin, M.T.; Zancheta, R.; Paro, A.H.; Possi, A.P.; Cruz, F.C.; Planeta, C.S. Comparison of caffeine-induced locomotor activity between adolescent and adult rats. Eur. J. Pharmacol.,  2011, 660(2-3), 363-367.
[http://dx.doi.org/10.1016/j.ejphar.2011.03.052] [PMID:  21497160] 
[174] 
Hughes, R.N.; Hancock, N.J. Effects of acute caffeine on anxiety-related behavior in rats chronically exposed to the drug, with some evidence of possible withdrawal-reversal. Behav. Brain Res.,  2017, 321, 87-98.
[http://dx.doi.org/10.1016/j.bbr.2016.12.019] [PMID:  28043898] 
[175] 
Raymond, J.; Chanin, S.; Michael Steward, A.; Kyzar, E.; Gaikwad, S.; Roth, A. Assessing habituation phenotypes in adult zebrafish: intra- and inter-trial habituation in the novel tank task; Zebrafish Protocols for Neurobehavioral Research, 2012, pp. 71-84.
[176] 
Ardais, A.P.; Borges, M.F.; Rocha, A.S.; Sallaberry, C.; Cunha, R.A.; Porciúncula, L.O. Caffeine triggers behavioral and neurochemical alterations in adolescent rats. Neuroscience,  2014, 270, 27-39.
[http://dx.doi.org/10.1016/j.neuroscience.2014.04.003] [PMID:  24726984] 
[177] 
Bhattacharya, S.K.; Satyan, K.S.; Chakrabarti, A. Anxiogenic action of caffeine: an experimental study in rats. J. Psychopharmacol.,  1997, 11(3), 219-224.
[http://dx.doi.org/10.1177/026988119701100304] [PMID:  9305413] 
[178] 
El Yacoubi, M.; Ledent, C.; Parmentier, M.; Costentin, J.; Vaugeois, J-M. .The anxiogenic-like effect of caffeine in two experimental	procedures measuring anxiety in the mouse is not shared by selective	A(2A) adenosine receptor antagonists. Psychopharmacology (Berl.), 2000, 148(2), 153-163. b
[http://dx.doi.org/10.1007/s002130050037] [PMID:  10663430] 
[179] 
Gulick, D.; Gould, T.J. Effects of ethanol and caffeine on behavior in C57BL/6 mice in the plus-maze discriminative avoidance task. Behav. Neurosci.,  2009, 123(6), 1271-1278.
[http://dx.doi.org/10.1037/a0017610] [PMID:  20001110] 
[180] 
Lopez-Cruz, L.; Pardo, M.; Salamone, J.D.; Correa, M. Comparison between high doses of caffeine and theophylline on motor and axiogenic effects in CD1 mice: studies of acute and chronic administration. Behav. Pharmacol.,  2011, 22, e1-e73.
[181] 
Maximino, C.; da Silva, A.W.; Araújo, J.; Lima, M.G.; Miranda, V.; Puty, B.; Benzecry, R.; Picanço-Diniz, D.L.; Gouveia, A., Jr; Oliveira, K.R.; Herculano, A.M. Fingerprinting of psychoactive drugs in zebrafish anxiety-like behaviors. PLoS One,  2014, 9(7) ,e103943
[http://dx.doi.org/10.1371/journal.pone.0103943] [PMID:  25079766] 
[182] 
Stewart, A.; Wu, N.; Cachat, J.; Hart, P.; Gaikwad, S.; Wong, K.; Utterback, E.; Gilder, T.; Kyzar, E.; Newman, A.; Carlos, D.; Chang, K.; Hook, M.; Rhymes, C.; Caffery, M.; Greenberg, M.; Zadina, J.; Kalueff, A.V. Pharmacological modulation of anxiety-like phenotypes in adult zebrafish behavioral models. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2011, 35(6), 1421-1431.
[http://dx.doi.org/10.1016/j.pnpbp.2010.11.035] [PMID:  21122812] 
[183] 
La-Vu, M.; Tobias, B.C.; Schuette, P.J.; Adhikari, A. To approach or to avoid: an introductory overview of teh study of anxiety using rodent assays. Front. Behav. Neurosci.,  2020, 14, 145.
[http://dx.doi.org/10.3389/fnbeh.2020.00145] [PMID:  33005134] 
[184] 
Enríquez-Castillo, A.; Alamilla, J.; Barral, J.; Gourbière, S.; Flores-Serrano, A.G.; Góngora-Alfaro, J.L.; Pineda, J.C. Differential effects of caffeine on the antidepressant-like effect of amitriptyline in female rat subpopulations with low and high immobility in the forced swimming test. Physiol. Behav.,  2008, 94(3), 501-509.
[http://dx.doi.org/10.1016/j.physbeh.2008.03.004] [PMID:  18436269] 
[185] 
Rosa, L.V.; Costa, F.V.; Canzian, J.; Borba, J.V.; Quadros, V.A.; Rosemberg, D.B. Three- and bi-dimensional analyses of the shoaling behavior in zebrafish: Influence of modulators of anxiety-like responses. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 102 ,109957
[http://dx.doi.org/10.1016/j.pnpbp.2020.109957] [PMID:  32360787] 
[186] 
Bailey, R.L.; Saldanha, L.G.; Dwyer, J.T.; Dwyer, J. Estimating caffeine intake from energy drinks and dietary supplements in the United States. Nutr. Rev.,  2014, 72(9-13)(Suppl. 1), 9-13.
[http://dx.doi.org/10.1111/nure.12138] [PMID:  25293539] 
[187] 
Seifert, S.M.; Schaechter, J.L.; Hershorin, E.R.; Lipshultz, S.E. Health effects of energy drinks on children, adolescents, and young adults. Pediatrics,  2011, 127(3), 511-528.
[http://dx.doi.org/10.1542/peds.2009-3592] [PMID:  21321035] 
[188] 
Franklin, K.M.; Hauser, S.R.; Bell, R.L.; Engleman, E.A. Caffeinated alcoholic beverages - an emerging trend in alcohol abuse. J. Addict. Res. Ther.,  2013(Suppl. 4), S4-S012.
[PMID:  25419478] 
[189] 
Griffiths, R.; Juliano, L.; Chausmer, A. Caffeine pharmacology and clinical effects. Principles of Addiction Med.,  2003, 3, 193-224.
[190] 
McKetin, R.; Coen, A.; Kaye, S. A comprehensive review of the effects of mixing caffeinated energy drinks with alcohol. Drug Alcohol Depend.,  2015, 151, 15-30.
[http://dx.doi.org/10.1016/j.drugalcdep.2015.01.047] [PMID:  25861944] 
[191] 
Peacock, A.; Pennay, A.; Droste, N.; Bruno, R.; Lubman, D.I. ‘High’ risk? A systematic review of the acute outcomes of mixing alcohol with energy drinks. Addiction,  2014, 109(10), 1612-1633.
[http://dx.doi.org/10.1111/add.12622] [PMID:  24846217] 
[192] 
Arria, A.M.; Caldeira, K.M.; Kasperski, S.J.; Vincent, K.B.; Griffiths, R.R.; O’Grady, K.E. Energy drink consumption and increased risk for alcohol dependence. Alcohol. Clin. Exp. Res.,  2011, 35(2), 365-375.
[http://dx.doi.org/10.1111/j.1530-0277.2010.01352.x] [PMID:  21073486] 
[193] 
O’Brien, M.C.; McCoy, T.P.; Rhodes, S.D.; Wagoner, A.; Wolfson, M. Caffeinated cocktails: energy drink consumption, high-risk drinking, and alcohol-related consequences among college students. Acad. Emerg. Med.,  2008, 15(5), 453-460.
[http://dx.doi.org/10.1111/j.1553-2712.2008.00085.x] [PMID:  18439201] 
[194] 
Thombs, D.; Rossheim, M.; Barnett, T.E.; Weiler, R.M.; Moorhouse, M.D.; Coleman, B.N. Is there a misplaced focus on AmED? Associations between caffeine mixers and bar patron intoxication. Drug Alcohol Depend.,  2011, 116(1-3), 31-36.
[http://dx.doi.org/10.1016/j.drugalcdep.2010.11.014] [PMID:  21177047] 
[195] 
Jones, S.C.; Barrie, L.; Berry, N. Why (not) alcohol energy drinks? A qualitative study with Australian university students. Drug Alcohol Rev.,  2012, 31(3), 281-287.
[http://dx.doi.org/10.1111/j.1465-3362.2011.00319.x] [PMID:  21605204] 
[196] 
Spinetta, M.J.; Woodlee, M.T.; Feinberg, L.M.; Stroud, C.; Schallert, K.; Cormack, L.K.; Schallert, T. Alcohol-induced retrograde memory impairment in rats: prevention by caffeine. Psychopharmacology (Berl.),  2008, 201(3), 361-371.
[http://dx.doi.org/10.1007/s00213-008-1294-5] [PMID:  18758756] 
[197] 
Dash, P.K.; Moore, A.N.; Moody, M.R.; Treadwell, R.; Felix, J.L.; Clifton, G.L. Post-trauma administration of caffeine plus ethanol reduces contusion volume and improves working memory in rats. J. Neurotrauma,  2004, 21(11), 1573-1583.
[http://dx.doi.org/10.1089/neu.2004.21.1573] [PMID:  15684650] 
[198] 
Pires, R.G.; Pereira, S.R.; Oliveira-Silva, I.F.; Franco, G.C.; Ribeiro, A.M. Cholinergic parameters and the retrieval of learned and re-learned spatial information: a study using a model of Wernicke-Korsakoff Syndrome. Behav. Brain Res.,  2005, 162(1), 11-21.
[http://dx.doi.org/10.1016/j.bbr.2005.02.032] [PMID:  15922063] 
[199] 
Pereira, S.R.; Menezes, G.A.; Franco, G.C.; Costa, A.E.; Ribeiro, A.M. Chronic ethanol consumption impairs spatial remote memory in rats but does not affect cortical cholinergic parameters. Pharmacol. Biochem. Behav.,  1998, 60(2), 305-311.
[http://dx.doi.org/10.1016/S0091-3057(97)00472-3] [PMID:  9632211] 
[200] 
Stancampiano, R.; Carta, M.; Cocco, S.; Curreli, R.; Rossetti, Z.L.; Fadda, F. Biphasic effects of ethanol on acetylcholine release in the rat prefrontal cortex. Brain Res.,  2004, 997(1), 128-132.
[http://dx.doi.org/10.1016/j.brainres.2003.09.078] [PMID:  14715158] 
[201] 
Santos, L.C.; Ruiz-Oliveira, J.; Oliveira, J.J.; Silva, P.F.; Luchiari, A.C. Irish coffee: Effects of alcohol and caffeine on object discrimination in zebrafish. Pharmacol. Biochem. Behav.,  2016, 143, 34-43.
[http://dx.doi.org/10.1016/j.pbb.2016.01.013] [PMID:  26850919] 
[202] 
Boison, D.; Chen, J-F.; Fredholm, B.B. Adenosine signaling and function in glial cells. Cell Death Differ.,  2010, 17(7), 1071-1082.
[http://dx.doi.org/10.1038/cdd.2009.131] [PMID:  19763139] 
[203] 
Brown, R.M.; Short, J.L. Adenosine A(2A) receptors and their role in drug addiction. J. Pharm. Pharmacol.,  2008, 60(11), 1409-1430.
[http://dx.doi.org/10.1211/jpp/60.11.0001] [PMID:  18957161] 
[204] 
Ruby, C.L.; Adams, C.A.; Knight, E.J.; Nam, H.W.; Choi, D-S. An essential role for adenosine signaling in alcohol abuse. Curr. Drug Abuse Rev.,  2010, 3(3), 163-174.
[http://dx.doi.org/10.2174/1874473711003030163] [PMID:  21054262] 
[205] 
Kaplan, G.B.; Bharmal, N.H.; Leite-Morris, K.A.; Adams, W.R. Role of adenosine A1 and A2A receptors in the alcohol withdrawal syndrome. Alcohol,  1999, 19(2), 157-162.
[http://dx.doi.org/10.1016/S0741-8329(99)00033-6] [PMID:  10548160] 
[206] 
Krauss, S.W.; Ghirnikar, R.B.; Diamond, I.; Gordon, A.S. Inhibition of adenosine uptake by ethanol is specific for one class of nucleoside transporters. Mol. Pharmacol.,  1993, 44(5), 1021-1026.
[PMID:  7902530] 
[207] 
Nagy, L.E.; Diamond, I.; Casso, D.J.; Franklin, C.; Gordon, A.S. Ethanol increases extracellular adenosine by inhibiting adenosine uptake via the nucleoside transporter. J. Biol. Chem.,  1990, 265(4), 1946-1951.
[http://dx.doi.org/10.1016/S0021-9258(19)39923-5] [PMID:  2298733] 
[208] 
Zhang, D.; Xiong, W.; Jackson, M.F.; Parkinson, F.E. Ethanol tolerance affects endogenous adenosine signaling in mouse hippocampus. J. Pharmacol. Exp. Ther.,  2016, 358(1), 31-38.
[http://dx.doi.org/10.1124/jpet.116.232231] [PMID:  27189965] 
[209] 
Lutte, A.H.; Majolo, J.H.; Da Silva, R.S. Inhibition of ecto-5′-nucleotidase and adenosine deaminase is able to reverse long-term behavioural effects of early ethanol exposure in zebrafish (Danio rerio). Sci. Rep.,  2020, 10(1), 17809.
[http://dx.doi.org/10.1038/s41598-020-74832-0] [PMID:  33082435] 
[210] 
Rico, E.P.; Rosemberg, D.B.; Berteli, J.F.A.; da Silveira Langoni, A.; Souto, A.A.; Bogo, M.R.; Bonan, C.D.; Souza, D.O. Adenosine deaminase activity and gene expression patterns are altered after chronic ethanol exposure in zebrafish brain. Neurotoxicol. Teratol.,  2018, 65, 14-18.
[http://dx.doi.org/10.1016/j.ntt.2017.11.001] [PMID:  29122710] 
[211] 
Rico, E.P.; Rosemberg, D.B. Langoni, Ada.S.; Souto, A.A.; Dias, R.D.; Bogo, M.R.; Bonan, C.D.; Souza, D.O. Chronic ethanol treatment alters purine nucleotide hydrolysis and nucleotidase gene expression pattern in zebrafish brain. Neurotoxicol.,  2011, 32(6), 871-878.
[http://dx.doi.org/10.1016/j.neuro.2011.05.010] [PMID:  21704070] 
[212] 
Carmichael, F.J.; Israel, Y.; Crawford, M.; Minhas, K.; Saldivia, V.; Sandrin, S.; Campisi, P.; Orrego, H. Central nervous system effects of acetate: contribution to the central effects of ethanol. J. Pharmacol. Exp. Ther.,  1991, 259(1), 403-408.
[PMID:  1920128] 
[213] 
Dohrman, D.P.; Diamond, I.; Gordon, A.S. The role of the neuromodulator adenosine in alcohol’s actions. Alcohol Health Res. World,  1997, 21(2), 136-143.
[PMID:  15704350] 
[214] 
Pechlivanova, D.; Tchekalarova, J.; Nikolov, R.; Yakimova, K. Dose-dependent effects of caffeine on behavior and thermoregulation in a chronic unpredictable stress model of depression in rats. Behav. Brain Res.,  2010, 209(2), 205-211.
[http://dx.doi.org/10.1016/j.bbr.2010.01.037] [PMID:  20122970] 
[215] 
Kuzmin, A.; Johansson, B.; Gimenez, L.; Ogren, S.O.; Fredholm, B.B. Combination of adenosine A1 and A2A receptor blocking agents induces caffeine-like locomotor stimulation in mice. Eur. Neuropsychopharmacol.,  2006, 16(2), 129-136.
[http://dx.doi.org/10.1016/j.euroneuro.2005.07.001] [PMID:  16054807] 
[216] 
Jain, N.; Kemp, N.; Adeyemo, O.; Buchanan, P.; Stone, T.W. Anxiolytic activity of adenosine receptor activation in mice. Br. J. Pharmacol.,  1995, 116(3), 2127-2133.
[http://dx.doi.org/10.1111/j.1476-5381.1995.tb16421.x] [PMID:  8640355] 
[217] 
Prediger, R.D.; Batista, L.C.; Takahashi, R.N. Adenosine A1 receptors modulate the anxiolytic-like effect of ethanol in the elevated plus-maze in mice. Eur. J. Pharmacol.,  2004, 499(1-2), 147-154.
[http://dx.doi.org/10.1016/j.ejphar.2004.07.106] [PMID:  15363961] 
[218] 
Giménez-Llort, L.; Fernández-Teruel, A.; Escorihuela, R.M.; Fredholm, B.B.; Tobeña, A.; Pekny, M.; Johansson, B. Mice lacking the adenosine A1 receptor are anxious and aggressive, but are normal learners with reduced muscle strength and survival rate. Eur. J. Neurosci.,  2002, 16(3), 547-550.
[http://dx.doi.org/10.1046/j.1460-9568.2002.02122.x] [PMID:  12193199] 
[219] 
Johansson, B.; Halldner, L.; Dunwiddie, T.V.; Masino, S.A.; Poelchen, W.; Giménez-Llort, L.; Escorihuela, R.M.; Fernández-Teruel, A.; Wiesenfeld-Hallin, Z.; Xu, X.J.; Hårdemark, A.; Betsholtz, C.; Herlenius, E.; Fredholm, B.B. Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc. Natl. Acad. Sci. USA,  2001, 98(16), 9407-9412.
[http://dx.doi.org/10.1073/pnas.161292398] [PMID:  11470917] 
[220] 
Lang, U.E.; Lang, F.; Richter, K.; Vallon, V.; Lipp, H.P.; Schnermann, J.; Wolfer, D.P. Emotional instability but intact spatial cognition in adenosine receptor 1 knock out mice. Behav. Brain Res.,  2003, 145(1-2), 179-188.
[http://dx.doi.org/10.1016/S0166-4328(03)00108-6] [PMID:  14529816] 
[221] 
Adams, C.L.; Cowen, M.S.; Short, J.L.; Lawrence, A.J. Combined antagonism of glutamate mGlu5 and adenosine A2A receptors interact to regulate alcohol-seeking in rats. Int. J. Neuropsychopharmacol.,  2008, 11(2), 229-241.
[http://dx.doi.org/10.1017/S1461145707007845] [PMID:  17517168] 
[222] 
Arolfo, M.P.; Yao, L.; Gordon, A.S.; Diamond, I.; Janak, P.H. Ethanol operant self-administration in rats is regulated by adenosine A2 receptors. Alcohol. Clin. Exp. Res.,  2004, 28(9), 1308-1316.
[http://dx.doi.org/10.1097/01.ALC.0000139821.38167.20] [PMID:  15365300] 
[223] 
Thorsell, A.; Johnson, J.; Heilig, M. Effect of the adenosine A2a receptor antagonist 3,7-dimethyl-propargylxanthine on anxiety-like and depression-like behavior and alcohol consumption in Wistar Rats. Alcohol. Clin. Exp. Res.,  2007, 31(8), 1302-1307.
[http://dx.doi.org/10.1111/j.1530-0277.2007.00425.x] [PMID:  17550371] 
[224] 
Micioni Di Bonaventura, M.V.; Cifani, C.; Lambertucci, C.; Volpini, R.; Cristalli, G.; Froldi, R.; Massi, M. Effects of A2A adenosine receptor blockade or stimulation on alcohol intake in alcohol-preferring rats. Psychopharmacology (Berl.),  2012, 219(4), 945-957.
[http://dx.doi.org/10.1007/s00213-011-2430-1] [PMID:  21833502] 
[225] 
Fredholm, B.B.; IJzerman, A.P.; Jacobson, K.A.; Klotz, K.N.; Linden, J. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev.,  2001, 53(4), 527-552.
[PMID:  11734617] 
[226] 
Ferre, S.; Ciruela, F.; Borycz, J.; Solinas, M.; Quarta, D.; Antoniou, K.; Quiroz, C.; Justinova, Z.; Lluis, C.; Franco, R.; Goldberg, S.R. Adenosine A1-A2A receptor heteromers: new targets for caffeine in the brain. Front. Biosci.,  2008, 13, 2391-2399.
[http://dx.doi.org/10.2741/2852] [PMID:  17981720] 
[227] 
Shook, B.C.; Jackson, P.F. Adenosine A2A receptor antagonists and Parkinson’s disease. ACS Chem. Neurosci.,  2011, 2(10), 555-567.
[http://dx.doi.org/10.1021/cn2000537] [PMID:  22860156] 
[228] 
Rezvani, A.H.; Sexton, H.G.; Johnson, J.; Wells, C.; Gordon, K.; Levin, E.D. Effects of caffeine on alcohol consumption and nicotine self-administration in rats. Alcohol. Clin. Exp. Res.,  2013, 37(9), 1609-1617.
[http://dx.doi.org/10.1111/acer.12127] [PMID:  23895206] 
[229] 
Collier, A.D.; Min, S.S.; Campbell, S.D.; Roberts, M.Y.; Camidge, K.; Leibowitz, S.F. Maternal ethanol consumption before paternal fertilization: Stimulation of hypocretin neurogenesis and ethanol intake in zebrafish offspring. Prog. Neuropsychopharmacol. Biol. Psychiatry,  2020, 96 ,109728
[http://dx.doi.org/10.1016/j.pnpbp.2019.109728] [PMID:  31394141] 
[230] 
Sterling, M.E.; Karatayev, O.; Chang, G.Q.; Algava, D.B.; Leibowitz, S.F. Model of voluntary ethanol intake in zebrafish: effect on behavior and hypothalamic orexigenic peptides. Brain Behav Res.,  2015, 278, 29-39.
[http://dx.doi.org/10.1016/j.bbr.2014.09.024] [PMID:  25257106] 
[231] 
Zheng, X.; Dai, W.; Chen, X.; Wang, K.; Zhang, W.; Liu, L.; Hou, J. Caffeine reduces hepatic lipid accumulation through regulation of lipogenesis and ER stress in zebrafish larvae. J. Biomed. Sci.,  2015, 22, 105.
[http://dx.doi.org/10.1186/s12929-015-0206-3] [PMID:  26572131] 
[232] 
SanMiguel, N.; López-Cruz, L.; Müller, C.E.; Salamone, J.D.; Correa, M. Caffeine modulates voluntary alcohol intake in mice depending on the access conditions: Involvement of adenosine receptors and the role of individual differences. Pharmacol. Biochem. Behav.,  2019, 186(172789) ,172789
[http://dx.doi.org/10.1016/j.pbb.2019.172789] [PMID:  31499144] 
[233] 
Dietze, M.A.; Kulkosky, P.J. Effects of caffeine and bombesin on ethanol and food intake. Life Sci.,  1991, 48(19), 1837-1844.
[http://dx.doi.org/10.1016/0024-3205(91)90239-8] [PMID:  2041457] 
[234] 
Hederra, A.; Aidunate, J.; Segovia-Riquelme, N.; Mardones, J. Effects of caffeine on the voluntary EtOH intake of rats.The effects of centrally active drugs on voluntary EtOH consumption.,  1975, 24, 9-13.
[235] 
de Carvalho, C.; da Cruz, J.; Takahashi, R. Prolonged exposure to caffeinated alcoholic solutions prevents the alcohol deprivation effect in rats. J. Caffeine Res.,  2012, 2, 83-89.
[http://dx.doi.org/10.1089/jcr.2012.0013] 
[236] 
Okhuarobo, A.; Igbe, I.; Yahaya, A.; Sule, Z. Effect of caffeine on alcohol consumption and alcohol-induced conditioned place preference in rodents. J. Basic Clin. Physiol. Pharmacol.,  2018, 30(1), 19-28.
[http://dx.doi.org/10.1515/jbcpp-2018-0068] [PMID:  30099411] 
[237] 
Kunin, D.; Gaskin, S.; Rogan, F.; Smith, B.R.; Amit, Z. Caffeine promotes ethanol drinking in rats. Examination using a limited-access free choice paradigm. Alcohol,  2000, 21(3), 271-277.
[http://dx.doi.org/10.1016/S0741-8329(00)00101-4] [PMID:  11091031] 
[238] 
Fritz, B.M.; Quoilin, C.; Kasten, C.R.; Smoker, M.; Boehm, S.L., II Concomitant caffeine increases binge consumption of ethanol in adolescent and adult mice, but produces additive motor stimulation only in adolescent animals. Alcohol. Clin. Exp. Res.,  2016, 40(6), 1351-1360.
[http://dx.doi.org/10.1111/acer.13089] [PMID:  27154344] 
[239] 
Collier, A. Anxiety-like behaviors and c-fos expression in adult zebrafish: effects of housing conditions, alcohol and caffeine; University of Southern Mississippi, 2017. 
[240] 
El Yacoubi, M.; Ledent, C.; Parmentier, M.; Costentin, J.; Vaugeois, J-M. Caffeine reduces hypnotic effects of alcohol through adenosine A2A receptor blockade. Neuropharmacology,  2003, 45(7), 977-985.
[http://dx.doi.org/10.1016/S0028-3908(03)00254-5] [PMID:  14573390] 
[241] 
Khor, Y.M.; Soga, T.; Parhar, I.S. Caffeine neuroprotects against dexamethasone-induced anxiety-like behaviour in the Zebrafish (Danio rerio). Gen. Comp. Endocrinol.,  2013, 181, 310-315.
[http://dx.doi.org/10.1016/j.ygcen.2012.09.021] [PMID:  23044054] 
[242] 
Clayman, C. The role of ethanol pre-exposure in ethanol-induced behavioral responses and reward pathways in zebrafish (Danio rerio); American University: Washington, DC, 2016. 
[243] 
Hughes, R.N. Adult anxiety-related behavior of rats following consumption during late adolescence of alcohol alone and in combination with caffeine. Alcohol,  2011, 45(4), 365-372.
[http://dx.doi.org/10.1016/j.alcohol.2010.10.006] [PMID:  21145693] 
[244] 
Fuxe, K.; Ferré, S.; Genedani, S.; Franco, R.; Agnati, L.F. Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function. Physiol. Behav.,  2007, 92(1-2), 210-217.
[http://dx.doi.org/10.1016/j.physbeh.2007.05.034] [PMID:  17572452] 
[245] 
Boeck, C.R.; Marques, V.B.; Valvassori, S.S.; Constantino, L.C.; Rosa, D.V.; Lima, F.F.; Romano-Silva, M.A.; Quevedo, J. Early long-term exposure with caffeine induces cross-sensitization to methylphenidate with involvement of DARPP-32 in adulthood of rats. Neurochem. Int.,  2009, 55(5), 318-322.
[http://dx.doi.org/10.1016/j.neuint.2009.03.015] [PMID:  19576520] 
[246] 
Capiotti, K.M.; Menezes, F.P.; Nazario, L.R.; Pohlmann, J.B.; de Oliveira, G.M.; Fazenda, L.; Bogo, M.R.; Bonan, C.D.; Da Silva, R.S. Early exposure to caffeine affects gene expression of adenosine receptors, DARPP-32 and BDNF without affecting sensibility and morphology of developing zebrafish (Danio rerio). Neurotoxicol. Teratol.,  2011, 33(6), 680-685.
[http://dx.doi.org/10.1016/j.ntt.2011.08.010] [PMID:  21914471] 
[247] 
López-Cruz, L.; Salamone, J.D.; Correa, M. The impact of caffeine on the behavioral effects of ethanol related to abuse and addiction: a review of animal studies. J. Caffeine Res.,  2013, 3(1), 9-21.
[http://dx.doi.org/10.1089/jcr.2013.0003] [PMID:  24761272] 
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DOI https://dx.doi.org/10.2174/1570159X19666211111142027	Print ISSN 1570-159X
Publisher Name Bentham Science Publisher	Online ISSN 1875-6190
Current Neuropharmacology

Neurochemical and Behavioral Consequences of Ethanol and/or Caffeine Exposure: Effects in Zebrafish and Rodents

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