Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Systematic Review Article

Contributions of Zebrafish Studies to the Behavioural Consequences of Early Alcohol Exposure: A Systematic Review

Author(s): Flavia Gheller Schaidhauer, Higor Arruda Caetano , Guilherme Pietro da Silva and Rosane Souza da Silva *

Volume 20, Issue 3, 2022

Page: [579 - 593] Pages: 15

DOI: 10.2174/1570159X19666210428114317

Price: $65

Abstract

Background: The consequences of mild to severe exposure to alcohol during brain development is still a matter of debate and scientific investigation. The long-term behavioural effects of ethanol exposure have been related to impaired social skills and cognition. Zebrafish have become a suitable animal model to investigate the effects of early ethanol exposure because it is very feasible to promote drug delivery during early development.

Objective: The goal of the current report is to review existing behavioural studies addressing the impact of early alcohol exposure using zebrafish to determine whether these models resemble the behavioural effects of early alcohol exposure in humans.

Methods: A comprehensive search of biomedical databases was performed using the operation order: “ZEBRAFISH AND BEHAV* AND (ETHANOL OR ALCOHOL)”. The eligibility of studies was determined using the PICOS strategy, contemplating the population as zebrafish, intervention as exposure to ethanol, comparison with a non-exposed control animal, and outcomes as behavioural parameters.

Results: The systematic search revealed 29 scientific articles as eligible. The zebrafish is presented as a versatile animal model that is useful to study FASD short and long-term behaviour impairments, such as anxiety, impaired sociability, aggressiveness, learning problems, memory impairment, seizure susceptibility, sleep disorders, motivational problems, and addiction.

Conclusion: This systematic review further promotes the use of zebrafish as a model system to study the pathophysiological and behavioural consequences of early alcohol exposure (PROSPERO CRD42020215072).

Keywords: Foetal alcohol syndrome, ethanol, neurodevelopment, animal model, long-term effects, cognition, behavioural teratology.

« Previous Next »
Graphical Abstract

[1]
Hoyme, H.E.; May, P.A.; Kalberg, W.O.; Kodituwakku, P.; Gossage, J.P.; Trujillo, P.M.; Buckley, D.G.; Miller, J.H.; Aragon, A.S.; Khaole, N.; Viljoen, D.L.; Jones, K.L.; Robinson, L.K. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: Clarification of the 1996 institute of medicine criteria. Pediatrics, 2005, 115(1), 39-47.
[http://dx.doi.org/10.1542/peds.2004-0259] [PMID: 15629980]
[2]
Hoyme, H.E.; Kalberg, W.O.; Elliott, A.J.; Blankenship, J.; Buckley, D.; Marais, A.S.; Manning, M.A.; Robinson, L.K.; Adam, M.P.; Abdul-Rahman, O.; Jewett, T.; Coles, C.D.; Chambers, C.; Jones, K.L.; Adnams, C.M.; Shah, P.E.; Riley, E.P.; Charness, M.E.; Warren, K.R.; May, P.A. Updated clinical guidelines for diagnosing fetal alcohol spectrum disorders. Pediatrics, 2016, 138(2)e20154256
[http://dx.doi.org/10.1542/peds.2015-4256] [PMID: 27464676]
[3]
Lange, S.; Probst, C.; Gmel, G.; Rehm, J.; Burd, L.; Popova, S. Global prevalence of fetal alcohol spectrum disorder among children and youth: A systematic review and meta-analysis. JAMA Pediatr., 2017, 171(10), 948-956.
[http://dx.doi.org/10.1001/jamapediatrics.2017.1919] [PMID: 28828483]
[4]
Urban, M.F.; Olivier, L.; Viljoen, D.; Lombard, C.; Louw, J.G.; Drotsky, L.M.; Temmerman, M.; Chersich, M.F. Prevalence of fetal alcohol syndrome in a South African city with a predominantly Black African population. Alcohol. Clin. Exp. Res., 2015, 39(6), 1016-1026.
[http://dx.doi.org/10.1111/acer.12726] [PMID: 25941030]
[5]
Alvik, A.; Aalen, O.O.; Lindemann, R. Early fetal binge alcohol exposure predicts high behavioral symptom scores in 5.5-year-old children. Alcohol. Clin. Exp. Res., 2013, 37(11), 1954-1962.
[http://dx.doi.org/10.1111/acer.12182] [PMID: 23888929]
[6]
Maier, S.E.; West, J.R. Drinking patterns and alcohol-related birth defects. Alcohol Res. Health, 2001, 25(3), 168-174.
[PMID: 11810954]
[7]
Chasnoff, I.J.; Wells, A.M.; King, L. Misdiagnosis and missed diagnoses in foster and adopted children with prenatal alcohol exposure. Pediatrics, 2015, 135(2), 264-270.
[http://dx.doi.org/10.1542/peds.2014-2171] [PMID: 25583914]
[8]
Vaurio, L.; Riley, E.P.; Mattson, S.N. Differences in executive functioning in children with heavy prenatal alcohol exposure or attention-deficit/hyperactivity disorder. J. Int. Neuropsychol. Soc., 2008, 14(1), 119-129.
[http://dx.doi.org/10.1017/S1355617708080144] [PMID: 18078538]
[9]
Lucas, B.R.; Latimer, J.; Pinto, R.Z.; Ferreira, M.L.; Doney, R.; Lau, M.; Jones, T.; Dries, D.; Elliott, E.J. Gross motor deficits in children prenatally exposed to alcohol: A meta-analysis. Pediatrics, 2014, 134(1), e192-e209.
[http://dx.doi.org/10.1542/peds.2013-3733] [PMID: 24913787]
[10]
Inkelis, S.M.; Thomas, J.D. Sleep in infants and children with prenatal alcohol exposure. Alcohol. Clin. Exp. Res., 2018.
[http://dx.doi.org/10.1111/acer.13803] [PMID: 29852534]
[11]
Lee, K.T.; Mattson, S.N.; Riley, E.P. Classifying children with heavy prenatal alcohol exposure using measures of attention. J. Int. Neuropsychol. Soc., 2004, 10(2), 271-277.
[http://dx.doi.org/10.1017/S1355617704102142] [PMID: 15012847]
[12]
McGee, C.L.; Bjorkquist, O.A.; Riley, E.P.; Mattson, S.N. Impaired language performance in young children with heavy prenatal alcohol exposure. Neurotoxicol. Teratol., 2009, 31(2), 71-75.
[http://dx.doi.org/10.1016/j.ntt.2008.09.004] [PMID: 18938239]
[13]
Kingdon, D.; Cardoso, C.; McGrath, J.J. Research Review: Executive function deficits in fetal alcohol spectrum disorders and attention-deficit/hyperactivity disorder - A meta-analysis. J. Child Psychol. Psychiatry, 2016, 57(2), 116-131.
[http://dx.doi.org/10.1111/jcpp.12451] [PMID: 26251262]
[14]
Crocker, N.; Vaurio, L.; Riley, E.P.; Mattson, S.N. Comparison of adaptive behavior in children with heavy prenatal alcohol exposure or attention-deficit/hyperactivity disorder. Alcohol. Clin. Exp. Res., 2009, 33(11), 2015-2023.
[http://dx.doi.org/10.1111/j.1530-0277.2009.01040.x] [PMID: 19719794]
[15]
Fagerlund, Å.; Autti-Rämö, I.; Kalland, M.; Santtila, P.; Hoyme, H.E.; Mattson, S.N.; Korkman, M. Adaptive behaviour in children and adolescents with foetal alcohol spectrum disorders: A comparison with specific learning disability and typical development. Eur. Child Adolesc. Psychiatry, 2012, 21(4), 221-231.
[http://dx.doi.org/10.1007/s00787-012-0256-y] [PMID: 22358422]
[16]
Streissguth, A.P.; Bookstein, F.L.; Barr, H.M.; Sampson, P.D.; O’Malley, K.; Young, J.K. Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. J. Dev. Behav. Pediatr., 2004, 25(4), 228-238.
[http://dx.doi.org/10.1097/00004703-200408000-00002] [PMID: 15308923]
[17]
Coons, K. Determinants of drinking during pregnancy and lifespan outcomes for individuals with fetal alcohol spectrum disorder. J. Dev. Disabil., 2013, 19(3), 15-29.
[18]
Mattson, S.N.; Crocker, N.; Nguyen, T.T. Fetal alcohol spectrum disorders: neuropsychological and behavioral features. Neuropsychol. Rev., 2011, 21(2), 81-101.
[http://dx.doi.org/10.1007/s11065-011-9167-9] [PMID: 21503685]
[19]
Christoffersen, M.N.; Soothill, K. The long-term consequences of parental alcohol abuse: A cohort study of children in Denmark. J. Subst. Abuse Treat., 2003, 25(2), 107-116.
[http://dx.doi.org/10.1016/S0740-5472(03)00116-8] [PMID: 14629993]
[20]
Jones, K.L. The effects of alcohol on fetal development. Birth Defects Res. C Embryo Today, 2011, 93(1), 3-11.
[http://dx.doi.org/10.1002/bdrc.20200] [PMID: 21425437]
[21]
Nicita, F.; Verrotti, A.; Pruna, D.; Striano, P.; Capovilla, G.; Savasta, S.; Spartà, M.V.; Parisi, P.; Parlapiano, G.; Tarani, L.; Spalice, A. Seizures in fetal alcohol spectrum disorders: Evaluation of clinical, electroencephalographic, and neuroradiologic features in a pediatric case series. Epilepsia, 2014, 55(6), e60-e66.
[http://dx.doi.org/10.1111/epi.12638] [PMID: 24815902]
[22]
Wilson, S.E.; Cudd, T.A. Focus on: The use of animal models for the study of fetal alcohol spectrum disorders. Alcohol Res. Health, 2011, 34(1), 92-98.
[PMID: 23580046]
[23]
Lieschke, G.J.; Currie, P.D. Animal models of human disease: Zebrafish swim into view. Nat. Rev. Genet., 2007, 8(5), 353-367.
[http://dx.doi.org/10.1038/nrg2091] [PMID: 17440532]
[24]
Bilotta, J.; Barnett, J.A.; Hancock, L.; Saszik, S. Ethanol exposure alters zebrafish development: A novel model of fetal alcohol syndrome. Neurotoxicol. Teratol., 2004, 26(6), 737-743.
[http://dx.doi.org/10.1016/j.ntt.2004.06.011] [PMID: 15451038]
[25]
Ali, S.; Champagne, D.L.; Spaink, H.P.; Richardson, M.K. Zebrafish embryos and larvae: A new generation of disease models and drug screens. Birth Defects Res. C Embryo Today, 2011, 93(2), 115-133.
[http://dx.doi.org/10.1002/bdrc.20206] [PMID: 21671352]
[26]
Kalueff, A.V.; Stewart, A.M.; Gerlai, R. Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol. Sci., 2014, 35(2), 63-75.
[http://dx.doi.org/10.1016/j.tips.2013.12.002] [PMID: 24412421]
[27]
Kelly, S.J.; Goodlett, C.R.; Hannigan, J.H. Animal models of fetal alcohol spectrum disorders: Impact of the social environment. Dev. Disabil. Res. Rev., 2009, 15(3), 200-208.
[http://dx.doi.org/10.1002/ddrr.69] [PMID: 19731387]
[28]
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]
[29]
Gerlai, R. Embryonic alcohol exposure: Towards the development of a zebrafish model of fetal alcohol spectrum disorders. Dev. Psychobiol., 2015, 57(7), 787-798.
[http://dx.doi.org/10.1002/dev.21318] [PMID: 26079519]
[30]
Hooijmans, C.R.; Rovers, M.M.; de Vries, R.B.; Leenaars, M.; Ritskes-Hoitinga, M.; Langendam, M.W. SYRCLE’s risk of bias tool for animal studies. BMC Med. Res. Methodol., 2014, 14, 43.
[http://dx.doi.org/10.1186/1471-2288-14-43] [PMID: 24667063]
[31]
Kimmel, C.B.; Ballard, W.W.; Kimmel, S.R.; Ullmann, B.; Schilling, T.F. Stages of embryonic development of the zebrafish. Dev. Dyn., 1995, 203(3), 253-310.
[http://dx.doi.org/10.1002/aja.1002030302] [PMID: 8589427]
[32]
Seguin, D.; Shams, S.; Gerlai, R. Behavioral responses to novelty or to a predator stimulus are not altered in adult zebrafish by early embryonic alcohol exposure. Alcohol. Clin. Exp. Res., 2016, 40(12), 2667-2675.
[http://dx.doi.org/10.1111/acer.13249] [PMID: 27790739]
[33]
Parker, M.O.; Evans, A.M.; Brock, A.J.; Combe, F.J.; Teh, M.T.; Brennan, C.H. Moderate alcohol exposure during early brain development increases stimulus-response habits in adulthood. Addict. Biol., 2016, 21(1), 49-60.
[http://dx.doi.org/10.1111/adb.12176] [PMID: 25138642]
[34]
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, 97109774
[http://dx.doi.org/10.1016/j.pnpbp.2019.109774] [PMID: 31655157]
[35]
Wang, K.; Chen, X.; Liu, J.; Zou, L.P.; Feng, W.; Cai, L.; Wu, X.; Chen, S.Y. Embryonic exposure to ethanol increases the susceptibility of larval zebrafish to chemically induced seizures. Sci. Rep., 2018, 8(1), 1845.
[http://dx.doi.org/10.1038/s41598-018-20288-2] [PMID: 29382872]
[36]
Ramlan, N.F.; Sata, N.S.A.M.; Hassan, S.N.; Bakar, N.A.; Ahmad, S.; Zulkifli, S.Z.; Abdullah, C.A.C.; Ibrahim, W.N.W. Time dependent effect of chronic embryonic exposure to ethanol on zebrafish: Morphology, biochemical and anxiety alterations. Behav. Brain Res., 2017, 332, 40-49.
[http://dx.doi.org/10.1016/j.bbr.2017.05.048] [PMID: 28559182]
[37]
Fernandes, P.; Monteiro, S.M.; Venâncio, C.; Félix, L. 24-Epibrassinolide protects against ethanol-induced behavioural teratogenesis in zebrafish embryo. Chem. Biol. Interact., 2020, 328109193
[http://dx.doi.org/10.1016/j.cbi.2020.109193] [PMID: 32668205]
[38]
Basnet, R.M.; Zizioli, D.; Taweedet, S.; Finazzi, D.; Memo, M. Zebrafish larvae as a behavioral model in neuropharmacology. Biomedicines, 2019, 7(1)E23
[http://dx.doi.org/10.3390/biomedicines7010023] [PMID: 30917585]
[39]
Tal, T.L.; Franzosa, J.A.; Tilton, S.C.; Philbrick, K.A.; Iwaniec, U.T.; Turner, R.T.; Waters, K.M.; Tanguay, R.L. MicroRNAs control neurobehavioral development and function in zebrafish. FASEB J., 2012, 26(4), 1452-1461.
[http://dx.doi.org/10.1096/fj.11-194464] [PMID: 22253472]
[40]
Cadena, P.G.; Cadena, M.R.S.; Sarmah, S.; Marrs, J.A. Folic acid reduces the ethanol-induced morphological and behavioral defects in embryonic and larval zebrafish (Danio rerio) as a model for fetal alcohol spectrum disorder (FASD). Reprod. Toxicol., 2020, 96, 249-257.
[http://dx.doi.org/10.1016/j.reprotox.2020.07.013] [PMID: 32763456]
[41]
Cadena, P.G.; Sales Cadena, M.R.; Sarmah, S.; Marrs, J.A. Protective effects of quercetin, polydatin, and folic acid and their mixtures in a zebrafish (Danio rerio) fetal alcohol spectrum disorder model. Neurotoxicol. Teratol., 2020, 82106928
[http://dx.doi.org/10.1016/j.ntt.2020.106928] [PMID: 32861842]
[42]
Ali, S.; Champagne, D.L.; Alia, A.; Richardson, M.K. Large-scale analysis of acute ethanol exposure in zebrafish development: C critical time window and resilience. PLoS One, 2011, 6(5)e20037
[http://dx.doi.org/10.1371/journal.pone.0020037] [PMID: 21625530]
[43]
Pinheiro-da-Silva, J.; Agues-Barbosa, T.; Luchiari, A.C. Embryonic exposure to ethanol increases anxiety-like behavior in fry zebrafish. Alcohol Alcohol., 2020, 55(6), 581-590.
[http://dx.doi.org/10.1093/alcalc/agaa087] [PMID: 32886092]
[44]
Sterling, M.E.; Chang, G.Q.; Karatayev, O.; Chang, S.Y.; Leibowitz, S.F. Effects of embryonic ethanol exposure at low doses on neuronal development, voluntary ethanol consumption and related behaviors in larval and adult zebrafish: Role of hypothalamic orexigenic peptides. Behav. Brain Res., 2016, 304, 125-138.
[http://dx.doi.org/10.1016/j.bbr.2016.01.013] [PMID: 26778786]
[45]
Baiamonte, M.; Parker, M.O.; Vinson, G.P.; Brennan, C.H. Sustained effects of developmental exposure to ethanol on zebrafish anxiety-like behaviour. PLoS One, 2016, 11(2)e0148425
[http://dx.doi.org/10.1371/journal.pone.0148425] [PMID: 26862749]
[46]
Burton, D.F.; Zhang, C.; Boa-Amponsem, O.; Mackinnon, S.; Cole, G.J. Long-term behavioral change as a result of acute ethanol exposure in zebrafish: Evidence for a role for sonic hedgehog but not retinoic acid signaling. Neurotoxicol. Teratol., 2017, 61, 66-73.
[http://dx.doi.org/10.1016/j.ntt.2017.01.006] [PMID: 28223149]
[47]
Boa-Amponsem, O.; Zhang, C.; Mukhopadhyay, S.; Ardrey, I.; Cole, G.J. Ethanol and cannabinoids interact to alter behavior in a zebrafish fetal alcohol spectrum disorder model. Birth Defects Res., 2019, 111(12), 775-788.
[http://dx.doi.org/10.1002/bdr2.1458] [PMID: 30648819]
[48]
Bailey, J.M.; Oliveri, A.N.; Zhang, C.; Frazier, J.M.; Mackinnon, S.; Cole, G.J.; Levin, E.D. Long-term behavioral impairment following acute embryonic ethanol exposure in zebrafish. Neurotoxicol. Teratol., 2015, 48, 1-8.
[http://dx.doi.org/10.1016/j.ntt.2015.01.005] [PMID: 25599606]
[49]
Weeks, O.; Bossé, G.D.; Oderberg, I.M.; Akle, S.; Houvras, Y.; Wrighton, P.J.; LaBella, K.; Iversen, I.; Tavakoli, S.; Adatto, I.; Schwartz, A.; Kloosterman, D.; Tsomides, A.; Charness, M.E.; Peterson, R.T.; Steinhauser, M.L.; Fazeli, P.K.; Goessling, W. Fetal alcohol spectrum disorder predisposes to metabolic abnormalities in adulthood. J. Clin. Invest., 2020, 130(5), 2252-2269.
[http://dx.doi.org/10.1172/JCI132139] [PMID: 32202514]
[50]
Fernandes, Y.; Rampersad, M.; Jones, E.M.; Eberhart, J.K. Social deficits following embryonic ethanol exposure arise in post-larval zebrafish. Addict. Biol., 2019, 24(5), 898-907.
[http://dx.doi.org/10.1111/adb.12649] [PMID: 30178621]
[51]
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]
[52]
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]
[53]
Fernandes, Y.; Rampersad, M.; Gerlai, A.R. Impairment of social behaviour persists two years after embryonic alcohol exposure in zebrafish: A model of fetal alcohol spectrum disorders. Behav. Brain Res., 2015, 292, 102-108.
[http://dx.doi.org/10.1016/j.bbr.2015.05.060] [PMID: 26097005]
[54]
Parker, M.O.; Annan, L.V.; Kanellopoulos, A.H.; Brock, A.J.; Combe, F.J.; Baiamonte, M.; Teh, M.T.; Brennan, C.H. The utility of zebrafish to study the mechanisms by which ethanol affects social behavior and anxiety during early brain development. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2014, 55, 94-100.
[http://dx.doi.org/10.1016/j.pnpbp.2014.03.011] [PMID: 24690524]
[55]
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]
[56]
Baggio, S.; Mussulini, B.H.; de Oliveira, D.L.; Gerlai, R.; Rico, E.P. Embryonic alcohol exposure leading to social avoidance and altered anxiety responses in adult zebrafish. Behav. Brain Res., 2018, 352, 62-69.
[http://dx.doi.org/10.1016/j.bbr.2017.08.039] [PMID: 28882694]
[57]
Fernandes, Y.; Rampersad, M.; Eberhart, J.K. Social behavioral phenotyping of the zebrafish casper mutant following embryonic alcohol exposure. Behav. Brain Res., 2019, 356, 46-50.
[http://dx.doi.org/10.1016/j.bbr.2018.08.004] [PMID: 30107225]
[58]
Fernandes, Y.; Rampersad, M.; Gerlai, R. Embryonic alcohol exposure impairs the dopaminergic system and social behavioral responses in adult zebrafish. Int. J. Neuropsychopharmacol., 2015, 18(6)pyu089
[http://dx.doi.org/10.1093/ijnp/pyu089] [PMID: 25568285]
[59]
Cleal, M.; Parker, M.O. Moderate developmental alcohol exposure reduces repetitive alternation in a zebrafish model of fetal alcohol spectrum disorders. Neurotoxicol. Teratol., 2018, 70, 1-9.
[http://dx.doi.org/10.1016/j.ntt.2018.09.001] [PMID: 30201482]
[60]
Fernandes, Y.; Tran, S.; Abraham, E.; Gerlai, R. Embryonic alcohol exposure impairs associative learning performance in adult zebrafish. Behav. Brain Res., 2014, 265, 181-187.
[http://dx.doi.org/10.1016/j.bbr.2014.02.035] [PMID: 24594368]
[61]
Haab Lutte, A.; Huppes Majolo, J.; Reali Nazario, L.; Da Silva, R.S. Early exposure to ethanol is able to affect the memory of adult zebrafish: Possible role of adenosine. Neurotoxicology, 2018, 69, 17-22.
[http://dx.doi.org/10.1016/j.neuro.2018.08.012] [PMID: 30157450]
[62]
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]
[63]
Tran, S.; Facciol, A.; Gerlai, R. The zebrafish, a novel model organism for screening compounds affecting acute and chronic ethanol-induced effects. Int. Rev. Neurobiol., 2016, 126, 467-484.
[http://dx.doi.org/10.1016/bs.irn.2016.02.016] [PMID: 27055623]
[64]
Bailey, C.D.C.; Gerlai, R.; Cameron, N.M.; Marcolin, M.L.; McCormick, C.M. Preclinical methodological approaches investigating of the effects of alcohol on perinatal and adolescent neurodevelopment. Neurosci. Biobehav. Rev., 2020, 116, 436-451.
[http://dx.doi.org/10.1016/j.neubiorev.2020.07.011] [PMID: 32681938]
[65]
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]
[66]
Baggio, S.; Mussulini, B.H.; de Oliveira, D.L.; Zenki, K.C.; Santos da Silva, E.; Rico, E.P. Embryonic alcohol exposure promotes long-term effects on cerebral glutamate transport of adult zebrafish. Neurosci. Lett., 2017, 636, 265-269.
[http://dx.doi.org/10.1016/j.neulet.2016.11.016] [PMID: 27838452]
[67]
Weyrauch, D.; Schwartz, M.; Hart, B.; Klug, M.G.; Burd, L. Comorbid mental disorders in fetal alcohol spectrum disorders: A systematic review. J. Dev. Behav. Pediatr., 2017, 38(4), 283-291.
[http://dx.doi.org/10.1097/DBP.0000000000000440] [PMID: 28460370]
[68]
Lovely, C.B.; Nobles, R.D.; Eberhart, J.K. Developmental age strengthens barriers to ethanol accumulation in zebrafish. Alcohol, 2014, 48(6), 595-602.
[http://dx.doi.org/10.1016/j.alcohol.2014.06.003] [PMID: 25012627]
[69]
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]
[70]
Gilbert, M.J.; Zerulla, T.C.; Tierney, K.B. Zebrafish (Danio rerio) as a model for the study of aging and exercise: Physical ability and trainability decrease with age. Exp. Gerontol., 2014, 50, 106-113.
[http://dx.doi.org/10.1016/j.exger.2013.11.013] [PMID: 24316042]
[71]
Andersen, S.L. Trajectories of brain development: Point of vulnerability or window of opportunity? Neurosci. Biobehav. Rev., 2003, 27(1-2), 3-18.
[http://dx.doi.org/10.1016/S0149-7634(03)00005-8] [PMID: 12732219]
[72]
Dobbing, J.; Sands, J. Comparative aspects of the brain growth spurt. Early Hum. Dev., 1979, 3(1), 79-83.
[http://dx.doi.org/10.1016/0378-3782(79)90022-7] [PMID: 118862]
[73]
Hildebrand, D.G.C.; Cicconet, M.; Torres, R.M.; Choi, W.; Quan, T.M.; Moon, J.; Wetzel, A.W.; Scott Champion, A.; Graham, B.J.; Randlett, O.; Plummer, G.S.; Portugues, R.; Bianco, I.H.; Saalfeld, S.; Baden, A.D.; Lillaney, K.; Burns, R.; Vogelstein, J.T.; Schier, A.F.; Lee, W.A.; Jeong, W.K.; Lichtman, J.W.; Engert, F. Whole-brain serial-section electron microscopy in larval zebrafish. Nature, 2017, 545(7654), 345-349.
[http://dx.doi.org/10.1038/nature22356] [PMID: 28489821]
[74]
Hellemans, K.G.; Sliwowska, J.H.; Verma, P.; Weinberg, J. Prenatal alcohol exposure: Fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci. Biobehav. Rev., 2010, 34(6), 791-807.
[http://dx.doi.org/10.1016/j.neubiorev.2009.06.004] [PMID: 19545588]
[75]
Streissguth, A.P.; Barr, H.M.; Olson, H.C.; Sampson, P.D.; Bookstein, F.L.; Burgess, D.M. Drinking during pregnancy decreases word attack and arithmetic scores on standardized tests: Adolescent data from a population-based prospective study. Alcohol. Clin. Exp. Res., 1994, 18(2), 248-254.
[http://dx.doi.org/10.1111/j.1530-0277.1994.tb00009.x] [PMID: 8048722]
[76]
Streissguth, A.P.; Barr, H.M.; Sampson, P.D. Moderate prenatal alcohol exposure: Effects on child IQ and learning problems at age 7 1/2 years. Alcohol. Clin. Exp. Res., 1990, 14(5), 662-669.
[http://dx.doi.org/10.1111/j.1530-0277.1990.tb01224.x] [PMID: 2264594]
[77]
Burd, L.; Popova, S. Fetal alcohol spectrum disorders: Fixing our aim to aim for the fix. Int. J. Environ. Res. Public Health, 2019, 16(20)E3978
[http://dx.doi.org/10.3390/ijerph16203978] [PMID: 31635265]

Rights & Permissions Print Cite
Article Metrics
21
1
© 2024 Bentham Science Publishers | Privacy Policy