Intermittent voluntary ethanol drinking during periadolescence impairs adult spatial learning after a long abstinence period in rats
- Díaz, Ana
- García Burgos, David
- Manrique, Tatiana
- González, Felisa
- Gallo, Milagros
ISSN: 1576-8597
Année de publication: 2011
Volumen: 32
Número: 2
Pages: 347-365
Type: Article
D'autres publications dans: Psicológica: Revista de metodología y psicología experimental
Résumé
Although previous findings point to the long-term impact of ethanol exposure during periadolescence on hippocampal-dependent learning tasks, comparisons considering different onset and exposure periods during this developmental range of ages are still needed. The aim of this experiment was to determine whether intermittent voluntary chronic ethanol consumption onset at different ages, beginning either in pre-adolescence or adolescence, differentially produces impairment in the hidden-platformwater- maze-task performance persisting in adult rats after a 27-day-long period of abstinence. The performance of two groups of adult Wistar rats of both sexes, whose ethanol drinking onset was at postnatal day 19 (preadolescent) or 28 (adolescent), was compared with that of an adult control non-ethanol exposed group. The results indicated that voluntary intermittent ethanol drinking during the periadolescent period caused dramatic long-term detrimental effects in female rats which were unable to learn. Male rats were also impaired during the initial training blocks, the impact being greater in the group exposed during adolescence, but they exhibited no differences with the non-ethanol exposed control group by the end of training (block 6) and in a probe trial. These data support a greater vulnerability in females during periadolescence and point to adolescence as an especially sensitive period during male development to the long-term detrimental effects of ethanol in learning.
Références bibliographiques
- Acheson, S.K., Richardson, R., and Swartzwelder, H.S. (1999). Developmental changes in seizure susceptibility during ethanol withdrawal. Alcohol, 18(1), 23-26.
- Barron, S., and Riley, E.P. (1990). Passive avoidance performance following neonatal alcohol exposure. Neurotoxicology and teratology, 12(2), 135-38.
- Barron S, White A, Swartzwelder HS, Bell RL, Rodd ZA, Slawecki CJ, Ehlers CL, Levin ED, Rezvani AH and Spear LP. (2005). Adolescent vulnerabilities to chronic alcohol or nicotine exposure: findings from rodent models. Alcoholism, clinical and experimental research, 29(9), 1720-5.
- Berman, R.F. and Hannigan, J.H. (2000). Effects of prenatal alcohol exposure on the hippocampus: spatial behavior, electrophysiology, and neuroanatomy. Hippocampus, 10(1), 94-110.
- Bilgi, C., Tokgöz, S., Aydin, A., Celik, T., and Uzbay, I.T. (2003). The effects of chronic ethanol consumption and ethanol withdrawal on serum cholinesterase activity in rats. Alcohol, 38(4), 316-20.
- Boulouard, M., Lelong, V., Daoust, M. and Naassila, M. (2002). Chronic ethanol consumption induces tolerance to the spatial memory impairing effects of acute ethanol administration in rats. Behavioural brain research, 136(1), 239-46.
- Brown, S.A., and Tapert, S.F. (2004). Adolescence and the trajectory of alcohol use: basic to clinical studies. Annals of the New York Academy of Sciences, 1021, 234-44.
- Brunell, S.C., and Spear, L.P. (2006). Effects of acute ethanol or amphetamine administration on the acoustic startle response and prepulse inhibition in adolescent and adult rats. Psychopharmacology, 186(4), 579-86.
- Celik, T., Cakir, E., Kayir, H., Bilgi, C., and Uzbay, I.T. (2005). The effects of chronic ethanol consumption and withdrawal on passive avoidance task and serum cholinesterase level in rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 29(4), 505-09.
- Chin, V.S., Van Skike, C.E. and Matthews, D.B. (2010). Effects of ethanol on hippocampal function during adolescence: a look at the past and thoughts on the future. Alcohol, 44(1), 3-14.
- Crews, F.T., Braun, C.H.J., Hoplight, B., Switzer, R.C. 3rd, and Knapp, D.J. (2000). Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcoholism, clinical and experimental research, 24(11), 1712-23.
- Esmorís-Arranz, F.J., Mendez, C and Spear, N.E. (2008). Contextual fear conditioning differs for infant, adolescent, and adult rats. Behavioral Processes, 78(3), 340-52.
- Garcia-Burgos, D., González, F., Manrique, T., and Gallo, M. (2009). Patterns of ethanol intake in preadolescent, adolescent, and adult Wistar rats under acquisition, maintenance, and relapse-like conditions. Alcoholism, clinical and experimental research, 33(4), 722-28.
- Garcia-Burgos, D., Manrique, T., Gallo, M., and González, F. (2010). Sex differences on the alcohol deprivation effect in rats. Psicothema, 22(4), 887-92.
- Girard, T.A., Xing, H.C., Ward, G.R. and Wainwright, P.E. (2000). Early postnatal ethanol exposure has long-term effects on the performance of male rats in a delayed matching-to-place task in the Morris water maze. Alcoholism, clinical and experimental research, 24(3), 300-06.
- Guerri, C. and Pascual, M. (2010). Mechanisms involved in the neurotoxic, cognitive, and neurobehavioral effects of alcohol consumption during adolescence. Alcohol, 44(1) 15-26.
- Goodlett, C.R., and Peterson, S.D. (1995). Sex differences in vulnerability to developmental spatial learning deficits induced by limited binge alcohol exposure in neonatal rats. Neurobiology of learning and memory, 64(3), 265-75.
- Kelly, S.J., Goodlett, C.R., Hulsether, S.A., and West, J.R. (1988). Impaired spatial navigation in adult female but not adult male rats exposed to alcohol during the brain growth spurt. Behavioral brain research, 27(3), 247-57.
- Lukoyanov, N.V., Andrade, J.P., Dulce Madeira, and M., Paula-Barbosa, M.M. (1999). Effects of age and sex on the water maze performance and hippocampal cholinergic fibers in rats. Neuroscience letters, 269(3), 141-44.
- Lukoyanov, N.V., Sá, M.J., Madeira, M.D., Paula-Barbosa, M.M. (2004). Selective loss of hilar neurons and impairment of initial learning in rats after repeated administration of electroconvulsive shock seizures. Experimental brain research, 154(2), 192-200.
- Macey, D.J., Schulteis, G., Heinrichs, S.C., and Koob, G.F. (1996). Time-dependent quantifiable withdrawal from ethanol in the rat: effect of method of dependence induction. Alcohol, 13(2), 163-70.
- Manrique T, Gámiz F, Morón I, Ballesteros MA, Gallo M. (2009). Peculiar modulation of taste aversion learning by the time of day in developing rats. Developmental Psychobiology, 51(2):147-57.
- Manrique, T., Molero, A., Cándido, A., and Gallo, M. (2005). Early learning failure impairs adult learning in rats. Developmental psychobiology, 46(4), 340-49.
- Masten, A.S., Faden, V.B., Zucker, R.A. and Apear, L.P. (2009). A developmental perspective on underage alcohol use. Alcohol research & health: the journal of the National Institute on Alcohol Abuse and Alcoholism, 32(1), 3-15.
- Matthews, D.B. (2010). Adolescence and alcohol: recent advances in understanding the impact of alcohol use during a critical developmental window. Alcohol, 44(1), 1-2.
- Matthews, D.B., and Silvers, J.R. (2004). The use of acute ethanol administration as a tool to investigate multiple memory systems. Neurobiology of learning and memory, 82(3), 299-308.
- Molina, J.C., Spear, N.E., Spear, L.P., Mennella, J.A., and Lewis, M.J. (2007). The International society for developmental psychobiology 39th annual meeting symposium: Alcohol and development: beyond fetal alcohol syndrome. Developmental psychobiology, 49(3), 227-42.
- Morris, S.A., Kelsom M.L., Liput, D.J. Marshall, S.A. and Nixon, M.K. (2010). Similar withdrawal severity in adolescents and adults in a rat model of alcohol dependence. Alcohol, 44(1) 89-98.
- Pascual, M., Blanco, A.M., Caulli, O., Miñarro, J., and Guerri, C. (2007). Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. The European journal of neuroscience, 25(2) 541-50.
- Rice, D., and Barone, S. Jr. (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental health perspectives, 108(3), 511-33.
- Santín, L.J., Rubio, S., Begega, A., Miranda, R., and Arias, J.L. (2000). Spatial learning and the hippocampus. Revista de Neurologi, 31(5), 455-62.
- Santucci, A.C., Cortes, C., Bettica, A., and Cortes, F. (2008). Chronic ethanol consumption in rats produces residual increases in anxiety 4 months after withdrawal. Behavioral brain research, 188(1), 24-31.
- Santucci, A.C., Mercado, M., Bettica, A., Cortes, C., York, D., and Moody, E. (2004). Residual behavioral and neuroanatomical effects of short-term chronic ethanol consumption in rats. Brain research. Cognitive brain research, 20(3), 449-61.
- Schulteis, G., Archer, C, Tapert, S.F., and Frank, L.R. (2008). Intermittent binge alcohol exposure during the periadolescent period induces spatial working memory deficits in young adult rats. Alcohol, 42(6), 459-67.
- Siciliano, D., and Smith, R.F. (2001). Periadolescent alcohol alters adult behavioral characteristics in the rat. Physiology & behavior, 74(4-5), 637-43.
- Sircar, R, and Sircar, D. (2005). Adolescent rats exposed to repeated ethanol treatment show lingering behavioral impairments. Alcoholism, clinical and experimental research, 29(8), 1402-10.
- Sircar, R., Basak, A.K., and Sircar, D. (2009). Repeated ethanol exposure affects the acquisition of spatial memory in adolescent female rats. Behavioral brain research, 202(2), 225-31.
- Spanagel, R., Holter, S.M. (1999). Long-term alcohol self-administration with repeated alcohol deprivation phases: an animal model of alcoholism? Alcohol, 34(2) 231-43.
- Spear, N.E., and Molina, J.C. (2005). Fetal or infantile exposure to ethanol promotes ethanol ingestion in adolescence and adulthood: a theoretical review. Alcoholism, clinical and experimental research, 29(6), 909-29.
- Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and biobehavioral reviews, Rev 24(4) 417-63.
- Spear, L.P, and Varlinskaya, E.I. (2005). Adolescence. Alcohol sensitivity, tolerance, and intake. Recent developments in alcoholism: an official publication of the American Medical Society on Alcoholism, the Research Society on Alcoholism, and the National Council on Alcoholism, 17, 143-59.
- Squeglia, L.M., Jacobus, J., and Tapert, S.F. (2009). The influence of substance use on adolescent brain development. Clinical EEG and neuroscience: official journal of the EEG and Clinical Neuroscience Society (ENCS), 40(1), 31-8. Review.
- Stanton, M. (2000). Multiple memory systems, development and conditioning. Behavioral brain research, 110(1-2), 25-37.
- Vetter, C.S., Doremus-Fitzwater, T.L., and Spear, L.P. (2007). Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcoholism, clinical and experimental research, 31(7), 1159-68.
- Windle, M., Spear, L.P., Fuligni, A.J., Angold, A., Brown, J.D., Pine, D., Smith, G.T., Giedd, J., and Dahl, R.E. (2008). Transitions into underage and problem drinking: developmental processes and mechanisms between 10 and 15 years of age. Pediatrics, 121, Suppl 4, S273-89.
- White, A.M., and Swartzwelder, H.S. (2004). Hippocampal function during adolescence: a unique target of ethanol effects. Annals of the New York Academy of Sciences, 1021, 206-20.
- White, A.M., and Swartzwelder, H.S. (2005). Age-related effects of alcohol on memory and memory-related brain function in adolescents and adults. Recent developments in alcoholism: an official publication of the American Medical Society on Alcoholism, the Research Society on Alcoholism, and the National Council on Alcoholism, 17, 161-76.
- Witt, E.D. (2010). Research on alcohol and adolescent brain development: opportunities and future directions. Alcohol, 44(1) 119-24.
- Yap CS, Richardson R. (2005). Latent inhibition in the developing rat: an examination of context-specific effects. Developmental Psychobiology, 47(1), 55-65.