Diferencias sexuales en tareas emocionales y cognitivas en ratas expuestas a atracones de alcohol y en controles durante la adultez temprana Sex differences in emotional and cognitive tasks in rats exposed to alcohol binges and controls during early adulthood

Autores/as

  • Leticia López-Valencia Universidad Complutense de Madrid
  • Eva Bonilla Universidad Complutense de Madrid
  • Berta Escudero Universidad Complutense de Madrid
  • Laura Orio Universidad Complutense de Madrid

DOI:

https://doi.org/10.20882/adicciones.2450

Palabras clave:

alcohol, adolescencia, comportamiento, atracones, diferencias sexuales Alcohol, Aolescence, behaviour, binge drinking, sex differences

Resumen

Integrar la perspectiva de sexo en estudios preclínicos sobre la exposición excesiva a alcohol durante la juventud o la adultez temprana sigue siendo limitada. Este estudio tuvo como objetivo evaluar los efectos de altas dosis de etanol en el comportamiento emocional y la cognición en ratas de 8 semanas de edad, considerando diferencias de sexo. Machos y hembras fueron expuestos a atracones de etanol (3 g/kg, vía oral; 3 veces al día durante 4 días) en un paradigma de dos días alternos, y evaluados en el laberinto elevado en cruz (EPM), la prueba de natación forzada (FST), la prueba de preferencia de sacarina (SPT), el laberinto acuático de Morris (MWM) y la prueba de reconocimiento de objetos nuevos (NOR). Se observaron diferencias basales entre machos y hembras controles en tareas emocionales, motivacionales y cognitivas. Además, la Exposición Intensiva al Alcohol (EIA) ejerció efectos específicos por sexo en: a) EPM: los machos mostraron ansiedad y ningún efecto en las hembras; b) FST: síntomas similares a la depresión en ambos sexos, pero un tiempo de inmovilidad más pronunciado en las hembras; c) Prueba NOR: Se observó deterioro de la memoria a corto plazo en ambos sexos, pero las hembras mostraron un mejor rendimiento a largo plazo en comparación con sus controles. No se observaron efectos relacionados con la EIA en las pruebas de conducta SPT ni en MWM. Estos resultados sugieren diferencias inherentes entre sexos en el rendimiento de los roedores en pruebas conductuales que evalúan las conductas emocionales, motivacionales y cognitivas. Además, la EIA podría afectar de forma diferente a machos y hembras durante la abstinencia en adultez temprana. Estos hallazgos subrayan la importancia de considerar el sexo como una variable crítica en los estudios preclínicos.
A sex perspective in the behavioural effects induced by alcohol binge exposure during youth or early adulthood remain limited. This study aimed to evaluate the effects of high doses of ethanol on emotional behaviour and cognition in 8-weeks old rats, from a sex perspective. Male and female animals were exposed to ethanol binges (3 g/kg, i.g.; 3 times/day x 4 days) in a 2days on-2days off paradigm and assessed in the elevated plus maze (EPM), forced swimming test (FST), saccharin preference test (SPT), Morris water maze (MWM) and novel object recognition (NOR) test. Baseline differences between control male and females were observed in emotional, motivational and cognitive tasks. Additionally, Intensive Alcohol Exposure (IAE) exerted sex-specific effects in: a) EPM: males showed anxiety and no effect in females; b) FST: depressive-like symptoms in both sexes but more pronounce immobility time in females; c) NOR test: impairment in a short-term memory in both sexes but females displayed improved performance in a long-term versus their controls. No IAE-related effects were found in the SPT or MWM. These results suggest inherent sex-differences in rodent performance in behavioural tests assessing emotional, motivational and cognitive behaviours. Additionally, IAE may impact male and females differently during abstinence in early adulthood. These findings underscore the importance of considering sex as a critical variable for preclinical studies.

Citas

Abderrahim, L., Hicham, E. M., Aboubaker, E., Fatima, A., Tarik, T., Soufiane, B. y Abdelhalim, M. (2022). Sex differences in behavioral, cognitive and voluntary ethanol-intake effects in Dexamethasone-induced depression-like state in Wistar rat. AIMS Neuroscience, 30(7), 228–249. https://doi.org/10.3934/neuroscience.2022012

Albrechet-Souza, L., Schratz, C. L. y Gilpin, N. W. (2020). Sex differences in traumatic stress reactivity in rats with and without a history of alcohol drinking. Biology of Sex Differences, 11(1). https://doi.org/10.1186/s13293-020-00303-w

Antón, M., Alén, F., Gómez de Heras, R., Serrano, A., Pavón, F. J., Leza, J. C., García-Bueno, B., Rodríguez de Fonseca, F. y Orio, L. (2017). Oleoylethanolamide prevents neuroimmune HMGB1/TLR4/NF-kB danger signaling in rat frontal cortex and depressive-like behavior induced by ethanol binge administration. Addict. Biol., 22(3), 724–741. https://doi.org/10.1111/adb.12365

Antón, M., Rodríguez-González, A., Ballesta, A., González, N., Del Pozo, A., de Fonseca, F.R., Gómez-Lus, M.L., Leza, J.C., García-Bueno, B., Caso, J.R. y Orio, L. (2018). Alcohol binge disrupts the rat intestinal barrier: the partial protective role of oleoylethanolamide. Br J Pharmacol. 175(24), 4464-4479. https://doi: 10.1111/bph.14501

Ardinger, C. E., Chen, Y., Kimbrough, A., Grahame, N. J. y Lapish, C. C. (2024). Sex differences in neural networks recruited by frontloaded binge alcohol drinking. Addiction Biology, 29(9). https://doi.org/10.1111/adb.13434

Armario, A. (2021). The forced swim test: Historical, conceptual and methodological considerations and its relationship with individual behavioral traits. Neuroscience and Biobehavioral Reviews, 128, 74–86. https://doi.org/10.1016/j.neubiorev.2021.06.014

Bach, E. C., Morgan, J. W., Ewin, S. E., Barth, S. H., Raab-Graham, K. F. y Weiner, J. L. (2021). Chronic Ethanol Exposures Leads to a Negative Affective State in Female Rats That Is Accompanied by a Paradoxical Decrease in Ventral Hippocampus Excitability. Frontiers in Neuroscience, 15. https://doi.org/10.3389/fnins.2021.669075

Baraona, E., Abittan, C. S., Dohmen, K., Moretti, M., Pozzato, G., Chayes, Z. W., Schaefer, C. y Lieber, C. S. (2001). Gender differences in pharmacokinetics of alcohol. Alcoholism: Clinical and Experimental Research, 25(4), 502–507. https://doi.org/10.1111/j.1530-0277.2001.tb02242.x

Bevins, R. A. y Besheer, J. (2006). Object recognition in rats and mice: A one-trial non-matching-to-sample learning task to study “recognition memory.” Nature Protocols, 1(3), 1306–1311. https://doi.org/10.1038/nprot.2006.205

Bowman, R., Frankfurt, M. y Luine, V. (2022). Sex differences in cognition following variations in endocrine status. In Learning and Memory (Vol. 29, Issue 9, pp. 234–245). Cold Spring Harbor Laboratory Press. https://doi.org/10.1101/lm.053509.121

Buján, G. E., D’Alessio, L., Serra, H. A., Guelman, L. R. y Molina, S. J. (2024). Assessment of Hippocampal-Related Behavioral Changes in Adolescent Rats of both Sexes Following Voluntary Intermittent Ethanol Intake and Noise Exposure: A Putative Underlying Mechanism and Implementation of a Non-pharmacological Preventive Strategy. Neurotoxicity Research, 42(3). https://doi.org/10.1007/s12640-024-00707-1

Campbell, H. M., Guo, J. D. y Kuhn, C. M. (2024). Applying the Research Domain Criteria to Rodent Studies of Sex Differences in Chronic Stress Susceptibility. In Biological Psychiatry. Elsevier Inc. https://doi.org/10.1016/j.biopsych.2024.05.016

Chen, L., Lu, Y., Hua, X., Zhang, H., Sun, S. y Han, C. (2024). Three methods of behavioural testing to measure anxiety – A review. In Behavioural Processes (Vol. 215). Elsevier B.V. https://doi.org/10.1016/j.beproc.2024.104997

Chung, T., Creswell, K. G., Bachrach, R., Clark, D. B. y Martin, C. S. (2018). Adolescent Binge Drinking Developmental Context and Opportunities for Prevention.

Corbett, C. M., Bozarth, S. L. y West, E. A. (2024). Effects of sex and estrous cycle on action-outcome contingencies. Behavioural Brain Research, 477. https://doi.org/10.1016/j.bbr.2024.115317

Cosquer, B., Galani, R., Kuster, N. y Cassel, J. C. (2005). Whole-body exposure to 2.45 GHz electromagnetic fields does not alter anxiety responses in rats: A plus-maze study including test validation. Behavioural Brain Research, 156(1), 65–74. https://doi.org/10.1016/j.bbr.2004.05.007

Costa-Valle, M. T., Gomes, J. F., De Oliveira, C. R., Scherer, A., Franco De Oliveira, S. C. W. de S. E., Menezes, R. C. R., Leal, M. B., Romão, P. R. T. y Dallegrave, E. (2022). Energy drinks and alcohol in a binge drinking protocol in Wistar rats: Male and female behavioral and reproductive effects. Pharmacology Biochemistry and Behavior, 221. https://doi.org/10.1016/j.pbb.2022.173487

Crews, F.T., Vetreno, R.T., Broadwater, M.A. y Robinson, D.N. (2016) Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior. Pharmacol Rev 68(4):1074-1109. https://doi: 10.1124/pr.115.012138.

Cryan, J. F., Markou, A. y Lucki, I. (2002). Assessing antidepressant activity in rodents: Recent developments and future needs. TRENDS in Pharmacological Sciences, 23(5). https://doi.org/10.1016/s0165-6147(02)02017-5

Dalla, C., Pitychoutis, P. M., Kokras, N. y Papadopoulou-Daifoti, Z. (2010). Sex differences in animal models of depression and antidepressant response. Basic and Clinical Pharmacology and Toxicology, 106(3), 226–233. https://doi.org/10.1111/j.1742-7843.2009.00516.x

Detke, M. J., Rickels, M., Lucki, I., Rickels, M. y Detke, M. J. (1995). Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology, 121, 66–72. https://doi.org/10.1007/BF02245592

Desroches, D., Orevillo, C. y Verina, D. (1995). Sex-and Strain-Related Differences in First-Pass Alcohol Metabolism in Mice. Alcohol, 12(3), 221–226

Donner, N. C. y Lowry, C. A. (2013). Sex differences in anxiety and emotional behavior. In Pflugers Archiv European Journal of Physiology (Vol. 465, Issue 5, pp. 601–626). https://doi.org/10.1007/s00424-013-1271-7

Elena Quintanilla, M., Tampier, L., Sapag, A., Gerdtzen, Z. y Israel, Y. (2007). Sex differences, alcohol dehydrogenase, acetaldehyde burst, and aversion to ethanol in the rat: A systems perspective. American Journal of Physiology-Endocrinology and Metabolism, 293, E531–E537. https://doi.org/10.1152/ajpendo.00187.2007

Erol, A. y Karpyak, V. M. (2015). Sex and gender-related differences in alcohol use and its consequences: Contemporary knowledge and future research considerations. Drug and Alcohol Dependence, 156, 1–13. https://doi.org/10.1016/j.drugalcdep.2015.08.023

Gutiérrez-Menéndez, A., Méndez, M. y Arias, J. L. (2023). Learning and metabolic brain differences between juvenile male and female rats in the execution of different training regimes of a spatial memory task. Physiology & Behavior, 267, 114203. https://doi.org/10.1016/j.physbeh.2023.114203

Hamson, D. K., Roes, M. M. y Galea, L. A. M. (2016). Sex hormones and cognition: Neuroendocrine influences on memory and learning. Comprehensive Physiology. https://doi.org/10.1002/cphy.c150031

He, W., Zhang, S., Qi, Z. y Liu, W. (2024). Unveiling the potential of estrogen: Exploring its role in neuropsychiatric disorders and exercise intervention. Pharmacological Research, 204, 107201. https://doi.org/10.1016/j.phrs.2024.107201

Healey, K. L., Kibble, S., Dubester, K., Bell, A. y Swartzwelder, H. S. (2023). Adolescent intermittent ethanol exposure enhances adult stress effects in male rats. Pharmacology Biochemistry and Behavior, 223, 173513. https://doi.org/10.1016/j.pbb.2022.173513

Jia, W., Li, C., Chen, H., Wang, X., Liu, Y., Shang, W., Wang, B., Meng, W., Guo, Y., Zhu, L., Wang, D., Zhou, D., Zhao, B. y Wei, L. (2024). ISRIB ameliorates spatial learning and memory impairment induced by adolescent intermittent ethanol exposure in adult male rats. Neurochemistry International, 179, 105834. https://doi.org/10.1016/j.neuint.2024.105834

Kaluve, A. M., Le, J. T. y Graham, B. M. (2022). Female rodents are not more variable than male rodents: A meta-analysis of preclinical studies of fear and anxiety. Neuroscience & Biobehavioral Reviews, 143, 104962. https://doi.org/10.1016/j.neubiorev.2022.104962

Kishimoto, R., Ogishi, Y., Ueda, M., Matsdsaki, M., Amako, K., Goda, K. y Park, S.-S. (2002). Gender-related differences in mouse hepatic ethanol metabolism. Journal of Nutritional Science and Vitaminology, 48(3), 216–224.

Klein Marcondes, F., Miguel, K. J., Lins Melo, L. y Spadari-Bratfisch, R. C. (2001). Estrous cycle influences the response of female rats in the elevated plus-maze test. Brazilian Journal of Medical and Biological Research, 34(11), 1491–1498. https://doi.org/10.1590/s0100-879x2001001100006

Kokras, N., Antoniou, K., Mikail, H. G., Kafetzopoulos, V., Papadopoulou-Daifoti, Z. y Dalla, C. (2015). Forced swim test: What about females? Neuropharmacology, 99, 408–421. https://doi.org/10.1016/j.neuropharm.2015.03.016

Koszałka, A., Lustyk, K. y Pytka, K. (2023). Sex-dependent differences in animal cognition. Neuroscience & Biobehavioral Reviews, 153, 105374. https://doi.org/10.1016/j.neubiorev.2023.105374

Lamont, M. G., McCallum, P., Head, N., Blundell, J. y Weber, J. T. (2020). Binge drinking in male adolescent rats and its relationship to persistent behavioral impairments and elevated proinflammatory/proapoptotic proteins in the cerebellum. Psychopharmacology, 237(5), 1305–1315. https://doi.org/10.1007/s00213-020-05458-3

Lees, B., Mewton, L., Stapinski, L. A., Squeglia, L. M., Rae, C. D. y Teesson, M. (2019). Neurobiological and cognitive profile of young binge drinkers: A systematic review and meta-analysis. Neuropsychology Review, 29(3), 357–385. https://doi.org/10.1007/s11065-019-09411-w

Leonardo Jimenez Chavez, C., Coelho, M. A., Brewin, L. W., Swauncy, I., Tran, T., Albanese, T., Laguna, A., Gabriela, I. y Szumlinski, K. K. (2020). Incubation of negative affect during protracted alcohol withdrawal is age-, but not sex-selective. Brain Sciences, 10(6), Article 405. https://doi.org/10.3390/brainsci10060405

Lopez, M. F., Simpson, D. D., White, N. M. y Randall, C. L. (2003). Age- and sex-related differences in alcohol and nicotine effects in C57BL/6J mice. Addiction Biology, 8(4), 419–427. https://doi.org/10.1080/13556210310001648176

Livy, D. J., Parnell, S. E. y West, J. R. (2003). Blood ethanol concentration profiles: A comparison between rats and mice. Alcohol, 29(3), 165–171. https://doi.org/10.1016/S0741-8329(03)00025-9

López-Valencia, L., Moya, M., Escudero, B., García-Bueno, B. y Orio, L. (2024). Bacterial lipopolysaccharide forms aggregates with apolipoproteins in male and female rat brains after ethanol binges. Journal of Lipid Research, 65(3), 100509. https://doi.org/10.1016/j.jlr.2024.100509

Magee, S. N., Sereno, A. C. y Herman, M. A. (2024). Sex differences in basal motivated behavior, chronic ethanol drinking, and amygdala activity in female and male mice. Alcohol, 120, 85–97. https://doi.org/10.1016/j.alcohol.2024.06.004

Maldonado-Devincci, A. M., Makdisi, J. G., Hill, A. M., Waters, R. C., Hall, N. I., Shobande, M. J. y Kumari, A. (2022). Adolescent intermittent ethanol exposure induces sex-dependent divergent changes in ethanol drinking and motor activity in adulthood in C57BL/6J mice. Journal of Neuroscience Research, 100(8), 1560–1572. https://doi.org/10.1002/jnr.24814

Marco, E. M., Ballesta, J. A., Irala, C., Hernández, M. D., Serrano, M. E., Mela, V. y Viveros, M. P. (2017). Sex-dependent influence of chronic mild stress (CMS) on voluntary alcohol consumption; study of neurobiological consequences. Pharmacology Biochemistry and Behavior, 152, 68-80. https://doi.org/10.1016/j.pbb.2016.11.005

Marco, E. M., Valero, M., De La Serna, O., Aisa, B., Borcel, E., Ramirez, M. J. y Viveros, M. P. (2013). Maternal deprivation effects on brain plasticity and recognition memory in adolescent male and female rats. Neuropharmacology, 68, 223–231. https://doi.org/10.1016/j.neuropharm.2012.08.014

Moya, M., López-Valencia, L., García-Bueno, B. y Orio, L. (2022). Disinhibition-like behavior correlates with frontal cortex damage in an animal model of chronic alcohol consumption and thiamine deficiency. Biomedicines, 10(2), 260. https://doi.org/10.3390/biomedicines10020260

Moya, M., San Felipe, D., Ballesta, A., Alén, F., de Fonseca, F. R., García-Bueno, B. y Orio, L. (2021). Cerebellar and cortical TLR4 activation and behavioral impairments in Wernicke-Korsakoff Syndrome: Pharmacological effects of oleoylethanolamide. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 108, 110190. https://doi.org/10.1016/j.pnpbp.2020.110190

Obernier, J. A., Bouldin, T. W. y Crews, F. T. (2002). Binge ethanol exposure in adult rats causes necrotic cell death. Alcoholism: Clinical and Experimental Research, 26(4), 547–557. https://doi.org/10.1111/j.1530-0277.2002.tb02574.x

Org, E., Mehrabian, M., Parks, B. W., Shipkova, P., Liu, X., Drake, T. A. y Lusis, A. J. (2016). Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes, 7(4), 313–322. https://doi.org/10.1080/19490976.2016.1203502

Orio, L., Antón, M., Rodríguez-Rojo, I. C., Correas, Á., García-Bueno, B., Corral, M., de Fonseca, F. R., García-Moreno, L. M., Maestú, F. y Cadaveira, F. (2018). Young alcohol binge drinkers have elevated blood endotoxin, peripheral inflammation and low cortisol levels: Neuropsychological correlations in women. Addiction Biology, 23(5), 1130–1144. https://doi.org/10.1111/adb.12543

Orio, L. (2020). The multifaceted potential of the lipid transmitter oleoylethanolamide to treat alcohol-induced neuroinflammation and alcohol use disorders. Neural Regeneration Research, 15(1), 71–72. https://doi.org/10.4103/1673-5374.264457

Orio, L., Alén, F., Pavón, F. J., Serrano, A. y García-Bueno, B. (2019). Oleoylethanolamide, neuroinflammation, and alcohol abuse. Frontiers in Molecular Neuroscience, 11, 490. https://doi.org/10.3389/fnmol.2018.00490

Paiva-Santos, M. A., Leão, A. H. F. F., Kurita, J. P. F., Becegato, M. S., Lima, A. C., Bioni, V. S., Meurer, Y. S. R., Cunha, D. M. G., Medeiros, A. M. y Silva, R. H. (2022). Sex differences in the acute ethanol effects on object recognition memory: Influence of estrous cycle. Behavioural Pharmacology, 33(5), 322–332. https://doi.org/10.1097/FBP.0000000000000680

Pascual, M., Blanco, A. M., Cauli, O., Miñarro, J. y Guerri, C. (2007). Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. European Journal of Neuroscience, 25(2), 541–550. https://doi.org/10.1111/j.1460-9568.2006.05298.x

Pascual, M., Pla, A., Miñarro, J. y Guerri, C. (2014). Neuroimmune activation and myelin changes in adolescent rats exposed to high-dose alcohol and associated cognitive dysfunction: A review with reference to human adolescent drinking. Alcohol, 49(2), 187–192. https://doi.org/10.1093/alcalc/agt164

Patrick, M. E., Evans-Polce, R. J., Parks, M. J. y Terry-McElrath, Y. M. (2021). Drinking intensity at age 29/30 as a predictor of alcohol use disorder symptoms at age 35 in a national sample. Journal of Studies on Alcohol and Drugs, 82(6), 740–748. https://doi.org/10.15288/jsad.2021.82.740

Pavlova, I. V., Broshevitskaya, N. D., Onufriev, M. V. y Moiseeva, Y. V. (2020). Sex-related differences in anxious-depressive and defensive behavior in Wistar rats. Neuroscience and Behavioral Physiology, 50(9), 1163–1175. https://doi.org/10.1007/s11055-020-01028-4

Pellow, S., Chopin, P., File, S. E. y Briley, M. (1985). Validation of open: Closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, 14(3), 149–167. https://doi.org/10.1016/0165-0270(85)90031-7

Penta, P. T., Villarreal, S., Rameas, C. I., Collins, E. C., Towner, T. T., Varlinskaya, E. I. y Werner, D. F. (2024). Sex-dependent effects of ethanol withdrawal from a single- and repeated binge episode exposures on social anxiety-like behavior and neuropeptide gene expression in adolescent rats. Alcohol. https://doi.org/10.1016/j.alcohol.2024.10.001

Porsolt, R. D., Le Pichon, M. y Jalfre, M. (1977). Depression: A new animal model sensitive to antidepressant treatments. Nature, 266(5604), 730–732. https://doi.org/10.1038/266730a0

Qi, X., Zhang, K., Xu, T., Yamaki, V. N., Wei, Z., Huang, M., Rose, G. M. y Cai, X. (2016). Sex differences in long-term potentiation at temporoammonic-CA1 synapses: Potential implications for memory consolidation. PLoS ONE, 11(11), e0165891. https://doi.org/10.1371/journal.pone.0165891

Rath, M., Guergues, J., Pinho, J. P. C., Zhang, P., Nguyen, T. G., MacFadyen, K. A., Peris, J., McLaughlin, J. P., Stevens, S. M. y Liu, B. (2020). Chronic voluntary binge ethanol consumption causes sex-specific differences in microglial signaling pathways and withdrawal-associated behaviors in mice. Alcoholism: Clinical and Experimental Research, 44(9), 1791–1806. https://doi.org/10.1111/acer.14420

Rendeiro, C., Spencer, J. P. E., Vauzour, D., Butler, L. T., Ellis, J. A. y Williams, C. M. (2009). The impact of flavonoids on spatial memory in rodents: From behaviour to underlying hippocampal mechanisms. Genes & Nutrition, 4(4), 251–270. https://doi.org/10.1007/s12263-009-0134-6

Rivera-Irizarry, J. K., Zallar, L. J., Levine, O. B., Skelly, M. J., Boyce, J. E., Barney, T., Kopyto, R. y Pleil, K. E. (2023). Sex differences in binge alcohol drinking and the behavioral consequences of protracted abstinence in C57BL/6J mice. Biology of Sex Differences, 14, 65. https://doi.org/10.1186/s13293-023-00565-0

Rodríguez-González, A., Vitali, F., Moya, M., De Filippo, C., Passani, M. B. y Orio, L. (2021). Effects of alcohol binge drinking and oleoylethanolamide pretreatment in the gut microbiota. Frontiers in Cellular and Infection Microbiology, 11, 731910. https://doi.org/10.3389/fcimb.2021.731910

Rodríguez-González, A. y Orio, L. (2020). Microbiota and alcohol use disorder: Are psychobiotics a novel therapeutic strategy? Current Pharmaceutical Design, 26(20), 2426–2437. https://doi.org/10.2174/1381612826666200122153541

Rodríguez-González, A., Moya, M., Rodríguez de Fonseca, F., Gómez de Heras, R. y Orio, L. (2023). Alcohol binge drinking induces downregulation of blood-brain barrier proteins in the rat frontal cortex—but not in the hippocampus—that is not prevented by OEA pretreatment. Advances in Drug and Alcohol Research, 3, 11091. https://doi.org/10.3389/adar.2023.11091

Sanz-Martos, A. B., Fuentes-Verdugo, E., Merino, B., Morales, L., Pérez, V., Capellán, R., Pellón, R., Miguéns, M. y del Olmo, N. (2023). Schedule-induced alcohol intake during adolescence sex dependently impairs hippocampal synaptic plasticity and spatial memory. Behavioural Brain Research, 452, 114576. https://doi.org/10.1016/j.bbr.2023.114576

Sayd, A., Antón, M., Alén, F., Caso, J. R., Pavón, J., Leza, J. C., De Fonseca, F. R., García-Bueno, B. y Orio, L. (2015). Systemic administration of oleoylethanolamide protects from neuroinflammation and anhedonia induced by LPS in rats. International Journal of Neuropsychopharmacology, 18(6), 1–14. https://doi.org/10.1093/ijnp/pyu111

Scheggi, S., De Montis, M. G. y Gambarana, C. (2018). Making sense of rodent models of anhedonia. International Journal of Neuropsychopharmacology, 21(11), 1049–1065. https://doi.org/10.1093/ijnp/pyy083

Scholl, J. L., Afzal, A., Fox, L. C., Watt, M. J. y Forster, G. L. (2019). Sex differences in anxiety-like behaviors in rats. Physiology and Behavior, 211, 112670. https://doi.org/10.1016/j.physbeh.2019.112670

Shansky, R. M. (2018). Sex differences in behavioral strategies: Avoiding interpretational pitfalls. Current Opinion in Neurobiology, 49, 95–98. https://doi.org/10.1016/j.conb.2018.01.007

Shirazi, T. N., Levenberg, K., Cunningham, H., Self, H., Dawood, K., Cárdenas, R., Ortiz, T. L., Carré, J. M., Breedlove, S. M. y Puts, D. A. (2021). Relationships between ovarian hormone concentrations and mental rotations performance in naturally-cycling women. Hormones and Behavior, 127, 104886. https://doi.org/10.1016/j.yhbeh.2020.104886

Sicher, A. R., Duerr, A., Starnes, W. D. y Crowley, N. A. (2022). Adolescent alcohol and stress exposure rewires key cortical neurocircuitry. Frontiers in Neuroscience, 16, 896880. https://doi.org/10.3389/fnins.2022.896880

Simon, F. R., Fortune, J., Iwahashi, M., Sutherland, E. y Simon, F. R. (2002). Sexual dimorphic expression of ADH in rat liver: Importance of the hypothalamic-pituitary-liver axis. American Journal of Physiology-Gastrointestinal and Liver Physiology, 283, 646–655. https://doi.org/10.1152/ajpgi.00438.2001

Sircar, R. (2019). Estrogen modulates ethanol-induced memory deficit in postpubertal adolescent rats. Alcoholism: Clinical and Experimental Research, 43(1), 61–68. https://doi.org/10.1111/acer.13921

Slattery, D. A. y Cryan, J. F. (2012). Using the rat forced swim test to assess antidepressant-like activity in rodents. Nature Protocols, 7(6), 1009–1014. https://doi.org/10.1038/nprot.2012.044

Slattery, D. A., Markou, A. y Cryan, J. F. (2007). Evaluation of reward processes in an animal model of depression. Psychopharmacology, 190(4), 555–568. https://doi.org/10.1007/s00213-006-0630-x

Spear, L. P. (2018). Effects of adolescent alcohol consumption on the brain and behaviour. Nature Reviews Neuroscience, 19(4), 197–214. https://doi.org/10.1038/nrn.2018.10

Thomasson, H. R. (2002). Gender differences in alcohol metabolism. In Recent Developments in Alcoholism (Vol. 12, pp. 163–179). Springer US. https://doi.org/10.1007/0-306-47138-8_9

van Goethem, N. P., Rutten, K., van der Staay, F. J., Jans, L. A. W., Akkerman, S., Steinbusch, H. W. M., Blokland, A., van’t Klooster, J. y Prickaerts, J. (2012). Object recognition testing: Rodent species, strains, housing conditions, and estrous cycle. Behavioural Brain Research, 232(2), 323–334. https://doi.org/10.1016/j.bbr.2012.03.023

Van Hees, L., Didone, V., Charlet-Briart, M., Van Ingelgom, T., Alexandre, A., Quertemont, E., Nguyen, L. y Laguesse, S. (2022). Voluntary alcohol binge-drinking in adolescent C57Bl6 mice induces delayed appearance of behavioural defects in both males and females. Addiction Biology, 27(1), e13102. https://doi.org/10.1111/adb.13102

Varlinskaya, E. I., Hosová, D., Towner, T., Werner, D. F. y Spear, L. P. (2020). Effects of chronic intermittent ethanol exposure during early and late adolescence on anxiety-like behaviors and behavioral flexibility in adulthood. Behavioural Brain Research, 378, 112292. https://doi.org/10.1016/j.bbr.2019.112292

Vijayakumar, N., Op de Macks, Z., Shirtcliff, E. A. y Pfeifer, J. H. (2018). Puberty and the human brain: Insights into adolescent development. Neuroscience and Biobehavioral Reviews, 92, 417–436. https://doi.org/10.1016/j.neubiorev.2018.06.004

Vorhees, C. V. y Williams, M. T. (2006). Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nature Protocols, 1(2), 848–858. https://doi.org/10.1038/nprot.2006.116

Walker, B. M., Drimmer, D. A., Walker, J. L., Liu, T., Mathé, A. A. y Ehlers, C. L. (2010). Effects of prolonged ethanol vapor exposure on forced swim behavior, and neuropeptide Y and corticotropin-releasing factor levels in rat brains. Alcohol, 44(6), 487–493. https://doi.org/10.1016/j.alcohol.2010.04.003

Waszkiewicz, N., Galińska-Skok, B., Nestsiarovich, A., Kułak-Bejda, A., Wilczyńska, K., Simonienko, K., Kwiatkowski, M. y Konarzewska, B. (2018). Neurobiological effects of binge drinking help in its detection and differential diagnosis from alcohol dependence. Disease Markers, 2018, 5623683. https://doi.org/10.1155/2018/5623683

World Health Organization. (2024). Global status report on alcohol and health and treatment of substance use disorders.

World Health Organization. (1948). Constitution of the World Health Organization. Alcohol. https://www.who.int/news-room/fact-sheets/detail/alcohol

Xia, J., Wang, H., Zhang, C., Liu, B., Li, Y., Li, K., Li, P. y Song, C. (2023). The comparison of sex differences in depression-like behaviors and neuroinflammatory changes in a rat model of depression induced by chronic stress. Frontiers in Behavioral Neuroscience, 16. https://doi.org/10.3389/fnbeh.2022.1059594

Yankelevitch-Yahav, R., Franko, M., Huly, A. y Doron, R. (2015). The forced swim test as a model of depressive-like behavior. Journal of Visualized Experiments, 2015(97). https://doi.org/10.3791/52587

Zorzo, C., Arias, J. L. y Méndez, M. (2024). Are there sex differences in spatial reference memory in the Morris water maze? A large-sample experimental study. Learning and Behavior, 52(2), 179–190. https://doi.org/10.3758/s13420-023-00598-w

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2025-12-23

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Vol. 37 Núm. 4 (2025)

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