Binge drinking during adolescence and young adulthood is associated with deficits in verbal episodic memory

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Carbia, Carina ^a   Cadaveira, Fernando ^a   Caamaño Isorna, Francisco ^a   Rodríguez Holguín, Socorro ^a   Corral, Montse ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CANNABIS;

ADULT; ARTICLE; BINGE DRINKING; CANNABIS USE; CONTROLLED STUDY; DISTRESS SYNDROME; EPISODIC MEMORY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MEMORY DISORDER; ONSET AGE; REY AUDITORY VERBAL LEARNING TEST; RISK FACTOR; SHORT TERM MEMORY; TOBACCO USE; VERBAL MEMORY; ADOLESCENT; ADVERSE EFFECTS; ALCOHOLIC BEVERAGE; CHEMICALLY INDUCED; COMPLICATION; DRUG EFFECTS; NEUROPSYCHOLOGICAL TEST; RECALL; YOUNG ADULT;

ADOLESCENT; ALCOHOLIC BEVERAGES; BINGE DRINKING; FEMALE; HUMANS; MALE; MEMORY DISORDERS; MEMORY, EPISODIC; MENTAL RECALL; NEUROPSYCHOLOGICAL TESTS; YOUNG ADULT;

EID: 85011347213     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171393     Document Type: Article

References (80)

1. Marshall EJ. Adolescent alcohol use: Risks and consequences. Alcohol Alcohol. 2014; 49(2): 160-164. doi:10.1093/alcalc/agt180 PMID: 24402246.
2. Substance Abuse and Mental Health Services Administration Results from the 2012 National Survey on Drug Use and Health: Summary of National Findings, NSDUH Series H-46, HHS. Rockville, MD: Substance Abuse and Mental Health Services Administration. 2013. Publication No. (SMA) 13-4795.
3. National Institute of Alcohol Abuse and Alcoholism. NIAAA council approves definition of binge drinking. NIAAA Newsletter, p. 3. 2004. Available from: http://pubs.niaaa.nih.gov/publications/Newsletter/winter2004/Newsletter-Number3.pdf.
4. Kuntsche E, & Gmel G. Alcohol consumption in late adolescence and early adulthood-where is the problem. Swiss Med Wkly. 2013; 143: W13826. doi:10.4414/smw.2013.13826 PMID: 23888405.
5. Spear LP. Adolescent neurodevelopment. J Adolesc Health Care. 2013; 52(2): S7-S13.
6. Bava S, & Tapert SF. Adolescent brain development and the risk for alcohol and other drug problems. Neuropsychol Rev. 2010; 20(4): 398-413. doi:10.1007/s11065-010-9146-6 PMID: 20953990.
7. Nixon K, & McClain JA. Adolescence as a critical window for developing an alcohol use disorder: current findings in neuroscience. Curr Opin Psychiatry. 2010; 23(3): 227. doi:10.1097/YCO.0b013e32833864fe PMID: 20224404.
8. Crews F, He J, & Hodge C. Adolescent cortical development: A critical period of vulnerability for addiction. Pharmacol Biochem Behav. 2007; 86(2): 189-199. doi:10.1016/j.pbb.2006.12.001 PMID: 17222895.
9. Squeglia LM, & Gray KM. (2016). Alcohol and drug use and the developing brain. Curr Psychiatry Rep. 2016; 18(5): 1-10.
10. Crews FT, Braun CJ., Hoplight B, Switzer RC, & Knapp DJ. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Re. 2000; 24: 1712-1723.
11. Guerri C, & Pascual M. Mechanisms involved in the neurotoxic, cognitive, and neurobehavioral effects of alcohol consumption during adolescence. Alcohol. 2010; 44: 15-26. doi:10.1016/j.alcohol.2009.10.003 PMID: 20113871.
12. Oscar-Berman M, & Marinković K. Alcohol: Effects on neurobehavioral functions and the brain. Neuropsychol Rev. 2007; 17(3): 239-257. doi:10.1007/s11065-007-9038-6 PMID: 17874302.
13. Silveri MM, Dager AD, Cohen-Gilbert JE, & Sneider JT. Neurobiological signatures associated with alcohol and drug use in the human adolescent brain. Neurosci Biobehav Rev. 2016; 70:244-259. doi:10.1016/j.neubiorev.2016.06.042 PMID: 27377691.
14. Pascual M, Pla A, Miñarro J, & Guerri C. 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 Alcohol. 2014; 49(2): 187-192. doi:10.1093/alcalc/agt164 PMID: 24217958.
15. Vargas WM, Bengston L, Gilpin NW, Whitcomb BW, & Richardson HN. Alcohol Binge Drinking during Adolescence or Dependence during Adulthood Reduces Prefrontal Myelin in Male Rats. J Neurosci. 2014; 34(44): 14777-14782. doi:10.1523/JNEUROSCI.3189-13.2014 PMID: 25355229.
16. Squeglia LM, Sorg SF, Schweinsburg AD, Wetherill RR, Pulido C, & Tapert SF. Binge drinking differentially affects adolescent male and female brain morphometry. Psychopharmacology. 2012; 220(3): 529-539. doi:10.1007/s00213-011-2500-4 PMID: 21952669.
17. Doallo S, Cadaveira F, Corral M, Mota N, LoÂpez-Caneda E, & Rodrõâguez Holguõân S. Larger mid-dorsolateral prefrontal gray matter volume in young binge drinkers revealed by voxel-based morphometry. PLoS ONE. 2014; 9(5).
18. Parada M., Corral M., Mota N., Crego A., RodrõÂguez Holguõân S., & Cadaveira F. Executive functioning and alcohol binge drinking in university students. Addict Behav. 2012; 37(2): 167-172. doi:10.1016/j.addbeh.2011.09.015 PMID: 21996093.
19. Salas-Gomez D, Fernandez-Gorgojo M, Pozueta A, Diaz-Ceballos I, Lamarain M, Perez C, & Sanchez- Juan P. Binge drinking in young university students is associated with alterations in executive functions related to their starting age. PLoS ONE. 2016; 11(11).
20. Scaife JC, & Duka T. Behavioural measures of frontal lobe function in a population of young social drinkers with binge drinking pattern. Pharmacol Biochem Behav. 2009; 93(3): 354-362. doi:10.1016/j.pbb.2009.05.015 PMID: 19497334.
21. Broadwater MA, Liu W, Crews FT., & Spear LP. Persistent loss of hippocampal neurogenesis and increased cell death following adolescent, but not adult, chronic ethanol exposure. Developmental Neuroscience. 2014; 36(0): 297-305.
22. Oliveira AC, Pereira MC, Santana LN, Fernandes RM, Teixeira FB, Oliveira GB, et al. Chronic ethanol exposure during adolescence through early adulthood in female rats induces emotional and memory deficits associated with morphological and molecular alterations in hippocampus. J Psychopharmacol. 2015; 29(6): 712-24. doi:10.1177/0269881115581960 PMID: 25922423.
23. Vetreno RP, & Crews FT. Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning. Front Neurosci. 2015; 9: 35. doi:10.3389/fnins.2015.00035 PMID: 25729346.
24. White AM, Matthews DB, & Best PJ. Ethanol, memory, and hippocampal function: A review of recent findings. Hippocampus. 2000; 10(1): 88-93. doi:10.1002/(SICI)1098-1063(2000)10:1<88::AIDHIPO10>3.0.CO;2-L PMID: 10706220.
25. Bernardin F, Maheut-Bosser A, & Paille F. Cognitive Impairments in Alcohol-Dependent Subjects. Front Psychiatry. 2014; 5: 78. doi:10.3389/fpsyt.2014.00078 PMID: 25076914.
26. De Bellis MD, Clark DB, Beers SR, Soloff PH, Boring AM, Hall J, et al. Hippocampal volume in adolescent- onset alcohol use disorders. Am J Psychiatry. 2000; 157(5): 737-744. doi:10.1176/appi.ajp.157.5.737 PMID: 10784466.
27. Medina KL., Schweinsburg AD, Cohen-Zion M, Nagel BJ, & Tapert SF. Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicol Teratol. 2007; 29(1): 141-152. doi:10.1016/j.ntt.2006.10.010 PMID: 17169528.
28. Nagel BJ, Schweinsburg AD, Phan V, & Tapert SF. Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res. Neuroimaging. 2005; 139 (3): 181-190. doi:10.1016/j.pscychresns.2005.05.008 PMID: 16054344.
29. Brown SA, Tapert SF, Granholm E, & Delis DC. Neurocognitive functioning of adolescents: Effects of protracted alcohol use. Alcohol Clin Exp Res. 2000; 24(2): 164-171. PMID: 10698367.
30. Brown SA, & Tapert SF. Adolescence and the trajectory of alcohol use: basic to clinical studies. Ann N Y Acad Sci. 2004; 1021(1): 234-244.
31. Simons JS, & Spiers HJ. Prefrontal and medial temporal lobe interactions in long-Term memory. Nat Rev Neurosci. 2003; 4(8): 637-648. doi:10.1038/nrn1178 PMID: 12894239.
32. Moscovitch M, Cabeza R, Winocur G, & Nadel L. Episodic memory and beyond: The hippocampus and neocortex in transformation. Annu Rev Psychol. 2016; 67: 105-134. doi:10.1146/annurev-psych-113011-143733 PMID: 26726963.
33. Shing YL, Werkle-Bergner M, Brehmer Y, Muè ller V, Li SC and Lindenberger U. Episodic memory across the lifespan: The contributions of associative and strategic components. Neurosci Biobehav Rev. 2010; 34(7): 1080-1091. doi:10.1016/j.neubiorev.2009.11.002 PMID: 19896974.
34. Sneider JT, Cohen-Gilbert JE., Crowley DJ, Paul MD, & Silveri MM. Differential effects of binge drinking on learning and memory in emerging adults. J Addict Res Ther. 2013; Suppl 7.
35. Garcõâa-Moreno LM, Expo sito J, Sanhueza C, & Angulo MT. Actividad prefrontal y alcoholismo de fin de semana en joÂvenes. Adicciones. 2008; 20(3): 271-279. PMID: 18813773.
36. Garcõâa-Moreno LM, Expoâsito J, Sanhueza C, & Gil S. Rendimiento cognitivo y consumo de alcohol durante los fines de semana en mujeres adolescentes. Revista Neuropsicologõâa, Neuropsiquiatrõâa y Neurociencias. 2009; 9: 75-91.
37. Sanhueza C, Garcõâa-Moreno LM, & Expoâsito J. Weekend alcoholism in youth and neurocognitive aging. Psicothema. 2011; 23: 209-214. PMID: 21504671.
38. Parada M, Corral M, Caamaño-Isorna F, Mota N, Crego A, Holguõân SR, et al. Binge drinking and declarative memory in university students. Alcohol Clin Exp Re. 2011; 35(8): 1475-1484.
39. Mota N, Parada M, Crego A, Doallo S, Caamaño-Isorna F, Rodrõâguez Holguõân S, et al. Binge drinking trajectory and neuropsychological functioning among university students: A longitudinal study. Drug Alcohol Depend. 2013; 133(1): 108-114. doi:10.1016/j.drugalcdep.2013.05.024 PMID: 23791027.
40. Gershberg FB, & Shimamura AP. Impaired use of organizational strategies in free recall following frontal lobe damage. Neuropsychologia. 1995; 33(10): 1305-1333. PMID: 8552230.
41. Stuss DT, Alexander MP, Palumbo CL, Buckle L, Sayer L, & Pogue J. Organizational strategies with unilateral or bilateral frontal lobe injury in word learning tasks. Neuropsychology. 1994; 8(3): 355-373.
42. Frisk V, & Milner B. The role of the left hippocampal region in the acquisition and retention of story content. Neuropsychologia. 1990; 28(4): 349-359. PMID: 2111523.
43. Sawrie SM, Martin RC, Gilliam F, Knowlton R, Faught E, & Kuzniecky R. Verbal retention lateralizes patients with unilateral temporal lobe epilepsy and bilateral hippocampal atrophy. Epilepsia. 2001; 42 (5): 651-659. PMID: 11380574.
44. Baldo JV, Delis D, Kramer J, & Shimamura AP. Memory performance on the California Verbal Learning Test-II: Findings from patients with focal frontal lesions. J Int Neuropsychol Soc. 2002; 8(04): 539-546.
45. Consonni M, Rossi S, Cerami C, Marcone A, Iannaccone S, Francesco Cappa S, & Perani D. Executive dysfunction affects word list recall performance: Evidence from amyotrophic lateral sclerosis and other neurodegenerative diseases. J Neuropsychol. 2015.
46. Hirst W, Volpe BT. Memory strategies with brain damage. Brain Cogn. 1988; 8(3):379-408. PMID: 3214591.
47. Brooks BL, Weaver LE, & Scialfa CT. Does impaired executive functioning differentially impact verbal memory measures in older adults with suspected dementia?. Clin Neuropsychol. 2006; 20(2): 230- 242. doi:10.1080/13854040590947461 PMID: 16690544.
48. Tremont G, Halpert S, Javorsky DJ, & Stern RA. Differential impact of executive dysfunction on verbal list learning and story recall. Clin Neuropsychol. 2000; 14(3): 295-302. doi:10.1076/1385-4046(200008)14:3;1-P;FT295 PMID: 11262704.
49. Shimamura AP, Jurica PJ, Mangels JA, Gershberg FB, & Knight RT. Susceptibility to memory interference effects following frontal lobe damage: Findings from tests of paired-Associate learning. J Cognitive Neurosci. 1995; 7(2): 144-152.
50. Alexander MP, Stuss DT, & Fansabedian N. California Verbal Learning Test: performance by patients with focal frontal and non-frontal lesions. Brain. 2003; 126(6): 1493-1503.
51. Lundervold AJ, Halleland HB, Brevik EJ, Haavik J, & Sørensen L. Verbal Memory Function in Intellectually Well-Functioning Adults With ADHD Relations to Working Memory and Response Inhibition. J Atten Disord. 2015.
52. Rouleau I, Imbault H, Laframboise M, & Bedard MA. Pattern of intrusions in verbal recall: comparison of Alzheimer's disease, Parkinson's disease, and frontal lobe dementia. Brain Cogn. 2001; 46(1); 244- 249.
53. Lezak MD. Neuropsychological assessment. USA: Oxford University Press; 2004.
54. Mitrushina M, Boone KB, Razani J, & Delia LF. Handbook of normative data for neuropsychological assessment. Oxford University Press; 2005.
55. Woodard JL, Goldstein FC, Roberts VJ, & McGuire C. Convergent and discriminant validity of the CVLT (dementia version). J Clin Exp Neuropsychol. 1999; 21(4): 553-558. doi:10.1076/jcen.21.4.553.878 PMID: 10550812.
56. Hanson KL, Cummins K, Tapert SF, & Brown SA. Changes in neuropsychological functioning over 10 years following adolescent substance abuse treatment. Psychol Addict Behav. 2011; 25(1): 127-142. doi:10.1037/a0022350PMID: 21443308.
57. Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG. AUDIT. The Alcohol Use Disorders Identification Test. Guidelines for Use in Primary Health Care, 2nd ed. Geneva: World Health Organization; 2001.
58. Caamaño-Isorna F, Corral M, Parada M, & Cadaveira F. Factors associated with risky consumption and heavy episodic drinking among Spanish university students. J Stud Alcohol Drugs. 2008; 69(2): 308- 312. PMID: 18299773.
59. Degoratis LR. SCL-90-R. Administration, scoring and procedures manual II for the revised version of the SCL-90-R. Baltimore: John Hopkins University Press; 1983.
60. Wechsler D. Wechsler Adult Intelligence Scale-III., San Antonio: The Psychological Corporation; 1997.
61. Rey A. L'examen clinique en psychologie. Paris: Presses Universitaires de France; 1964.
62. Wechsler D. Wechsler Memory Scale-III. San Antonio: The Psychological Corporation, 1997.
63. Brown H., & Prescott R. Applied mixed models in medicine. 2nd ed. New York: John Wiley & Sons; 2014.
64. Bates D, Maechler M, Bolker B, & Walker S. -lme4: Linear mixed-effects models using Eigen and S4-. R package version 1.1-7.2014, .
65. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2015 URL http://www.R-project.org/.
66. Gibbons RD, Hedeker D, & DuToit S. Advances in analysis of longitudinal data. Annu Rev Clin Psychol. 2010; 6: 79-107. doi:10.1146/annurev.clinpsy.032408.153550 PMID: 20192796.
67. Hartley DE, Elsabagha S, & File SE. Binge drinking and sex: Effects on mood and cognitive function in healthy young volunteers. Pharmacol Biochem Behav. 2004; 78, 611-619. doi:10.1016/j.pbb.2004.04.027 PMID: 15251270.
68. Nguyen-Louie TT, Tracas A, Squeglia L, M Matt GE, Eberson-Shumate S, & Tapert SF. Learning and memory in adolescent moderate, binge, and extreme-binge drinkers. Alcohol Clin Exp Re. 2016; 40(9): 1895-1904.
69. Buèhler M, & Mann K. Alcohol and the human brain: A systematic review of different neuroimaging methods. Alcohol Clin Exp Res. 2011; 35(10): 1771-1793. doi:10.1111/j.1530-0277.2011.01540.x PMID: 21777260.
70. Howell NA, Worbe Y, Lange I, Tait R, Irvine M, Banca P, et al. Increased ventral striatal volume in college-Aged binge drinkers. PloS One. 2013; 8(9): E74164. doi:10.1371/journal.pone.0074164 PMID: 24086317.
71. Ferrett HL, Carey PD, Thomas KG., Tapert SF, and Fein G. Neuropsychological performance of South African treatment-naive adolescents with alcohol dependence. Drug Alcohol Depend. 2010; 110(1): 8- 14.
72. Morris SA., Eaves DW, Smith AR., & Nixon K. Alcohol inhibition of neurogenesis: A mechanism of hippocampal neurodegeneration in an adolescent alcohol abuse model. Hippocampus. 2010; 20(5): 596- 607. doi:10.1002/hipo.20665 PMID: 19554644.
73. Nixon K, Morris SA, Liput DJ, & Kelso ML. Roles of neural stem cells and adult neurogenesis in adolescent alcohol use disorders. Alcohol. 2010; 44(1): 39-56. doi:10.1016/j.alcohol.2009.11.001 PMID: 20113873.
74. Crews FT, Mdzinarishvili A, Kim D, He J, & Nixon K. Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience. 2006; 137(2): 437-445. doi:10.1016/j.neuroscience.2005.08.090 PMID: 16289890.
75. He J, & Crews FT. Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav. 2007; 86(2): 327-333. doi:10.1016/j.pbb.2006.11.003 PMID: 17169417.
76. White AM, & Swartzwelder HS. Hippocampal function during adolescence: A unique target of ethanol effects. Ann N Y Acad Sci. 2004; 1021(1): 206-220.
77. Taffe MA, Kotzebue RW, Crean RD, Crawford EF, Edwards S, & Mandyam CD. Long-lasting reduction in hippocampal neurogenesis by alcohol consumption in adolescent nonhuman primates. Proc Natl Acad Sci. 2010; 107(24): 11104-11109. doi:10.1073/pnas.0912810107 PMID: 20534463.
78. Chin VS, Van Skike CE, & Matthews DB. Effects of ethanol on hippocampal function during adolescence: A look at the past and thoughts on the future. Alcohol. 2010; 44(1): 3-14. doi:10.1016/j.alcohol.2009.10.015 PMID: 20113870.
79. Winward JL, Hanson KL, Bekman NM, Tapert SF, & Brown SA. Adolescent heavy episodic drinking: Neurocognitive functioning during early abstinence. J Int Neuropsychol Soc. 2014; 20(2): 218-229. doi:10.1017/S1355617713001410 PMID: 24512674.
80. Hanson KL, Medina KL, Nagel BJ, Spadoni AD, Gorlick A, and Tapert SF. Hippocampal volumes in adolescents with and without a family history of alcoholism. Am J Drug Alcohol Abuse. 2010; 36(3): 161-167. doi:10.3109/00952991003736397 PMID: 20465374.