Adolescent Binge Drinking Linked to Abnormal Spatial Working Memory Brain Activation: Differential Gender Effects
Lindsay M. Squeglia
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorAlecia Dager Schweinsburg
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorCarmen Pulido
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorSusan F. Tapert
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorLindsay M. Squeglia
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorAlecia Dager Schweinsburg
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorCarmen Pulido
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorSusan F. Tapert
From the Joint Doctoral Program in Clinical Psychology (LMS), San Diego State University/University of California San Diego, San Diego, California; Department of Psychiatry (ADS), Yale University, New Haven, Connecticut; Department of Psychiatry (CP, SFT), University of California San Diego, San Diego, California; and VA San Diego HealthCare System (SFT), San Diego, California.
Search for more papers by this authorAbstract
Background: Binge drinking is prevalent during adolescence, and its effect on neurocognitive development is of concern. In adult and adolescent populations, heavy substance use has been associated with decrements in cognitive functioning, particularly on tasks of spatial working memory (SWM). Characterizing the gender-specific influences of heavy episodic drinking on SWM may help elucidate the early functional consequences of drinking on adolescent brain functioning.
Methods: Forty binge drinkers (13 females, 27 males) and 55 controls (24 females, 31 males), aged 16 to 19 years, completed neuropsychological testing, substance use interviews, and an SWM task during functional magnetic resonance imaging.
Results: Significant binge drinking status × gender interactions were found (p < 0.05) in 8 brain regions spanning bilateral frontal, anterior cingulate, temporal, and cerebellar cortices. In all regions, female binge drinkers showed less SWM activation than female controls, while male bingers exhibited greater SWM response than male controls. For female binge drinkers, less activation was associated with poorer sustained attention and working memory performances (p < 0.025). For male binge drinkers, greater activation was linked to better spatial performance (p < 0.025).
Conclusion: Binge drinking during adolescence is associated with gender-specific differences in frontal, temporal, and cerebellar brain activation during an SWM task, which in turn relate to cognitive performance. Activation correlates with neuropsychological performance, strengthening the argument that blood oxygen level–dependent activation is affected by alcohol use and is an important indicator of behavioral functioning. Females may be more vulnerable to the neurotoxic effects of heavy alcohol use during adolescence, while males may be more resilient to the deleterious effects of binge drinking. Future longitudinal research will examine the significance of SWM brain activation as an early neurocognitive marker of alcohol impact to the brain on future behaviors, such as driving safety, academic performance, and neuropsychological performance.
References
- Achenbach TM, Rescorla LA (2001) Manual for the ASEBA School-Age Forms & Profiles. University of Vermont, Research Center for Children, Youth, & Families, Burlington, VT.
- Åkerstedt T, Gillberg M (1990) Subjective and objective sleepiness in the active individual. Int J Neurosci 52: 29–37.
- APA (1994) Diagnostic and Statistical Manual of Mental Disorders, 4th ed (DSM-IV). American Psychiatric Association, Washington, DC.
- Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30: 161–173.
- Bava S, Frank LR, McQueeny T, Schweinsburg BC, Schweinsburg AD, Tapert SF (2009) Altered white matter microstructure in adolescent substance users. Psychiatry Res 173: 228–237.
- Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory-2. Psychological Corporation, San Antonio, TX.
- Brown SA, Myers MG, Lippke L, Tapert SF, Stewart DG, Vik PW (1998) Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): a measure of adolescent alcohol and drug involvement. J Stud Alcohol 59: 427–438.
- Caldwell LC, Schweinsburg AD, Nagel BJ, Barlett VC, Brown SA, Tapert SF (2005) Gender and adolescent alcohol use disorders on BOLD (blood oxygen level dependent) response to spatial working memory. Alcohol Alcohol 40: 194–200.
- Casey BJ, Getz S, Galvan A (2008) The adolescent brain. Dev Rev 28: 62–77.
- Chanraud S, Pitel AL, Rohlfing T, Pfefferbaum A, Sullivan EV (2010) Dual tasking and working memory in alcoholism: relation to frontocerebellar circuitry. Neuropsychopharmacology 35: 1868–1878.
- Clark CP, Brown GG, Eyler LT, Drummond SP, Braun DR, Tapert SF (2007) Decreased perfusion in young alcohol-dependent women as compared with age-matched controls. Am J Drug Alcohol Abuse 33: 13–19.
- Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory task. Nature 386: 604–608.
- Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29: 162–173.
-
Cox RW,
Jesmanowicz A (1999) Real-time 3D image registration for functional MRI.
Magn Reson Med
42: 1014–1018.
10.1002/(SICI)1522-2594(199912)42:6<1014::AID-MRM4>3.0.CO;2-F CAS PubMed Web of Science® Google Scholar
- Emanuele NV, LaPaglia N, Steiner JLK, Emanuele MA (2001) Effect of chronic ethanol exposure on female rat reproductive cyclicity and hormone secretion. Alcohol Clin Exp Res 25: 1025–1029.
- Fitzgerald EF (1995) Intoxication Test Evidence. 2nd ed. Clark Boardman Callaghan, Deerfield, IL.
- Frezza M, diPadova C, Pozzato G, Terpin M, Baraona E, Lieber CS (1990) High blood alcohol levels in women: the role of decreased gastric alcohol dehydrogenase activity and first-pass metabolism. N Engl J Med 322: 95–99.
- Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2: 861–863.
- Grant I (1987) Alcohol and the brain: neuropsychological correlates. J Consult Clin Psychol 55: 310–324.
- Hampson E (1995) Spatial cognition in humans: possible modulation by androgens and estrogens. J Psychiatry Neurosci 20: 397–404.
- Hollingshead AB (1965) Two-Factor Index of Social Position. Yale University Press, New Haven, CT.
- Hommer DW, Momenan R, Kaiser E, Rawlings RR (2001) Evidence for a gender–related effect of alcoholism on brain volumes. Am J Psychiatry 158: 198–204.
- Hommer DW, Momenan R, Rawlings R, Ragan P, Williams W, Rio D, Eckardt M (1996) Decreased corpus callosum size among alcoholic women. Arch Neurol 53: 359–363.
- Jacobson R (1986) The contributions of sex and drinking history to the CT brain scan changes in alcoholics. Psychol Med 16: 547–549.
- Johnston LD, O’Malley PM, Bachman JG, Schulenberg JE (2009) Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2008 (NIH Publication No. 09-7401). National Institute on Drug Abuse, Bethesda, MD.
- Kim JH, Kim HJ, Noh HS, Roh GS, Kang SS, Cho GJ, Park SK, Lee BJ, Choi WS (2003) Suppression by ethanol of male reproductive activity. Brain Res 989: 91–98.
- Kimura D (1963) Recurring Figures Test. D. K. Consultants, University of Western Ontario.
- Kindermann SS, Brown GG, Zorrilla LE, Olsen RK, Jeste DV (2004) Spatial working memory among middleaged and older patients with schizophrenia and volunteers using fMRI. Schizophr Res 68: 203–216.
- Lenroot RK, Giedd JN (2010) Sex differences in the adolescent brain. Brain Cogn 72: 46–55.
- Lewis RF (1995) Digit Vigilance Test. Psychological Assessment Resources, Odessa, FL.
- Lezak MD, Howieson DB, Loring DW, Hannay HJ, Fischer JS (2004) Neuropsychological Assessment. 4th ed. Oxford University Press, New York.
- Loring DW, Meador KJ (2003) The Medical College of Georgia (MCG) complex figures: four forms for follow-up, in Handbook of Rey-Osterrieth Complex Figure Usage: Clinical and Research Applications ( J Knight, E Kaplan eds). Psychological Assessment Resources, Odessa, FL.
- Lucas CP, Zhang H, Fisher PW, Shaffer D, Regier DA, Narrow WE, Bourdon K, Dulcan MK, Canino G, Rubio-Stipec M, Lahey BB, Friman P (2001) The DISC Predictive Scales (DPS): efficiently screening for diagnoses. J Am Acad Child Adolesc Psychiatry 40: 443–449.
- Luna B (2009) Developmental changes in cognitive control through adolescence. Adv Child Dev Behav 37: 233–278.
- Mann K, Batra A, Gunthner A, Schroth G (1992) Do women develop alcoholic brain damage more readily than men? Alcohol Clin Exp Res 16: 1052–1056.
- McCarthy G, Blamire AM, Puce A, Nobre AC, Bloch G, Hyder F, Goldman-Rakic P, Shulman RG (1994) Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proc Natl Acad Sci U S A 91: 8690–8694.
- McQueeny T, Schweinsburg BC, Schweinsburg AD, Jacobus J, Bava S, Frank LR, Tapert SF (2009) Altered white matter integrity in adolescent binge drinkers. Alcohol Clin Exp Res 33: 1278–1285.
- Meador KJ, Moore EE, Nichols ME, Abney OL, Taylor HS, Zamrini EY, Loring DW (1993) The role of cholinergic systems in visuospatial processing and memory. J Clin Exp Neuropsychol 15: 832–842.
- Medina KL, McQueeny T, Nagel BJ, Hanson KL, Schweinsburg AD, Tapert SF (2008) Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects. Alcohol Clin Exp Res 32: 386–394.
- NIAAA (2004) NIAAA Council approves definition of binge drinking, in NIAAA Newsletter, Vol. 3, 3. Office of Research Translation and Communications, NIAAA, NIH, DHHS, Bethesda, MD.
- Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolescence 17(2): 117–133.
- Pfefferbaum A, Desmond JE, Galloway C, Menon V, Glover GH, Sullivan EV (2001a) Reorganization of frontal systems used by alcoholics for spatial working memory: an fMRI study. NeuroImage 14(1 Pt 1): 7–20.
- Pfefferbaum A, Rosenbloom M, Deshmukh A, Sullivan EV (2001b) Sex differences in the effects of alcohol on brain structure. Am J Psychiatry 158: 188–197.
- Pfefferbaum A, Rosenbloom M, Rohlfing T, Sullivan EV (2009) Degradation of association and projection white matter systems in alcoholism detected with quantitative fiber tracking. Biol Psychiatry 65: 680–690.
- Pfefferbaum A, Sullivan EV, Hedehus M, Adalsteinsson E, Lim KO, Moseley M (2000) In vivo detection and functional correlates of white matter microstructural disruption in chronic alcoholism. Alcohol Clin Exp Res 24: 1214–1221.
- Rey A, Osterrieth PA (1993) Translations of excerpts from Andre Rey’s “Psychological examination of traumatic encephalopathy” and P.A. Osterrieth’s “The complex figure copy test” (J. Corwin & F. W. Bylsma, Trans.). Clin Neuropsychol 7: 3–21.
- Rice JP, Reich T, Bucholz KK, Neuman RJ, Fishman R, Rochberg N, Hesselbrock VM, Nurnberger JI Jr, Schuckit MA, Begleiter H (1995) Comparison of direct interview and family history diagnoses of alcohol dependence. Alcohol Clin Exp Res 19: 1018–1023.
- Schweinsburg AD, Nagel BJ, Tapert SF (2005) fMRI reveals alteration of spatial working memory networks across adolescence. J Int Neuropsychol Soc 11: 631–644.
- Sobell LC, Sobell MB (1992) Timeline Follow-back: a technique for assessing self-reported ethanol consumption, in Measuring Alcohol Consumption: Psychosocial and Biological Methods ( J Allen, RZ Litten eds), pp 41–72. Humana Press, Totowa, NJ.
- Spear LP (2009) The Behavioral Neuroscience of Adolescence. 1st ed. W. W. Norton & Co Inc., New York, NY.
- Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto, CA.
- Squeglia LM, Spadoni AD, Infante MA, Myers MG, Tapert SF (2009) Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys. Psychol Addict Behav 23: 715–722.
- Sullivan EV, Pfefferbaum A (2005) Neurocircuitry in alcoholism: a substrate of disruption and repair. Psychopharmacology 180: 583–594.
- Talairach J, Tournoux P (1988) Coplanar Stereotaxic Atlas of the Human Brain. Three-Dimensional Proportional System: An Approach to Cerebral Imaging. Thieme, New York, NY.
- Tapert SF, Baratta MV, Abrantes AM, Brown SA (2002) Attention dysfunction predicts substance involvement in community youth. J Am Acad Child Adolesc Psychiatry 41: 680–686.
- Tapert SF, Brown GG, Kindermann SS, Cheung EH, Frank LR, Brown SA (2001) fMRI measurement of brain dysfunction in alcohol-dependent young women. Alcohol Clin Exp Res 25: 236–245.
- Tapert SF, Brown SA (1999) Neuropsychological correlates of adolescent substance abuse: four-year outcomes. J Int Neuropsychol Soc 5: 481–493.
- Tapert SF, Schweinsburg AD, Barlett VC, Brown SA, Frank LR, Brown GG, Meloy MJ (2004) Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcohol Clin Exp Res 28: 1577–1586.
- Tapert SF, Schweinsburg AD, Drummond SPA, Paulus MP, Brown SA, Yang TT, Frank LR (2007) Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology 194: 173–184.
- Taylor LB (1969) Localisation of cerebral lesions by psychological testing. Clin Neurosurg 16: 269–287.
- Vuontela V, Steenari MR, Carlson S, Koivisto J, Fjallberg M, Aronen ET (2003) Audiospatial and visuospatial working memory in 6–13 year old school children. Learn Mem 10: 74–81.
- Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3: 255–274.
- Ward BD (2000) Simultaneous inference for fMRI data. Available at: http://afni.nimh.nih.gov/afni/doc/manual/AlphaSim. Accessed March 23, 2009.
- Wechsler D (1997) Wechsler Adult Intelligence Scale. 3rd ed. The Psychological Corporation, San Antonio, TX.
- Wechsler D (1999) Manual for the Wechsler Abbreviated Scale of Intelligence. Psychological Corporation, San Antonio, TX.
- Wechsler H, Davenport A, Dowdall G, Moeykens B, Castillo S (1994) Health and behavioral consequences of binge drinking in college. A national survey of students at 140 campuses. J Am Med Assoc 272: 1672–1677.
- Wechsler H, Dowdall GW, Davenport A, Rimm EB (1995) A gender-specific measure of binge drinking among college students. Am J Public Health 85: 982–985.
- Wechsler H, Isaac N (1992) ‘Binge’ drinkers at Massachusetts colleges. Prevalence, drinking style, time trends, and associated problems. J Am Med Assoc 267: 2929–2931.
- Widmark E (1922) A micromethod for the estimation of alcohol in blood. Biochemistry 131: 473–484.
- Wilkinson GS (1993) WRAT-3: Wide Range Achievement Test Administration Manual. 3rd ed. Western Psychological Services, Wilmington, DE.
- Williams CL, Meck WH (1991) The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16: 155–176.
- Zucker RA, Ellis DA, Fitzgerald HE (1994) Developmental evidence for at least two alcoholisms: I. Biopyschosocial variation among pathways into symptomatic difficulty, in Types of Alcoholics: Evidence from Clinical, Experimental and Genetic Research ( TF Babor, V Hesselbrock, RE Meyer, W Shoemaker eds), pp 134–146. The New York Academy of Sciences, New York.