Executive functioning and alcohol binge drinking in university students

EXECUTIVE FUNCTIONING AND ALCOHOL BINGE DRINKING IN UNIVERSITY STUDENTS Authors: María Parada, Montserrat Corral, Nayara Mota, Alberto Crego, Socorro Rodríguez Holguín, Fernando Cadaveira Department of Clinical Psychology and Psychobiology, University of Santiago de Compostela, Spain This is the peer reviewed version of the following article: Parada M; Corral M; Mota N; Crego A; Rodríguez Holguín S; Cadaveira F (2012). Executive functioning and alcohol binge drinking in university students. Addictive Behaviors, 37, 167–172 doi:10.1016/j.addbeh.2011.09.015. This article may be used for non-commercial purposes in accordance with Elsevier Ltd. Conditions for Use of Self-Archived Versions. 1 Executive functioning and alcohol binge drinking in university students María Parada, Montserrat Corral, Nayara Mota, Alberto Crego, Socorro Rodríguez Holguín, Fernando Cadaveira Department of Clinical Psychology and Psychobiology, University of Santiago de Compostela, Spain Corresponding author: María Parada. Departamento de Psicoloxía Clínica e Psicobioloxía, Facultade de Psicoloxía, Campus Vida, 15782, Santiago de Compostela, Galicia, Spain. Tel.: + 34 981 563100; fax: + 34 981 528071. E-mail address: [email protected] Abstract Background: Binge drinking (BD) is prevalent among college students. Studies on alcoholism have shown that the prefrontal cortex is vulnerable to the neurotoxic effects of alcohol. The prefrontal cortex undergoes both structural and functional changes during adolescence and young adulthood. Sex differences have been observed in brain maturation and in alcohol-induced damage. The objective of the present study was to analyze the relationship between BD and cognitive functions subserved by the prefrontal cortex in male and female university students. Methods: The sample comprised 122 undergraduates (aged 18 to 20 years): 62 BD (30 females) and 60 non-BD (29 females). Executive functions were assessed by WMS-III (Backward Digit Span and Backward Spatial Span), SOPT (abstract designs), Letter Fluency (PMR), BADS (Zoo Map and Key Search) and WCST-3. Results: BD students scored lower in the Backward Digit Span Subtest and generated more perseverative responses in the SOPT In relation to interaction BD by sex, BD males scored lower in the Backward Digit Span test than BD females and non-BD males. Conclusions: BD is associated with poorer performance of executive functions subserved by the dorsolateral prefrontal cortex. The results do not support enhanced vulnerability of women to alcohol neurotoxic effects. These difficulties may reflect developmental delay or frontal lobe dysfunction. Post-print (final draft post-refereeing) 2 Keywords: Binge drinking, Alcohol, University students, Adolescent development, Executive functions, Prefrontal cortex 1. Introduction Binge drinking (BD), or heavy episodic drinking, is becoming increasingly frequent among university students in different countries, even in Mediterranean countries traditionally characterized by regular and moderate alcohol intake (Courtney & Polich, 2009; Vicki, Kuntsche, & Gmel, 2010). BD is characterized by the intake of large amounts of alcohol within a short period and on a few days a week. Several studies have indicated that intermittent alcohol consumption may constitute a greater risk to neurocognitive functioning than regular alcohol consumption (Stephens & Duka, 2008). In addition, the adolescent brain may be more vulnerable to the effects of alcohol because of the extensive neuromaturational processes that occur during adolescence, when significant restructuring of the brain takes place (Casey, Jones, & Hare, 2008; Crews & Boettiger, 2009; Guerri & Pascual, 2010). At a neuropsychological level, adolescence is the period when most complex cognitive abilities are acquired. Significant improvements are observed in executive skills such as planning, problemsolving, working memory and inhibitory control at this stage of development (Conklin, Luciana, Hooper, & Yarger, 2007; Luciana & Nelson, 2002; Luna, Padmanabhan, & O'Hearn, 2010; Rubia et al., 2000; Salatas-Waters, 1982; Welsh, Pennington, & Groisser, 1991). Moreover, it has been suggested that cognitive development throughout adolescence is associated with progressively greater efficiency of cognitive control capacities, which appear to depend on maturation of the prefrontal cortex (Yurgelun-Todd, 2007). This is structurally one of the last cortical regions to reach full development (Blakemore & Choudhury, 2006; Gogtay et al., 2004; Sowell, Thompson, Tessner, & Toga, 2001). Animal studies have shown the sensitivity of the adolescent rat brain to the effects of alcohol. Intermittent administration of ethanol during adolescence induces prefrontal cortex damage (Crews, Braun, Hoplight, Switzer, & Knapp, 2000; Pascual, Blanco, Cauli, Miñarro, & Guerri, 2007), changes in dopaminergic and glutamatergic neurotransmission (Pascual, Boix, Felipo, & Guerri, 2009) and short and long-lasting cognitive and behavioral deficits (Obernier, White, Swartzwelder, & Crews, 2002; Pascual et al., 2007; Schulteis, Archer, Tapert, & Frank, 2008). In humans, it has been found that young people with Alcohol Use Disorder (AUD) have a smaller prefrontal cortex volume and perform less well in neuropsychological attention and working memory tasks than control subjects (De Bellis et al., 2005; Medina et al., 2008; Tapert, Baratta, Abrantes, & Post-print (final draft post-refereeing) 3 Brown, 2002; Tapert & Brown, 1999). Activation of the prefrontal cortex is also lower in subjects suffering from AUD than in control subjects during a working memory task (Caldwell et al., 2005; Tapert et al., 2001; Tapert et al., 2002). To date, few studies have been carried out to investigate the effects of BD on executive functions related to prefrontal cortex in the general adolescent population. Hartley, Elsabagh, and File (2004) compared the neuropsychological performance of 27 university students distributed in two groups according to their pattern of alcohol consumption: 14 BD (who consumed 10 or more alcoholic drinks on a single occasion) and 13 abstainers. BD subjects performed less well in attention and planning tasks. Performance was similar in men and women. In addition, when the BD group was divided on the basis of the amount of alcohol consumed (more than 18 drinks a week and less than 18 drinks a week), both groups performed similarly in the tests, which suggests that the differences between the BD and the abstainers were related to the pattern of alcohol consumption rather than to the amount of alcohol consumed. In a second study (García-Moreno, Expósito, Sanhueza, & Angulo, 2008; García-Moreno, Expósito, Sanhueza, & Gil, 2009) university students were divided into three groups: abstainers, subjects with moderate consumption of 4 or more alcoholic drinks on a single occasion, and subjects with abusive consumption of 5 or more drinks on one occasion. The subjects with a moderate or abusive pattern of alcohol consumption showed poorer performance in tasks related to the dorsolateral prefrontal cortex functioning. Finally, Nederkoorn, Baltus, Guerrieri, and Wiers (2009) evaluated the performance of 64 university students in an adapted version of the Stop Signal Task. The students were classified as light or heavy drinkers according to their alcohol consumption (upper/lower threshold of 11.5 units for females and 12.5 units for males). The authors found no differences in response inhibition between light and heavy drinkers, but heavy drinking females showed stronger response inhibition deficits than other groups. Studies with social drinkers from a wider age group (18–35 years) found that the young social drinkers with a BD pattern of alcohol consumption experienced more difficulties related to visuospatial working memory (Weissenborn & Duka, 2003) and inhibitory control (Townshend & Duka, 2005) than social drinkers who did not follow this pattern of consumption. Binge drinking women performed less well than other groups on visuospatial working memory and flexibility cognitive tasks (Scaife & Duka, 2009; Townshend & Duka, 2005). These results, together with reported by Hartley et al. (2004), show that the difficulties experienced by BD are possibly due to the peaks in consumption rather than to the amounts ingested, and indicate the need for further studies on this topic. Post-print (final draft post-refereeing) 4 In addiction, the impact of other associated risk factors (such as psychiatric comorbility, family history of alcoholism or cannabis consumption) has not controlled in all cases and this may limit the interpretation of results. Finally, only few studies have taken into account sex differences. The issue of increased vulnerability of women to the neurotoxic effects of alcohol is still controversial (Hommer, 2003; Oscar-Berman & Marinkovic, 2007 for reviews). Several studies have reported sex differences in the sensitivity to alcohol-induced brain damage in alcoholics (Acker, 1986; Hommer, Momenan, Kaiser, & Rawlings, 2001; Mann et al., 2005), AUD adolescents (Caldwell et al., 2005; Medina et al., 2008) and young social drinkers (Scaife & Duka, 2009; Townshend & Duka, 2005). However, other studies with alcoholics did not find any such differences (Glenn & Parsons, 1992; Sullivan, Fama, Rosenbloom, & Pfefferbaum, 2002). The first aim of the present study was to investigate the association between BD and executive skills in university students. Because of the important degree of maturation of the dorsolateral prefrontal cortex during adolescence, and taking into account the greater vulnerability of the frontal lobes to the neurotoxic effects of alcohol (Oscar-Berman & Marinkovic, 2007 for review), it is possible that this brain region may be particularly susceptible to damage during adolescence. We hypothesize that BD subjects will perform less well than non-BD subjects in tasks that evaluate functions associated with the dorsolateral prefrontal cortex. Secondly, to determine whether the relationship between BD and cognitive functioning is modulated by sex. Our hypothesis is those females are more vulnerable to neurocognitive effects of BD. 2. Material and methods 2.1. Sample Participants were selected through an anonymous questionnaire administered in-class to first-year students at the University of Santiago de Compostela (Spain) (Caamaño-Isorna, Corral, Parada, & Cadaveira, 2008). The questionnaire included the Galician version of Alcohol Use Disorders Identification Test (AUDIT) (Varela, Braña, Real, & Rial, 2005) and questions related to the use of alcohol (speed of consumption, age of onset on alcohol consumption, etc.). The classification criteria, as detailed in Crego et al. (2010), are based on their responses to two questions: the third question of the AUDIT (How often do you have six or more drinks on a single occasion? Never/Less than monthly/Monthly/Weekly/Daily or almost daily) and one question pertaining to the speed of consumption (drinks per hour). Taking into account that in Spain one SAD contains 10 g of alcohol, the BD group comprised those subjects who consumed 6 or more alcoholic drinks on a single occasion, one or more times per month, and drank 3 or more drinks per hour. The non-BD group was Post-print (final draft post-refereeing) 5 composed of those students who never consumed 6 or more alcoholic drinks on a single occasion or less than once per month and drank 2 or less drinks per hour. Sporadic cannabis users were not excluded from the study. A high correlation between alcohol and cannabis use in adolescents and in university students has been consistently reported (Chun et al., 2010; Degenhardt, Hall, & Lynskey, 2001; Falk, Yi, & Hiller-Sturmhöfel, 2008). Similarly, in the present study the percentage of cannabis users was significantly higher in the BD group than in the non-BD group. The exclusion criteria, assessed through a semi-structured interview, were as follows: a score above 90 in the Global Severity Index (GSI) of the SCL-90-R (Degoratis, 1983) or in at least two of the symptomatic dimensions, personal history of neurological or relevant systemic disease, regular consumption of cannabis or other illegal drugs, alcohol abuse/dependence according to the DSM-IV criteria, personal and/or family history of major mental disorder and history of alcoholism in firstdegree relatives. Finally, 122 participants were selected for neuropsychological assessment: 62 binge drinkers (32 males and 30 females) and 60 non-binge drinkers (31 males and 29 females). The sociodemographic, clinical and alcohol use pattern characteristics are shown in Table 1. Table 1 Participants were asked to abstain from consuming drugs and alcohol within 24 h prior to neuropsychological assessment. All of the individuals signed an informed consent form and received financial compensation for their participation in the study (15€). The evaluation was completed by psychological specialists in neuropsychology who were blind to the participants' condition. 2.2. Material Dorsolateral prefrontal functions were assessed by the following tests: Backward Digit Span (Wechsler Memory Scale-III, WMS-III) (Wechsler, 1997): Sequences of numbers are read out to participants who are asked to repeat them, in reverse order. The numbers are increased in length by one digit from trial to trial; the number of digits in the longest sequence recalled correctly is recorded. This test assesses verbal working memory. Backward Spatial Span (WMS-III) (Wechsler, 1997): The examiner taps cubes in sequences of increasing length, and immediately after participants are required to reproduce each sequence, in reverse order. This test evaluates spatial working memory. The Digit Span Backward and Spatial Span Backward tests are frequently used to assess the executive component of the working memory, which depends on the integrity of a network that includes the Post-print (final draft post-refereeing) 6 dorsolateral prefrontal cortex (Baddeley, 2003). Self-Ordered Pointing Test, abstract design version (SOPT) (Petrides & Milner, 1982): The subject is presented with a booklet consisting of different pages, each of which shows a series of abstract drawings (hard to verbalize designs). The stimuli are repeated on all pages in each test, but the position changes at random from page to page. The task is to point to one design on each page, without repeating previously indicated designs. The test consists of 4 trials with six, eight, ten and twelve stimuli. For each participant, the total number of errors and the perseverative errors (errors that occurred as a result of pointing to the same item that was chosen on the immediately preceding page) are recorded. The SOPT assesses planning and self-monitoring aspects of working memory. The performance is associated with scores on some other measures of executive function and working memory (Ross, Hanouskova, Giarla, Calhoun, & Tucker, 2007). Several investigations including nonhuman primate lesion studies (Petrides, 1991; Petrides, 1995) and human imaging studies (Curtis, Zald, & Pard, 2000; Petrides, Alivisatos, Evans, & Meyer, 1993) relate the importance of dorsolateral prefrontal cortex, specifically mid-dorsolateral regions, to successful performance of this task. Letter Fluency (Artiola I Fortuny, Hermosillo-Romo, Heaton, & Pardee, 1999): The subject is asked to say as many words as possible that begin with a certain letter (P, M, R) in 1 min. The total number of correct words was recorded. This task evaluates spontaneous cognitive flexibility, i.e. the capacity to produce a flow of ideas or of items in response to simple instructions. Studies of brain lesions (Henry & Crawford, 2004) and neuroimaging studies have related this process to functioning of the prefrontal cortex, especially the left dorsolateral region (Frith, Friston, Liddle, & Frackowlak, 1991; Gourovitch et al., 2000; Phelps, Hyder, Blamire & Shulman, 1997). Zoo Map subtest (Behavioural Assessment of Dysexecutive Syndrome, BADS (Wilson et al, 1996). This is a planning test in wich the subjects has to indicate on a map provided of a zoo, the route they would take to visit six of twelve possible locations. There were two versions of the trial, with the same aim but with different instructions. The first trial consist of a “high demand” version of the task. Participants are given a zoo map and a set of instructions relating to places they have to visit and rules to be observed. In the second trial, or “low demand” version, the participant is simply required to follow the instructions to reach the twelve locations and to produce an error-free performance. Comparison of the performance of the trials enables assessment of the planning ability when structure is minimal (first trial or high demand) and when structure is high (second trial of low demand). The Zoo Map Test has been shown to have ecological validity and to be useful to detect planning impairment in alcoholics (Fernández-Serrano, Pérez-García, Perales, & Verdejo-García, 2010; Moriyama et al., 2002). Key Search subtest (BADS) (Wilson et al., 1996): Evaluates planning and strategy making skills. The Post-print (final draft post-refereeing) 7 participant is shown a square drawn on a piece of paper and is asked to imagine that it is a field. The subject's task is to draw a continuous line showing the path to follow to find the keys that have been lost at an unknown point in the field. The Zoo Map and Key Search tests assess planning and have shown an adequate correlation with other measures of planning (Strauss, Sherman, & Spreen, 2006). Diverse studies have shown that the BADS is an adequate battery of tests to evaluate executive functions and that it has ecological validity (Allain et al., 2005; Bennett, Ong, & Ponsford, 2005; Wilson et al., 1996). Wisconsin Card Sorting Test-3 (WCST-3) (Robinson, Kester, Saykin, Kaplan, & Gur, 1991). This is a short version of the WCST (Grant & Berg, 1948) in which the subject has to match 64 cards, one by one, with one of the four stimulus cards placed in front of them. After each classification, the examiner indicates to the subject if the response in correct or incorrect. There are three classification principles (color, shape and number) that change, without prior warning, each time that the subject makes 10 consecutive correct matches. Unlike the original WCST, in which the color–shape– number sequence is repeated twice (so that the subject can match up to six categories), in the WCST-3 the task ends once the subject completes the sequence, or when all 64 cards have been used. Completed categories and perseverative responses were registered. The WCST assesses concept formation and reactive cognitive flexibility. Neuroimaging lesion studies have related adequate completion of this task with activation of the dorsolateral and medial prefrontal cortex (Buchsbaum, Greer, Chang, & Berman, 2005). 2.3. Statistical analyses The data were analyzed with SPSS, version 15.0 for Windows (SPSS, 2006). To analyze the effect of BD and sex on neuropsychological performance were carried out univariate ANOVAs with two factors, each with two levels, for each of the dependent variables. Differences were considered significant at p < 0.05. 3. Results 3.1. Binge drinking Statistical analysis revealed a significant effect of BD on performance of the Backward Digit Span test [F(1,115) = 6.816, p = .01]; BD subjects scored lower than non-BD subjects (Table 2). Table 2 Post-print (final draft post-refereeing) 8 A significant effect of BD was too observed on the number of perseverations of the SOPT [F (1,118) = 6.474, p = .012]. As a group, BD subjects produced more perseverations than non-BD subjects. 3.2. Binge drinking by Sex A significant interaction BD by Sex was observed in Backward Digit Span [F(1,115) = 4.945, p = .028]. Male BD obtained lower scores than non-BD males (p = .001) and females BD (p = .041). 3.3. BD without occasional consumption of cannabis To be sure that difference in occasional cannabis consumption among the groups was not confounding the results, we conducted a second analysis excluding these participants. The results confirm the significant effect of BD on performance of the Backward Digit Span Test [F(1,80) = 5.884, p = .018] and on the number of perseverations of SOPT [F(1,81) = 7.344, p = .008]. Besides, the differences on total errors of the SOPT achieved statistical significance [F(1,82) = 3.998, p = .049]. By contrast, the analysis did not show significant interaction effect of BD by Sex on Backward Digit Span Test [F(1,80) = 1.535, p = .219]. 4. Discussion The main objective of this study was to analyze the association between BD pattern of alcohol consumption and executive functions in young university students. The sample consisted of first year students with no other relevant risk factors (such as psychiatric comorbidity, family history of alcoholism or polyconsumption of drugs). A further aim of the study was to determine if sex modulates the association between BD and neuropsychological performance. As regards the first objective, the data show that in comparison with non-BD subjects, the BD university students obtain significantly lower scores in the Backward Digit Span test and commit more perseveration errors in the SOPT. These differences remained significant when analyzing the data excluding participants who have occasional consumption of cannabis. The poorer performance of the BD subjects in the Backward Digit Span test indicates a lower capacity to retain and manipulate information in verbal working memory. The pattern of performance of the Spatial Span test was similar to the Backward Digit Span Test, although in this case the differences Post-print (final draft post-refereeing) 15 induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. The European Journal of Neuroscience, 25, 541–550. Pascual, M., Boix, J., Felipo, V., & Guerri, C. (2009). Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. Journal of Neurochemistry, 108, 920–931. Petrides, M. (1991). Functional specialization within the dorsolateral frontal cortex for serial order memory. Proceedings of the Royal Society of London Series B-Biological Sciences, 23, 299– 306. Petrides, M. (1995). Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey. The Journal of Neuroscience, 15, 359–375. Petrides, M., Alivisatos, B., Evans, A. C., & Meyer, E. (1993). Dissociation of human middorsolateral from posterior dorsolateral frontal cortex in memory processing. Proceedings of the National Academy of Sciences of the United States of America, 90, 829–839. Petrides, M., & Milner, B. (1982). Deficits on subject-ordered tasks alter frontal and temporal lobe lesions in man. Neuropsychologia, 20, 249–262. Phelps, E. A., Hyder, F., Blamire, A. M., & Shulman, R. G. (1997). FMRI of the prefrontal cortex during overt verbal fluency. Neuroreport, 8, 561–565. Robinson, L. J., Kester, D. B., Saykin, A. J., Kaplan, E. F., & Gur, R. C. (1991). Comparison of two short forms of the Wisconsin Card Sorting Test. Archives of Clinical Neuropsychology, 6, 27– 33. Ross, T. P., Hanouskova, E., Giarla, K., Calhoun, E., & Tucker, M. (2007). The reliability and validity of the self-ordered pointing task. Archives of Clinical Neuropsychology, 22, 449–458. Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Williams, S. C., Simmons, A., et al. (2000). Functional frontalisation with age: Mapping neurodevelopmental trajectories with fMRI. Neuroscience and Biobehavioral Reviews, 24, 13–19. Salatas-Waters, H. (1982). Memory development in adolescence: Relationships between metamemory, strategy use, and performance. Journal of Experimental Child Psychology, 33, 183–195. Scaife, J. C., & Duka, T. (2009). Behavioural measures of frontal lobre function in a population of young social drinkers with binge drinking pattern. Pharmacology, Biochemistry, and Behavior, 93, 354–362. Schulteis, G., Archer, C., Tapert, S. F., & Frank, L. R. (2008). Intermittent binge alcohol exposure during the periadolescent period induces spatial working memory deficits in young adult rats. Alcohol, 42, 459–467. Sowell, E. R., Thompson, P. M., Tessner, K. D., & Toga, A. W. (2001). Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. The Journal of Neuroscience, 21, 8819–8829. SPSS (2006). Advanced statistics 15.0. Chicago: SPSS Inc. Stephens, D. N., & Duka, T. (2008). Cognitive and emotional consequences of binge drinking: Role of amygdala and prefrontal cortex. Proceedings: Biological Sciences, 12, 3169–3179. Strauss, E., Sherman, E. M. S., & Spreen, O. (2006). A compendium of neuropsychological tests: Administration, norms and commentary (3rd Ed.). New York: Oxford University Press. Sullivan, E. V., Fama, R., Rosenbloom, M. J., & Pfefferbaum, A. (2002). A profile of neuropsychological deficits in alcoholic women. Neuropsychology, 16, 74–83. Tapert, S. F., Baratta, M. V., Abrantes, A. M., & Brown, S. A. (2002). Attention dysfunction predicts Post-print (final draft post-refereeing) 16 substance involvement in community youths. Journal of the American Academy of Child and Adolescent Psychiatry, 41, 680–686. Tapert, S. F., & Brown, S. A. (1999). Neuropsychological correlates of adolescent substance abuse: Four-year outcomes. Journal of the International Neuropsychological Society, 5, 481–493. Tapert, S. F., Brown, G. G., Kindermann, S. S., Cheung, E. H., Frank, L. R., & Brown, S. A. (2001). fMRI measurement of brain dysfunction in alcohol-dependent young women. Alcoholism, Clinical and Experimental Research, 25, 236–245. Townshend, J. M., & Duka, T. (2005). Binge drinking, cognitive performance and mood in a population of young social drinkers. Alcoholism, Clinical and Experimental Research, 29, 317–325. Varela, J., Braña, T., Real, E., & Rial, A. (2005). Validación empírica do AUDIT (Cuestionario de Identificación dos Trastornos debido ó consumo de alcohol) na poboación xeral galega. Santiago de Compostela: Xunta de Galicia. Consellería de Sanidad-Sergas. Vicki, M., Kuntsche, E., & Gmel, G. (2010). Drinking at European universities? A review of students' alcohol use. Addictive Behaviors, 35, 913–924. Wechsler, D. (1997). Wechsler memory scale-III. San Antonio: The Psychological Corporation. Weissenborn, R., & Duka, T. (2003). Acute alcohol effects on cognitive function in social drinkers: Their relationship to drinking habits. Psychopharmacology, 165, 306–312. Welsh, M. C., Pennington, B. F., & Groisser, D. B. (1991). A normative-developmental study of executive in prefrontal function in children. Developmental Neuropsychology, 7, 131–149. Wilson, B. A., Evans, J. J., Alderman, N., Burgess, P. W., Emslec, H., & Evans, Y. (1996). Behavioral assessment of the dysexecutive syndrome. England: Thames Vallet Test Company. Yurgelun-Todd, D. (2007). Emotional and cognitive changes during adolescence. Current Opinion in Neurobiology, 17, 251–257. Post-print (final draft post-refereeing) 17 Tables Table 1. Mean (± SD) for sociodemographic, clinical and alcohol use pattern characteristics. No binge drinking Binge drinking Males Females Males Females n 31 29 32 30 Age 18.61 (0.55) 18.83 (0.53) 19.03 (0.53) 18.70 (0.59) Hand-dominance (right/left) 28/3 28/1 31/1 28/2 Socio-economic status (low//medium/high) 0/27/4 4/22/3 2/27/3 3/19/7 Caucasian ethnicity (%) 100 100 100 100 SCL-90-R (percentile GSI) 55.00 (28.83) 41.72 (25.57) 60.50 (31.86) 37.83 (26.96) Vocabulary, scaled score (WAIS-III) 12.65 (2.27) 12.52 (1.74) 12.59 (1.43) 11.57 (1.50) University entrance grade exam 6.59 (1.17) 6.63 (0.82) 6.38 (1.27) 6.31 (1.20) Occasional use of cannabisa 2 7 14 13 Tobacco smokers 0 1 4 8 Age of onset of regular consumption on alcohol⁎ 16.00 (0.85) 15.54 (1.25) 15.13 (1.26) 14.53 (1.26) Drinks in the last week b,⁎ 2.74 (4.09) 3.38 (3.87) 15.29 (12.56) 19.25 (12.64) Percentage of times became drunk when drinking⁎ 5.39 (11.62) 5.96 (7.78) 51.18 (31.04) 49.00 (34.72) Times drunk in the last two weeks⁎ 0.03 (0.18) 0.26 (0.71) 2.04 (1.82) 1.86 (2.03) Speed of consumption: drinks per hour⁎ 0.65 (1.14) 1.14 (0.99) 3.41 (1.38) 3.29 (0.76) Total AUDIT score 2.10 (2.16) 2.97 (1.93) 12.91 (4.72) 11.47 (4.04) Note: SCL-90-R (Symptom Checklist 90 Revised); GSI (Global Severity Index); WAIS-III (Wechsler Adult Intelligence Scale-III); AUDIT (Alcohol Use Disorder Identification Test). a Less than 10 occasions per year. b Self-reported. ⁎ p < 0.001 significant differences between groups. Post-print (final draft post-refereeing) 18 Table 2. Mean (± SD) scores for the neuropsychological tests. No binge drinking Binge drinking BD pattern BD × Sex Males (n = 31) Females (n = 29) Males (n = 32) Females (n = 30) p η2 p η2 Backward Digit Span (WMSIII) 6.13 (1.17) 5.79 (1.42) 5.06 (1.13) 5.70 (1.12) .010 .055 .028 .041 Backward Spatial Span (WMSIII) 6.40 (1.28) 6.38 (1.21) 5.94 (0.95) 6.03 (1.33) .065 .029 .789 .001 SOPT Perseverations 0.94 (1.18) 1.52 (1.18) 2.00 (1.90) 1.80 (1.42) .012 .053 .142 .018 Total errors 9.65 (5.12) 10.28 (4.34) 10.75 (6.20) 12.80 (7.76) .098 .023 .515 .004 Phonetic fluency (P/M/R) 43.58 (8.43) 44.69 (7.61) 42.25(10.54) 42.83 (8.51) .324 .008 .870 .000 Zoo Map (BADS) Direct score 1 5.77 (3.25) 5.17 (3.62) 4.72 (3.32) 4.00 (3.52) .076 .027 .925 .000 Direct score 2 8.00 (.00) 7.90 (.55) 7.56 (1.39) 7.57 (1.56) .054 .031 .786 .001 Key search (BADS) Direct score 11.58 (2.79) 11.90 (3.05) 11.50 (2.95) 11.57 (3.17) .706 .001 .819 .000 WCST-3 Number of categories 2.32 (0.91) 2.55 (0.74) 2.66 (0.60) 2.63 (0.62) .117 .021 .340 .008 Percentage perseverations 15.32 (9.55) 14.31 (7.73) 14.22 (9.81) 16.97 (9.88) .646 .002 .267 .010 Note: BD (Binge drinking); WMS-III (Wechsler Memory Scale-III); SOPT (Self-Ordered Pointing Test); WCST-3 (Wisconsin Card Sorting Test-3); BADS (Behavioral Assessment of Dysexecutive Syndrome) Post-print (final draft post-refereeing)