3V\FKRORJLFD Lannoy, S., et al. (2019). Behavioral and Cerebral Impairments Associated with Binge Drinking in ψ %HOJLFD Youth: A Critical Review. Psychologica Belgica, 59(1), pp. 116–155. DOI: https://doi.org/10.5334/pb.476

PHD CRITICAL REVIEW Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth: A Critical Review Séverine Lannoy*,†, Joël Billieux‡, Valérie Dormal† and Pierre Maurage†

Binge drinking is a widespread alcohol consumption pattern in youth that is linked to important behavioral and cerebral impairments, in both the short and the long term. From a critical review of the current literature on this topic, we conclude that binge drinkers display executive impairments, cerebral modifications, and prob- lems with emotion-related processes. Five key empirical and theoretical topics are discussed to pave the way for future research in the field: (1) the specificity of the brain modifications observed in binge drinkers that may index a compensatory mechanism or result from multiple withdrawals; (2) the nature of the relationship between binge drinking and impairments, suggesting reciprocal influences between excessive alcohol consumption and executive deficits; (3) the possible recovery of brain and cognitive functioning after the cessation of binge drinking; (4) the validity of the continuum hypothesis, suggesting links between binge drinking and severe alcohol use disorders; and (5) the existing strategies to reduce binge drink- ing habits or rehabilitate the associated cognitive deficits. Future perspectives are described in relation to the questions raised to identify the crucial variables to be addressed in research and clinical practice.

Keywords: binge drinking; neuropsychology; electrophysiology; neuroimaging; alcohol-use disorders; alcohol use disorder

Introduction particularly among students, where it is a Alcohol consumption is widespread in key component of the so-called academic Western societies and occurs in many eve- folklore (Wechsler & Nelson 2001). Despite ryday life situations. It also occupies an this ubiquity of alcohol consumption, lead- important position among young people, ing most people to consider it a relatively

* Cognition Health Society Laboratory (C2S Louvain-la-Neuve, BE – EA 6291), Université de Reims Champagne- ‡ Addictive and Compulsive Behaviours Lab Ardenne, Reims, FR (ACB-Lab), Institute for Health and Behaviour, † Laboratory for Experimental Psychopathol- University of Luxembourg, Esch-sur-Alzette, LU ogy (LEP), Psychological Science Research Corresponding author: Pierre Maurage Institute, Université catholique de Louvain, ([email protected]) Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 117 harmless substance, the danger of exces- could be considered a first step toward severe sive drinking habits has been recognized. alcohol use disorders (Bonomo et al., 2004). Alcohol-related disorders, currently identi- The main aim of this paper is therefore to fied as the third risk factor for premature identify the specific behavioral and cerebral death by the World Health Organization impairments related to binge drinking habits (WHO), lead to 3 million deaths per year in young adults through a critical review. It worldwide (WHO, 2016). Excessive alcohol is focused on two main processes that have consumption is thus considered a central been identified as central to the understand- public health problem (Nutt, King, & Phillips ing of alcohol-related disorders: executive 2010). The consequences of alcohol abuse functions and emotional processing. Beyond and dependence have also been extensively this literature review, we also address five explored in scientific research, which has specific research avenues: (1) the specific- mainly focused on long-term and chronic ity of the brain modifications observed in alcohol-related problems and shown, for binge drinkers, (2) the nature of the relation- example, cognitive (Stavro, Pelletier & Potvin ship between binge drinking and behavio- 2013), emotional (Donadon & Osório 2014), ral/cerebral impairments, (3) the possible interpersonal (Thoma, Friedmann & Suchan persistence of these impairments after the 2013), and cerebral (Bühler & Mann 2011) cessation of binge drinking habits, (4) the impairments related to alcohol dependence continuum hypothesis that links binge (as it is referred to in the DSM-IV) or severe drinking with severe alcohol use disorders, alcohol use disorders (as it is referred to in and (5) the perspectives for prevention and the DSM-5). Aside from these consequences intervention programs in binge drinking. in severe alcohol use disorders, which have These research avenues have been identified been largely documented, growing interest on the basis of major perspectives or limita- has recently been observed in the effects tions underlined in the existing literature. It of alcohol consumption on non-alcohol- is therefore essential to offer a critical state- dependent young people. Because nearly of-the-art discussion about these currently 2000 deaths per year in the United States prominent issues related to the binge drink- are related to excessive drinking in students ing research field. (Hingson, Zha & Weitzman 2009), research has started to explore whether excessive Definition and Conceptualization of drinking leads to deleterious consequences Binge Drinking and, if so, at which consumption threshold Binge drinking refers to an excessive but and frequency (Hingson, Zha, & White, 2017). episodic alcohol consumption pattern, char- Notably, some studies have suggested that acterized by repeated alternations between the specific binge drinking pattern, charac- large alcohol intakes and periods of absti- terized by repeated alternations between nence. Nevertheless, to date, the conceptu- intense intoxication and withdrawal, could alization of binge drinking remains a matter be associated with cognitive and emotional of debate in the scientific literature, and no impairments (Stephens & Duka 2008). consensus has been reached regarding its The problem of binge drinking is wide- definition. Two main proposals can, however, spread in youth: 40% of adolescents and be identified in existing studies that target young adults in Western countries presently alcohol consumption (i.e., number of drinks report at least one binge drinking episode consumed) or specific drinking pattern (i.e., per month (e.g., Archie et al., 2012; Kanny computation of a binge drinking score). et al., 2013). Other studies have found that The first classification that was proposed this consumption pattern leads to cognitive to capture binge drinking is based on the and cerebral consequences (Hermens et al., number of drinks consumed on one occa- 2013; Maurage, Petit & Campanella 2013a). It sion, commonly recognized as the 5/4 has even been suggested that binge drinking measure (i.e., 5 alcohol units for men, 4 for 118 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth women; Wechsler & Nelson 2001; Labhart drinking score: [(4 × consumption speed) + et al., 2018). Such an approach has been number of drunkenness episodes + (0.2 × widely used in epidemiological and public percentage of drunkenness episodes)]. This health research (e.g., Kanny et al., 2013). This binge drinking score has been widely used proposal was further specified through the in the literature (e.g., Bø et al., 2016a; Czapla calculation of the blood alcohol concentra- et al., 2015; Kessler et al., 2013) and cutoff tion (BAC) level. Specifically, the National scores have been provided to differentiate Institute on Alcohol Abuse and Alcoholism non-binge drinkers from binge drinkers (NIAAA, 2004) describes binge drinking as (Townshend & Duka 2005). However, these an alcohol consumption pattern leading to cutoff scores also depend on the quantity of a BAC level of 0.08 g/dL, typically observed alcohol contained in one unit. Typically, the after four (for women) or five (for men) initial studies that used this binge drinking alcohol drinks over a period of 2 hours. To score (Townshend & Duka 2002, 2005) were be considered binge drinkers, individuals conducted in England, where an alcohol have to present such a consumption pattern unit contains 8 g of pure ethanol. In these at least once a month. Although focusing studies, a score higher than 23 indicated on the BAC level offers an initial objective intense binge drinking, whereas a score definition, these quantities should take into lower than 17 characterized non-binge account national differences (e.g., an alco- drinkers. In Belgium, where an alcohol unit hol unit contains 8 g of pure ethanol in the comprises 10 g of pure ethanol, adapted United Kingdom, whereas it contains 10 g cutoffs have been proposed in accordance in most European countries and 14 g in the with other alcohol variables, such as num- United States). Another potential shortcom- ber of doses consumed per occasion or con- ing of this definition is that it does not focus sumption speed (e.g., Lannoy et al., 2017a): on the frequency of drinking habits, which binge drinkers were thus defined as hav- is known to be a key variable in explaining ing a score higher than 17, whereas non- the emergence of neurological consequences binge drinkers have a score lower than 13. and alcohol use disorder. Another advantage of the binge drinking Second, some authors have suggested that score is that it indirectly takes into account binge drinking should be described in refer- enhancement-related motives (e.g., eupho- ence to the drinking pattern rather than to ria), which constitute strong predictors of alcohol consumption per se (Townshend & binge drinking (e.g., Kuntsche et al., 2014). Duka 2002). This approach appears to be Consideration of consumption speed and particularly well adapted to the explora- drunkenness allows one to target the moti- tion of drinking among people who con- vational aspects of drinking (e.g., drinking a sume alcohol in large quantities but in an large amount to rapidly become intoxicated irregular pattern (i.e., binge drinkers), which and thus feel the positive sensations associ- might not be detected with the NIAAA defi- ated with alcohol). nition. The computation of a binge drink- ing score was thus proposed, based on (1) Definition of Related Alcohol consumption speed (i.e., number of alcohol Consumption Patterns units consumed per hour), (2) number of In this section, we briefly describe the differ- drunkenness episodes (drunkenness being ent terms used to refer to excessive drinking defined as reduced ability to speak clearly, among young adults that may be related to loss of coordination, and nausea), and (3) binge drinking, including hazardous drink- percentage of drunkenness episodes (i.e., ing, heavy episodic drinking, and social drink- ratio of drunkenness episodes to the total ing. Some of the studies that we review focus number of drinking episodes) in the last 6 on these alcohol consumption patterns and months. More precisely, the following for- describe them with the number of “binge mula has been proposed to compute a binge drinking episodes” in a specific time frame, Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 119 thus proposing a direct link with binge be proposed regarding its use. Despite this drinking. ongoing debate about definitions, many According to the WHO, alcohol consump- studies have explored the consequences of tion ranges from hazardous drinking to binge drinking during the last decades in physical dependence (Babor & Higgins- order to specify the cognitive and cerebral Biddle, 2001). Hazardous drinking refers to impairments related to this drinking pat- a repetitive pattern of alcohol consumption tern. In the next sections, we first review that leads to physical, mental, and social the behavioral results that show that binge consequences. This drinking mode consists drinking is related to large-scale executive of the consumption of at least five (women) deficits, and then describe the studies that or seven (men) drinks per occasion at least used neuroscience techniques to determine three times per week. In the literature, the the brain modifications observed among Alcohol Use Disorders Identification Test binge drinkers. score is used to categorize individuals as haz- ardous drinkers (e.g., Palfai & Ostafin, 2003; Literature Review Van Tyne et al., 2012), typically when they The current literature review capitalizes on a have a score higher than seven. critical approach to cover several important Heavy episodic drinking is defined by the fields in the binge drinking literature before NIAAA as a binge drinking pattern (at least identifying and discussing the major issues four or five United States alcohol units con- in these fields. In particular, we focus on two sumed per occasion) that occurs more than central processes involved in addiction and once a week (NIAAA, 2004). In most studies, even more so in alcohol-related disorders: heavy drinking is used as a synonym for binge executive functions and emotional process- drinking, without necessarily representing a ing. All of the studies that refer to binge more frequent pattern of excessive drinking drinking are included in this review, even (e.g., Nederkoorn et al., 2009). though the definition of binge drinking is Social drinking is mainly related to the moti- distinctly different among them (as men- vations underlying alcohol consumption and tioned earlier). We did not consider stud- characterizes individuals who drink alcohol ies that aimed to determine acute alcohol in social contexts. However, in the literature, effects or that targeted comorbidity between this term is often used to refer to excessive binge drinking and psychopathological dis- drinkers (mostly according to weekly alco- orders. In addition to considering behavioral hol consumption, e.g., Townshend & Duka, results, we also address cerebral modifica- 2001) but without a systematic evaluation tions related to binge drinking, in particular of drinking motives or alcohol expectancies cerebral changes during cognitive tasks, in (Petit et al., 2012). order to connect them with the behavioral findings. Moreover, in the neuroscience sec- Brief Conclusion tion, we mainly focus on electrophysiological This section highlighted the various related studies that describe the changes related to concepts used to define excessive alcohol specific cognitive stages. Finally, we briefly consumption habits in youth, particularly address neuroimaging data that provide a binge drinking. Most studies that focus on clear understanding of the compensatory binge drinking use one definition or another, brain mechanisms described in binge drink- but combining these definitions to simulta- ing (see critical discussion for more details). neously consider the BAC level and the binge drinking score might lead to a more valid Executive impairments associated with definition of specific binge drinking habits. binge drinking However, such a definition has to be consid- Executive functions have been studied inten- ered in terms of large samples and different sively because impairments in these func- populations so that a better consensus can tions are a crucial feature of severe alcohol 120 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth use disorders (Wilcox et al., 2014). In binge in the study by Hartley et al. (2004) than in drinking, studies that explored these difficul- that by Scaife and Duka (2009) (14 and 30 ties showed impairments in flexibility and in binge drinkers, respectively). Nonetheless, inhibition in particular (Table 1). although they did not observe flexibility impairments, Hartley et al. (2004) identi- Flexibility fied group differences in other experimen- Concerning flexibility, one study that tal tasks, suggesting that alternative factors included people who had at least one binge could explain this difference (e.g., related to drinking episode per month required par- the control group, as these participants were ticipants to alternately connect randomly either totally abstinent or low alcohol con- presented numbers (in ascending order) and sumers in these studies). Finally, a continu- letters (in alphabetical order) in the Trail ous approach that targeted various drinking Making Test (Salas-Gomez et al., 2016). The patterns rather than specific groups showed authors reported that this group had poorer that shifting did not predict the binge drink- performance in assessments of attention, ing score 18 months later (Bø et al., 2017). visuo-spatial abilities, and flexibility. Using the same task and criteria, Gil-Hernandez et Inhibition al. (2017) specified that this poorer flexibil- Inhibition is typically divided into three sub- ity only appeared in older binge drinkers and components (see Friedman & Miyake 2004): not among adolescents. However, another prepotent response inhibition (control of study showed that, when binge drinkers and automatic responses), resistance to distrac- non-binge drinkers were compared after 11 tor interference (ability to resist disturbances years, flexibility impairments were not sup- from inappropriate information), and resist- ported by either the Trail Making Test or ance to proactive interference (ability to the verbal fluency task (asking participants resist memory interference from previously to produce as many words as possible in 1 relevant information). However, the existing minute that started with a specific letter) binge drinking literature has mainly focused (Carbia et al., 2018a). By comparing groups on prepotent response inhibition, which is selected on the basis of the binge drinking more closely related to the control of alcohol score, Scaife and Duka (2009) specifically consumption (López-Caneda et al., 2014a); evaluated shifting and attentional flexibil- the present critical review also focuses on ity in a task that also involved rule acquisi- this type of inhibition. Study results have tion, visual discrimination, and attentional mostly indexed inhibition impairments in abilities (Intra/Extradimensional Set Shift binge drinking, which are potentially iden- Task, which requires participants to learn tified as both the cause and consequence the characteristics of the correct stimulus, of excessive consumption (López-Caneda representing color-filled shapes, white lines, et al., 2014a). Moreover, by asking partici- or both, while characteristics change across pants to perform a task that also involved successive blocks). Their findings revealed sustained attention, one study reported that impaired performance in female binge drink- binge drinkers presented more commis- ers (Scaife & Duka 2009). Nevertheless, using sion errors than controls did (Townshend & the same experimental task but comparing Duka, 2005). Another study showed that in binge drinkers to teetotalers (i.e., partici- the Stroop color-word task, the performance pants who never drink alcohol; binge drink- of binge drinkers was comparable to that of ers were recruited according to the NIAAA elderly people, suggesting premature aging definition and their binge drinking score), in binge drinking (Sanhueza, García-Moreno, Hartley, Elsabagh, and File (2004) could & Expósito, 2011). not identify any impairment in flexibility Nevertheless, some studies that used in binge drinkers. This contradictory result the classic Stroop or Stop Signal tasks did can be explained by the smaller sample size not find impairment of inhibition in binge Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 121 (Contd.) Results No group difference binge drinkers presented Female poor performance Binge drinkers showed poorer performance Shifting did not predict the binge months later drinking score 18 yo) presented Binge drinkers (19–22 poorer performance than matched Making Test controls in the Trail No group difference binge drinkers showed poorer Female performance (more commission errors) than female controls Inhibition performance did not ­ predict alcohol use and problems Tasks Intra/Extradimensional Set evaluates shiftingShift Task and attentional flexibility Intra/Extradimensional Set Shift Task (A, B) Making Test Trail B evaluates attentionalPart flexibility Intra/Extradimensional Set Shift Task (A, B) Making Test Trail fluencyVerbal assessing flexibility B Making Test, Trail fluencyVerbal measures response Digit Vigilance Test inhibition during sustained attention measuring the ability to Go/No-Go Task inhibit an inappropriate response measuring the ability Stop Signal Task to inhibit an already initiated response : 13–15 yo, : 13–15 1 : 19–22 yo) : 19–22 3 : 16–18 yo, : 16–18 Participants yo) mean age: 21.1 adults (N = 27; Young NIAAA criteria Binge drinking score adults (N = 60; mean age: 20.6 yo) Young Binge drinking score yo) adults (N = 206; mean age: 19.5 Young NIAAA criteria yo) mean age: 21.7 adults (N = 103; Young Binge drinking score (continuous approach) Adolescents and young adults (N = 322) categorized according to age ( 2 NIAAA criteria Adults after years of alcohol 11 ­ consumption (N = 63; age: 29 yo) score AUDIT-C mean age: 20.9 yo) adults (N = 100, Young Binge drinking score yo) adults (N = 75; mean age: 19.3 Young binge weekly consumption, AUDIT, Total drinking score (continuous approach) Summary of the behavioral studies exploring executive functions in binge drinking. Flexibility Hartley et al. (2004) Scaife & Duka (2009) Salas-Gomez et al. (2016) Bø et al. (2017) Gil-Hernandez et al. (2017) Carbia et al. (2018a) Inhibition & Duka (2005) Townshend et al. (2010) Fernie Table 1: Table 122 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth (Contd.) performance was comparable Results Inhibition performance was not related to alcohol consumption two years later Binge drinkers performed worse than controls of similar age. Their ­ to elderly participants in the word ­ reading condition but not in the word naming one. No group difference inhibition performance Poor ­ predicted the total consumption in the month, number of binge drinking episodes, and the highest number of drinks consumed. No group difference Binge drinkers presented poorer ­ performance in the alcohol condition Binge drinkers presented poorer performance No group difference - Tasks is a combination of Go Stop Task Go/No-Go and Stop Signal tasks evalu ating prepotent response inhibition evaluating the Stroop color-word Task ability to avoid an automatic response Go/No-Go Task Stop Task Go/No-Go Task Stop Signal Task with alcohol-related Go/No-Go Task stimuli Monetary Incentive Control Task ­ assessing prepotent response inhibition with reward contingency Stroop color-word Task Participants adults (N = 200; mean age: 20.4 yo) Young Consumption of more than 5 drinks at least two times in the past month yo) and people (mean age: 18.9 Young elderly adults (mean age: 69.4 yo) [N = 91] binge drinking, consumption of more For than 6 (female) or 8 (male) drinks in two hours adults (N = 68; mean age: 20 yo) Young score, more than 6 drinks in the last CAGE drinking episode yo) mean age: 19.6 adults (N = 109; Young NIAAA criteria (continuous approach) yo) adults (N = 44; mean age: 21.2 Young Binge drinking score adults (N = 32; mean age: 23.8 yo) Young Binge drinking score Adults (N = 84; mean age: 22.8 yo) Consumption of at least 6 drinks (with more than 2 drinks per hour) at least two times a month yo) adults (N = 206; mean age: 19.5 Young NIAAA criteria Goudriaan et al. (2011) Sanhueza et al. (2011) Moreno et al. (2012) Henges & Marczinski (2012) Sanchez-Roige et al. (2014) Czapla et al. (2015) et al. (2016) Poulton Salas-Gomez et al. (2016) Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 123 - (Contd.) Results Binge drinking score did not predict poor inhibition but faster reaction time and less adjustment following commission errors Binge drinkers presented poorer adjustment following commission errors in the alcohol condition Binge drinkers were slower than controls No group difference involving binge drinking No group difference No group difference at the ­ longitudinal level (after two years of binge drinking) At the longitudinal level, stable high binge drinkers group (according to the frequency) made less advanta geous choices in decision making stimuli) Go/No-Go Task with stimuli) Go/No-Go Task Tasks Stop Signal Task Speeded (time limit to process Go ­ ­ alcohol-related stimuli Stockings of Cambridge test evaluating planning abilities of Hanoi assessing planning Tower abilities Search tests Zoo Map and Key ­ measuring planning abilities Search tests Zoo Map and Key assessing decision Iowa Gambling Task making under ambiguity and under risk Participants yo) mean age: 21.7 adults (N = 121; Young Binge drinking score (continuous approach) adults (N = 44; mean age: 20.9 yo) Young Consumption of at least 6 drinks (minimum 2 drinks per hour) at least two times a week Binge drinking score yo) mean age: 21.1 adults (N = 27; Young NIAAA criteria Binge drinking score yo) and people (mean age: 18.9 Young elderly adults (mean age: 69.4 yo) [N = 91] binge drinking, consumption of more For than 6 (female) or 8 (male) drinks in two hours yo) mean age: 18.8 adults (N = 122; Young Consumption of at least 6 drinks (minimum 3 drinks/hour) once a month yo) adults (N = 89; mean age: 18.7 Young Consumption of at least 6 drinks (minimum 3 drinks/hour) once a month yo) adults (N = 200; mean age: 19.9 Young Consumption of more than 5 drinks at least two times in the past month Bø et al. (2016a) Lannoy et al. (2018a) Planning Hartley et al. (2004) Sanhueza et al. (2011) et al. (2012) Parada Mota et al. (2013) Decision-making Goudriaan et al. (2007) 124 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth - Results Binge drinkers had poorer decision making abilities, and advantageous decision making predicted less drinking problems one year later decision making was associ Poorer ated with higher binge drinking two years later Binge drinking score was related to poorer performance in the first trials of decision making Binge drinkers had poorer decision- making performance Tasks Iowa Gambling Task Iowa Gambling Task Iowa Gambling Task Iowa Gambling Task evaluating decision Task Two-Choice making Participants yo) mean age: 16.2 Adolescents (N = 181; NIAAA criteria adults (N = 200; mean age: 20.4 yo) Young Consumption of more than 5 drinks at least two times in the past month yo) mean age: 21.7 adults (N = 121; Young Binge drinking score (continuous approach) adults (N = 68; mean age: 20 yo) Young score, more than 6 drinks in the last CAGE drinking episode : The three first processes (flexibility, inhibition, planning) refer to executive functions subcomponents. NIAAA criteria correspond to at least one binge : The three first processes (flexibility, drinking episode per month. Binge drinking score is computed based on the following formula: [(4*consumption speed) + drunkenness frequency + (0.2 * (0.2 + frequency drunkenness + speed) [(4*consumption formula: following the on based computed is score drinking Binge month. per episode drinking intensity, frequency, consumption alcohol assessing questionnaire AUDIT the of items first three the of sum the of consists AUDIT-C percentage)]. drunkenness questionnaire evaluates problem drinking by four self-reported items. yo = years old. and the frequency of binge drinking episodes (more than 6 drinks). CAGE One drink corresponds to one alcohol unit. Xiao et al. (2009) Goudriaan et al. (2011) Bø et al. (2016) Moreno et al. (2012) Note Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 125 drinkers (e.g., Salas-Gomez et al., 2016; of a screen (Stockings of Cambridge test). Sanchez-Roige et al., 2014), suggesting that While there was no difference in the num- the involvement of this process is question- ber of moves necessary to obtain the correct able. First, some studies suggested instead schema, binge drinkers were slower than tee- that binge drinkers display decision-making totalers in planning their actions, especially deficits (e.g., Moreno et al., 2012). This result at the beginning of the task (Hartley et al., is supported by the study of Goudriaan and 2004). However, to our knowledge, no study colleagues (2011), which indicated that deci- has confirmed these higher level executive sion making, but not prepotent response difficulties in binge drinkers. Investigators inhibition, is an efficient predictor of binge have also stated that the comparison drinking habits 2 years later. Similarly, using between binge drinkers and teetotalers did a continuous approach that aimed to pre- not allow them to identify impairments that dict binge drinking, some studies found that were specifically related to the consumption inhibition difficulties predicted the num- pattern, as the difference might be due to a ber of drinks consumed on one occasion general difference in the quantity of alcohol (e.g., Henges & Marczinski 2012), while oth- consumed. In several studies that were based ers found that alcohol use and problems in on various experimental paradigms, investi- binge drinkers were predicted only by risk- gators did not observe planning difficulties taking tendencies (e.g., Fernie et al., 2010). in binge drinkers compared with control low Second, it has also been argued that binge drinkers (Parada et al., 2012; Sanhueza et al., drinkers present inhibition impairment only 2011), even after 2 years of continuous binge during the processing of alcohol-related cues drinking (Mota et al., 2013). (Czapla et al., 2015). However, with a more complex and reward-based task, binge drink- Decision making ers had altered inhibition in both neutral and In addition to executive difficulties, disad- reward contexts (Poulton et al., 2016). Third, vantageous choices during decision making some studies indicated that the relationship have also been identified in binge drinkers between binge drinking and inhibition was compared with controls, mainly through instead characterized by impairments in per- the use of the Iowa Gambling Task (in which formance monitoring, in particular difficulty participants have to learn the reward prob- in adjusting one’s behavioral response fol- abilities associated with card decks and lowing commission errors (Bø et al., 2016a). progressively orient their choices toward This proposal was confirmed by using behav- long-term rather than short-term rewarding ioral and electrophysiological measures in decks). On the basis of alcohol consumption case-control studies involving binge drink- patterns in the past 2 years, high stable binge ers and control participants (Lannoy et al., drinkers (having two or three binge drinking 2017b; Lannoy et al., 2018a; Smith & Mattick episodes per month for at least 2 years) were 2013). These inconsistencies between studies compared with the following groups: low were addressed in a recent systematic review binge drinkers (having less than one binge of the neuropsychological studies in binge drinking episode per month), stable moder- drinking; the authors concluded, after care- ate binge drinkers (having one or two binge ful consideration of the literature, that binge drinking episodes per month during the last drinkers are indeed characterized by inhibi- 2 years), and increasing binge drinkers (low tion impairments (Carbia et al., 2018b). binge drinkers at the first evaluation but having two or three binge drinking episodes Planning per month 2 years later). Results showed that Planning abilities have been evaluated with high stable binge drinkers made fewer advan- a task that asks participants to reproduce a tageous choices than did the other groups specific schema displayed on the upper part (Goudriaan, Grekin & Sher 2007). Moreover, 126 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth decision making also predicted future con- inhibition was mainly considered in these sumption: disadvantageous choices were studies, whereas other types of inhibition associated with higher binge drinking hab- (i.e., resistance to distractor and to proactive its 2 years later, mainly in males (Goudriaan, interference) were largely ignored. Grekin & Sher 2011), and better choices predicted reduced alcohol consumption Emotional difficulties associated and alcohol-related problems 1 year later in with binge drinking adolescents (Xiao et al., 2009). Finally, for a Beyond the cognitive impairments observed sample of college students, a recent study in using classic neuropsychological para- suggested that the binge drinking score digms, recent research has highlighted that is exclusively related to disadvantageous binge drinking might also be associated choices in the first trials of the decision-mak- with emotional disturbances, although lit- ing task (Bø, Billieux & Landrø 2016b). These tle has been reported in this research field decision-making difficulties were identified until now. Several studies have described in binge drinkers with the Iowa Gambling increased depression, anxiety, or negative Task, as well as with a two-choice task that mood levels in young adult binge drink- required participants to choose between two ers from self-reported measures and have possibilities: wait 5 seconds and win 5 points identified negative emotions as vulner- or wait 15 seconds and win 15 points (Moreno ability factors for future binge drinking et al., 2012). Surprisingly, Goudriaan and col- (e.g., Mushquash et al., 2013; Townshend leagues (2007) observed that the decision- & Duka 2005). However, these results have making performance of binge drinkers was not been confirmed by experimental stud- not related to impulsivity (measured with ies that focus on mood induction or affec- the Impulsive Sensation Seeking Scale and tive processing. Moreover, to our knowledge, the Barratt Impulsivity Scale), and Moreno only seven studies have directly explored and colleagues (2012) showed decision-mak- the processing of emotional stimuli in binge ing impairments in the absence of inhibition drinking by means of affective decoding difficulties. These results are in line with tasks, most of them focusing on neurosci- the proposal of Verdejo-Garcia (2017) that, ence measures. At the behavioral level, the although decision-making abilities and exec- first study to explore emotional cross-modal utive processes may be related, individuals integration (i.e., multisensorial decoding of can also have a dissociated pattern charac- emotions) showed an absence of behavioral terized by decision-making impairments but differences between binge drinkers and con- preserved executive skills, underscoring the trol participants (Lannoy et al., 2017c), but independent contribution of these processes the use of a more complex and sensitive task (Verdejo-Garcia, 2017). indexed poorer recognition of emotional facial expressions in binge drinking (Lannoy Brief conclusion et al., 2018b). Other findings were observed In summary, the available data clearly suggest through neurophysiological and neuroimag- that binge drinking is associated with impor- ing studies. At the electrophysiological level, tant and various cognitive impairments, but the event-related potential (ERP) compo- some findings need to be replicated (e.g., nents associated with the processing of emo- planning difficulties have been observed in tional human voices (Maurage et al., 2009) only one study). Contradictory results have and with emotional cross-modal integration also been identified, notably regarding inhi- (Lannoy et al., 2018c), as well as the images bition, that might index the implications of associated with negative valence (Connell, specific underlying processes (e.g., perfor- Patton & McKillop, 2015), were disrupted in mance monitoring). Furthermore, regard- binge drinkers. Moreover, the affective mod- ing inhibitory control, prepotent response ulation of event-related theta oscillations was Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 127 reduced in binge drinkers during the process- observed for P100 and N100 components in ing of emotional images (Huang et al., 2017). an oddball paradigm (a task that compares At the neuroimaging level, results showed the brain activations related to repeatedly that young binge drinkers had reduced per- presented stimuli with those evoked by formance in emotional voice categorization rare stimuli), and reduced amplitudes were at the behavioral level, linked to a double found for N170 and P200 components in brain alteration (Maurage et al., 2013b): binge drinkers (Maurage et al., 2012). This binge drinkers presented reduced activation study also emphasized brain dysfunctions in in the voice processing area (superior tempo- attentional and decisional processes, namely, ral gyrus) but showed increased activation in delayed latencies and reduced amplitudes other areas not usually involved in emotional of N2b and P3b, as well as a longer P3a processing (middle frontal gyrus). Therefore, latency. Furthermore, this study compared these preliminary findings suggest that two groups of binge drinkers (differing in binge drinking might also be associated with their intensity, i.e., low and high), a group of impairments in the processing of emotional daily drinkers (matched on the total number stimuli. As emotional impairments have of alcohol doses consumed per week with been found to play a crucial role in the devel- the low binge drinkers’ group), and a con- opment and maintenance of severe alcohol trol group. This experimental design has led use disorders, understanding the early altera- to important insights by showing a specific tions of these emotional difficulties in the effect of the binge drinking pattern, a vari- first stages of the disorders may be essential ation of the brain impairments according to and should be investigated further. the intensity of binge drinking, and a wide range of cerebral alterations (from early to Cerebral modifications associated later stages). Moreover, this amplitude reduc- with binge drinking tion in binge drinkers was confirmed at early Insights from electrophysiology (P100) and later (P3b) stages of cognitive pro- To assess what is known about the link cessing (Ehlers et al., 2007; Petit et al., 2014). between cerebral modifications and behav- The study by Ehlers et al. (2007) used a facial ioral performance, we focus in this section discrimination task and highlighted a shorter on studies that explored specific ERPs during latency for attentional processes related cognitive and emotional tasks. Alterations of to novelty (P3a) and a reduced amplitude various ERP components have been reported for decisional processes (P3b). The study of in binge drinkers compared with those Petit and colleagues (2014) confirmed this in control participants (Table 2), without amplitude reduction for early and later elec- always being related to detectable behavioral trophysiological components after 1 year of impairments. Cerebral modifications were binge drinking by using a visual oddball task. indexed by either a reduced or an increased Compared with control participants, binge amplitude of ERP components. drinkers also demonstrated a reduced late positive component under a high working Decrease in electrophysiological activity memory load (Crego et al., 2010). Modifications of the P100, N2a, and P3b components were described in the process- Increase in electrophysiological activity ing of auditory voices in an emotional judg- Conversely, some studies have indicated ment task, showing delayed latency of these enhancement in ERP components. Increased ERP components after 9 months of binge amplitude was mainly observed for later drinking (Maurage et al., 2009); these results components, as reported by studies with thus challenge those of previous studies oddball paradigms (Crego et al., 2012; López- that proposed that impairments appear only Caneda et al., 2013). These studies showed a after several years of consumption. At the larger P3b in binge drinkers than in controls. perceptual level, slower latencies were also The longitudinal research of López-Caneda 128 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth - (Contd.) Results Binge drinkers presented delayed P100 latency after 9 months of binge drinking Binge drinkers presented increased P100 latency and a difference was also related to the intensity of binge drinking amplitude Binge drinkers had higher P100 during the processing of alcohol-related stimuli ampli Binge drinkers showed reduced P100 tude (for all stimuli) after one year Binge drinkers presented increased N100 latency and a difference was also related to the intensity of binge drinking High binge drinkers showed larger N100 amplitude than both low binge drinkers and controls (no effect of stimulus type) emotional pictures Tasks Emotional valence detection task with auditory stimuli Visual Oddball Task with alcohol- Visual Oddball Task related stimuli with alcohol- Visual Oddball Task related and ­ Visual Oddball Task with alcohol- Go/No-Go Task related stimuli Participants yo, at adults (N = 36, mean age: 18.2 Young first assessment time) Consumption of more than 6 drinks at least once a week yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers yo) adults (N = 36, mean age: 21.6 Young NIAAA criteria, consumption of at least 3 drinks/hour adults (N = 30, mean age: 22 yo, at Young first assessment time) Consumption of at least 6 drinks (minimum 3 drinks/hour) at or 4 times a week yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria (frequency-based approach to categorize low/high binge drinkers) Summary of the electrophysiological studies exploring binge drinking. P100 – Visuospatial processing P100 Maurage et al. (2009) Maurage et al. (2012) et al. (2012) Petit et al. (2014) Petit – Auditory processing/Early processing of unexpected stimulus N100 Maurage et al. (2012) et al. (2016) Watson Table 2: Table Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 129 (Contd.) Results amplitude Binge drinkers had reduced N170 and a difference was also related to the intensity of binge drinking No group difference Binge drinkers presented larger VPP amplitude Binge drinkers had a delayed N2a latency after 9 months of binge drinking Binge drinkers had larger N2b amplitude Binge drinkers had reduced N2b amplitude and a difference was also related to the intensity of binge drinking No group difference was found for N2b Tasks Visual Oddball Task Association Task Pairs Face–Name assessing associative memory Association Task Pairs Face–Name Emotional valence detection task A visual identical-pairs is Task Continuous Performance a visual task with high working memory load Visual Oddball Task Visual Oddball Task Participants yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria, consumption of at least 3 drinks/hour adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria, consumption of at least 3 drinks/hour yo at adults (N = 36, mean age: 18.2 Young first assessment time) Consumption of more than 6 drinks at least once a week yo) adults (N = 95, mean age: 18.8 Young NIAAA criteria, consumption of at least 3 drinks per hour yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers yo) adults (N = 85, mean age: 21.6 Young NIAAA criteria, consumption of at least 3 drinks/hour N170 – Visual and face processing N170 Maurage et al. (2012) et al. (2017) Folgueira-Ares and face processing VPP – Perceptual et al. (2017) Folgueira-Ares N200 – N2a: auditory processing; N2b: attentional resources focusing Maurage et al. (2009) Crego et al. (2009) Maurage et al. (2012) Crego et al. (2012) 130 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth (Contd.) Results No group difference was found for N2b No group difference was found for N2b No group difference was found for N2b Binge drinkers had reduced P200 amplitude and a difference was also related to the intensity of binge drinking Binge drinkers presented reduced P3a latency and reduced P3b amplitude. No difference was observed according to drug consumption Binge drinkers had a delayed P3b latency after 9 months of binge drinking No group difference was observed for the P3 component Tasks with Visual Oddball Task ­ alcohol-related stimuli with Go/No-Go Task ­ alcohol-related stimuli Modified spatial 2-back Task assessing working memory Visual Oddball Task discrimination Task Face Emotional valence detection task Continuous A visual identical-pairs Task Performance - - Participants yo) adults (N = 36, mean age: 21.6 Young NIAAA criteria, consumption of at least 3 drinks/hour adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria (frequency-based approach to categorize low/high binge drinkers) adults (N = 50, mean age: 22.2 yo) Young Consumption of at least 4 (female) or 5 (male) drinks in one occasion more than once in the previous 2 weeks [with mini mum 2 (female) or 3 (male) drinks/hour]. yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers yo) mean age: 19.9 adults (N = 125, Young NIAAA criteria, at least one binge drinking episode during adolescence; with or out drug consumption yo at adults (N = 36, mean age: 18.2 Young first assessment time) Consumption of more than 6 drinks at least once a week yo) adults (N = 95, mean age: 18.8 Young NIAAA criteria, consumption of at least 3 drinks/hour Petit et al. (2012) Petit et al. (2016) Watson & Kim (2018) Park P200 – High level perceptual processing Maurage et al. (2012) P300 – P3a: attention and stimuli novelty; P3b: closure of cognitive processing Ehlers et al. (2007) Maurage et al. (2009) Crego et al. (2009) Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 131 (Contd.) difference were also related to the Results Binge drinkers presented delayed and reduced P3b as well longer P3a latency. These ­ intensity of binge drinking Binge drinkers had larger P3b during Go ­ trials at baseline and two years later as well as larger P3b during No-Go trials but only after two years of binge drinking. Binge drinkers had increased P3 amplitude No group difference was found for P3b Binge drinkers had a higher P3b amplitude for the processing of alcohol cues, and this effect was stronger in men Binge drinkers showed larger P3b at baseline and this difference increased two years later Binge drinkers had larger P3b amplitude during No-Go trials after two years of binge drinking while ex-binge drinkers did not significantly differ from controls and binge drinkers. Consumption speed and age of drinking onset significantly predicted No-Go P3b amplitude alcohol-related and Tasks Visual Oddball Task Go/No-Go Task Visual Oddball Task with Visual Oddball Task ­ alcohol-related stimuli Visual Oddball Task with ­ emotional pictures Visual Oddball Task Go/No-Go Task Participants yo) adults (N = 80, mean age: 21.5 Young Comparison of low (at least 5 drinks, 2/3 drinks, times a week) and high (at least 10 3/4 times a week) binge drinking with controls and daily drinkers yo at adults (N = 48, mean age: 18.7 Young first assessment time) Consumption of at least 6 drinks once a week or at least 6 drinks (with minimum 3 drinks/hour) once a month yo) adults (N = 85, mean age: 21.6 Young NIAAA criteria, consumption of at least 3 drinks/hour yo) adults (N = 36, mean: 21.6 Young NIAAA criteria, consumption of at least 3 drinks per hour yo) adults (N = 56, mean age: 21.8 Young Consumption of at least 6 drinks (minimum 3 drinks per hour) at three or four times a week yo, at mean age: 18.6 adults (N = 57, Young first assessment time) Consumption of at least 6 drinks once a week or at least 6 drinks (with minimum 3 drinks/hour) once a month adults (N = 57), inclusion of an “ex- Young group binge drinkers” Consumption of at least 6 drinks once a week or at least 6 drinks (with minimum 3 drinks/hour) once a month Maurage et al. (2012) López-Caneda et al. (2012) Crego et al. (2012) et al. (2012) Petit et al. (2013) Petit López-Caneda et al. (2013) López-Caneda et al. (2014b) 132 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth - Results Binge drinkers had reduced P3b amplitude for the processing of neutral stimuli after one year of binge drinking High and low binge drinkers presented larger P3a amplitude for neutral than alcohol-related stimuli but at different sites (C4 for high binge drinkers and FC2 low binge drinkers) Binge drinkers showed no significant differ ence between congruent and incongruent conditions whereas controls presented larger P3a amplitude for congruent stimuli Binge drinkers had a smaller LPC under high working memory load No Dm effect (larger amplitude for correct than incorrect encoding) was observed in binge drinkers whereas this effect was found in controls Tasks with alcohol- Visual Oddball Task related and emotional pictures with alcohol- Go/No-Go Task related stimuli Modified spatial 2-back Task Continuous Identical Pairs Task Performance Association Task Pairs Face–Name Participants adults (N = 30, mean age: 22 yo, at Young first assessment time) Consumption of at least 6 drinks (minimum 3 drinks per hour) at three or four times a week adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria (approach based on the frequency to categorize low and high binge drinkers) adults (N = 50, mean age: 22.2 yo) Young Consumption of at least 4 (female) or 5 (male) drinks in one occasion more than once in the previous 2 weeks (with minimum 2 (female) or 3 (male) drinks per hour). yo) adults (N = 95, mean age: 18.8 Young NIAAA criteria, consumption of at least 3 drinks per hour adults (N = 50, mean age: 20.6 yo) Young NIAAA criteria, consumption of at least 3 drinks/hour : VPP: vertex positive potential; LPC: late component. Dm effect: Difference due to memory effect; yo = years old. One drink corresponds to one alcohol unit. et al. (2014) Petit et al. (2016) Watson & Kim (2018) Park memory processing LPC – Working Crego et al. (2010) Dm effect et al. (2017) Folgueira-Ares Note Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 133 and colleagues (2013) confirmed that this however, this result has not been supported difference persisted and was more pro- by other studies that targeted the N2b com- nounced after 2 years of continuous binge ponent (e.g., Park and Kim, 2018; Petit et al., drinking. During inhibition tasks, a larger 2012; Watson et al., 2016). amplitude was also found for the P300 com- When investigators explored the effect of ponent (López-Caneda et al., 2012, 2014b). alcohol cue processing, a higher P100 ampli- The first longitudinal study that targeted a tude was observed in binge drinkers for the binge drinking trajectory showed a higher processing of alcohol-related stimuli, regard- P300 for Go trials at both evaluation times less of their valence (positive, negative, neu- and a larger P300 for No-Go trials after 2 tral). This increased P100 was also correlated years of binge drinking (López-Caneda et al., to longer binge drinking habits and a higher 2012). P300 was detected at frontal, central, number of doses consumed per occasion and parietal sites and thus corresponded to (Petit et al., 2012). Another study that evalu- P3b. Analyses were also conducted to iden- ated prepotent response inhibition reported tify the source location, indicating higher a larger amplitude for earlier components activation in the right inferior frontal cor- (N100) and during the processing of various tex among binge drinkers during success- alcohol-related and neutral stimuli (Watson ful inhibition. The second longitudinal et al., 2016), particularly in intense binge study evaluated the persistence of potential drinkers (reporting at least eight binge drink- cerebral dysfunctions in ex-binge drink- ing episodes per month). Targeting asso- ers (López-Caneda et al., 2014b). Findings ciative memory processes, Folgueira-Ares et revealed that binge drinkers had a larger P3b al. (2017) also showed that binge drinkers amplitude for No-Go trials than did controls, present an increased amplitude for earlier whereas ex-binge drinkers were in an inter- components, particularly regarding the ver- mediate position, suggesting that cessation tex positive potential, as well as an absence of binge drinking allows recovery of the neu- of difference due to memory effect. The rophysiological impairments related to inhi- converse of this effect was observed in con- bition. Moreover, the study by López-Caneda trols, who showed larger amplitudes for cor- et al. (2014b) underlined that the P300 rect than for incorrect encoding during the amplitude for No-Go trials at the frontal site experimental task. was predicted by age at drinking onset and Electrophysiological findings in binge consumption speed, supporting the idea drinking therefore highlight various modi- that P300 modifications were due to binge fications of brain processing and reveal cer- drinking. An increased P3 amplitude was ebral dysfunctions even when behavioral also observed during the processing of alco- performance is preserved. A strong consist- hol cues (Petit et al., 2013) and neutral cues ency has been observed between studies for (Watson, Newton-Mora, & Pirkle, 2016), and the P300 component, which supports the the effect observed by Petit and colleagues importance of this ERP in alcohol-related dis- (2013) was particularly patent in male binge orders (e.g., Ehlers et al., 2007). As a whole, drinkers. However, during a working mem- the studies on binge drinking showed a ory task that presented congruent, lure, and delayed latency for ERP components except incongruent conditions, no difference was for one; the faster P3a latency was inter- observed in binge drinkers at the P3 level, preted as more rapid detection from theoret- whereas control participants exhibited a ical assumptions that the early P300 mainly larger P3a for congruent stimuli (Park & Kim, reflects stimulus detection (Ehlers et al., 2018). Increased amplitudes were also found 2007). However, regarding amplitude, some for the N2b component in a visual working studies showed reduced amplitude (i.e., memory task, which could be explained by a fewer resources allocated, and thus impaired need for higher attentional resources to effi- processing), while others exhibited increased ciently perform the task (Crego et al., 2009); amplitude (i.e., more resources allocated, 134 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth and thus possible brain compensation). This on one occasion. Increased activity in the cer- dissociation between studies can be under- ebellum, thalamus, and insula was related to stood through the compensatory hypothesis, the number of drinking occasions per week further explained below. (Campanella et al., 2013). Moreover, some studies simultaneously showed reduced Insights from neuroimaging and increased activity across distinct brain In line with the section on electrophysiologi- regions in binge drinking (e.g., Schweinsburg cal studies, the current section focuses on et al., 2011; Squeglia et al., 2011), reduced functional brain modifications to allow a activation being interpreted as a reflection better understanding of the cerebral corre- of processing difficulty, whereas increased lates of behavioral impairments. Compared activation was generally observed in brain with controls, binge drinkers globally pre- regions not related to the ongoing task and sent modified brain activity during cognitive thus interpreted as a compensatory activ- tasks. Nevertheless, differential activations ity. In line with this finding, during a verbal can be observed, depending on the nature learning task, adolescent binge drinkers dis- of the paradigm, the mechanisms involved, played reduced activity in the inferior frontal and the stimuli presented (e.g., higher acti- and increased activity in the dorsal frontal vation during inhibition of alcohol-related and parietal brain regions (Schweinsburg et stimuli, Ames et al., 2014; reduced activation al., 2011). Of note, during working memory during inhibition of color shapes, Norman tasks, reduced activity was especially found et al., 2011). In decision-making tasks, vari- in women and increased activity in men ous results appeared, depending on the pro- (Squeglia et al., 2011). cesses measured (Cservenka & Brumback 2017): a risky decision-making process was Brief conclusion associated with reduced activation in the Previous sections underlined the cerebral dorsal striatum (Jones, Cservenka & Nagel modifications observed in young binge drink- 2016) and stronger impulsivity was related ers. Electrophysiological and neuroimaging to reduced activity in the prefrontal dor- studies seem to converge, showing distinct solateral cortex (Banca et al., 2016) among brain modifications according to the type binge drinkers. In an anticipated risk-taking of neurocognitive task. Hence, with both task, however, binge drinkers showed higher tools, inhibition for affective alcohol-related activities in the prefrontal, orbitofrontal, and stimuli (Ames et al., 2014; Petit et al., 2012) upper parietal dorsolateral cortex, associated was associated with increased brain activity. with risky responses (Worbe et al., 2014). Nonetheless, although it targeted different Interestingly, in an affective decision-making populations, inhibition during neutral pro- context (Iowa Gambling Task), reduced deci- cessing led to increased brain activity when sion-making abilities were observed through the electrophysiological components were increased activities in the left amygdala and explored (e.g., López-Caneda et al., 2012) and bilateral insula in binge drinkers compared reduced brain activity with neuroimaging with those in controls (Xiao et al., 2013); this measures (Norman et al., 2011). Regarding observation showed hyperactivity in affec- working memory, performance was related tive brain systems related to the processing to higher brain recruitment in binge drinkers of emotional and rewarding information in with both neuroimaging and electrophysi- the amygdala, as well as to the transforma- ological measures (Campanella et al., 2013; tion of physiological signals into feelings in Crego et al., 2009), which was interpreted as the insula. Enhanced brain activation was a compensatory mechanism. Concerning this also observed during a working memory task possible compensation, electrophysiological in binge drinking, where higher activity in results focus on the specific process at stake the dorsomedial prefrontal cortex was cor- (e.g., attentional component), whereas neu- related with the number of drinks consumed roimaging data contribute to the description Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 135 of which brain areas/networks are poten- task, binge drinkers presented reduced cere- tially recruited for compensation. Several bral activation in the regions usually involved cognitive functions should still be explored, in this memory processing (e.g., hippocam- however, to support the consistency between pal regions) and increased activation in other these techniques (e.g., decision making has regions (i.e., frontal and motor area), which to be examined with electrophysiology). In was not observed in control participants summary, independent of the neuroscience (Campanella et al., 2013; Schweinsburg et technique used, results have shown that al., 2011). This compensatory mechanism binge drinkers present cerebral modifica- would enable binge drinkers to maintain a tions of various intensities according to the relatively preserved performance in some neurocognitive domain explored. This pro- behavioral tasks, despite the presence of posal needs to be confirmed in future studies disturbed brain activities. The same pat- that target the same processes in populations tern of results was observed during the matched for age and alcohol consumption. processing of emotional stimuli (Maurage et al., 2013b). Recently, electrophysiologi- Questions and perspectives for cal explorations have also highlighted an future research enhanced amplitude of ERP components in Overall, this literature review has provided binge drinkers compared with that of con- important information about the behavioral trols, especially for attentional and execu- and cerebral impairments in executive abili- tive components, which was observed in the ties presented by binge drinkers, as well as absence of behavioral changes (e.g., Crego et possible emotional disturbances recently al., 2009; López-Caneda et al., 2012, 2014b). identified among this population. In view This can be explained by increased cerebral of these results, five key questions are dis- recruitment, which compensates for the dif- cussed below in terms of the development of ficulties associated with specific processing. this research field: (1) What reorganization Binge drinking among young people could occurs in the brain related to binge drink- therefore be associated with reorganiza- ing? (2) What is the causal link between tion of brain functioning rather than with binge drinking and related deficits? (3) Do global cerebral impairment. Moreover, some the deficits persist following changes in alco- behavioral impairments would be undetect- hol consumption? (4) Is there a transition able in young adults but could appear dur- between binge drinking and alcohol-related ing the chronification of excessive alcohol disorders? (5) What strategies can prevent or consumption. This proposal of compensa- reduce binge drinking habits? tory processes allows an understanding of the cerebral changes observed in binge What reorganization occurs in the brain drinkers and is in line with research show- related to binge drinking? ing this compensatory activity in patients As previously mentioned, neuroscience recovering from severe alcohol use disor- studies have emphasized various and some- ders (e.g., Padilla et al., 2011). Nevertheless, times contradictory results (e.g., reduced some studies have also highlighted reduced or increased activations), depending on the electrophysiological activities in the absence experimental paradigm chosen and the type of a behavioral counterpart (e.g., Maurage of processing explored. As a potential expla- et al., 2009), raising questions about which nation, increased activation can be inter- impairments are compensated for and how preted as a compensatory activity, which this compensation is indexed. An explora- would allow some behavioral impairments to tion of the mechanisms implicated in these be overcome. This proposal originated from increased, as opposed to reduced, brain the observation in neuroimaging research activities appears to be essential for a full and showed that, during a working memory understanding of this proposal. According to 136 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth previous work that suggested compensatory increased P3b observed in their study could activity in binge drinking (e.g., López-Caneda be explained by an imbalance in neural et al., 2012), such compensation is mostly activity due to repeated withdrawal experi- shown during executive processing (e.g., ences. The difference between reduced and inhibition). The studies that highlighted increased amplitude in ERP components reduced electrophysiological activities in the might thus be related to the age of binge absence of behavioral difficulty (e.g., Ehlers drinking onset, binge drinking first lowering et al., 2007; Maurage et al., 2009, 2012) these ERP amplitudes and then increasing used experimental paradigms that required them through the kindling effect in the long fewer executive resources (i.e., detection of run. This hypothesis is consistent with the emotional faces, oddball paradigm with neu- results of the study by Maurage et al. (2009) tral faces, and valence detection of affective that showed reduced P100, N2a, and P3b prosody). It might thus be hypothesized that components after 9 months of binge drink- these tasks did not allow identification of ing in youth who did not drink alcohol exces- behavioral impairments because of reduced sively at baseline. In the same vein, the study involvement of high-level abilities that are of Ehlers et al. (2007) targeted young people impaired in binge drinking, whereas they who had at least one binge drinking episode clearly indicated alterations at the cerebral in adolescence, which suggests a recent and level. This assumption should be further low binge drinking pattern. investigated, however, as other studies with simple paradigms have also shown a larger What is the causal link between binge P3 in binge drinkers (e.g., Crego et al., 2012). drinking and related deficits? An alternative hypothesis to explain the The current literature review has emphasized increased ERP amplitude among binge several cognitive and affective impairments drinkers may be related to the binge drink- in binge drinking, supporting the conclusion ing pattern itself. It has been proposed that that these difficulties are not just observed alcohol withdrawal induces specific cerebral in severe alcohol use disorders. However, the changes observed through hyperexcitability question of the causal link between these of the central nervous system (i.e., the kin- impairments and excessive alcohol con- dling effect; see Becker, 1998, for a review). sumption remains open. Most of the avail- This kindling effect is a phenomenon typi- able work consists of cross-sectional research cally observed after repeated weak electrical and does not allow determination of whether stimulation of the brain that initially does these impairments are present before the not produce an effect; repetition leads to development of excessive alcohol consump- the appearance of brain modifications, sug- tion (i.e., play a causal role in the emergence gesting sensitization to the stimulation. It of binge drinking habits) or result from the has thus been proposed that the repetition alcohol neurotoxic effect associated with of alcohol withdrawal induces a kindling binge drinking habits. This question needs to process (Becker, 1998). Current views clearly be explored through additional research and recognize that binge drinking is character- literature reviews that focus on adolescents ized by multiple withdrawals (Courtney & and young adults. Polich, 2009), which leads to brain distur- bances in several areas, such as the amyg- The presence of vulnerabilities in dala or the frontal cortex (Stephens & Duka, binge drinkers 2008). This proposal has been supported by Some studies have revealed the presence animal studies, showing increased neural of impairments or vulnerabilities that have excitability following repeated withdrawals potentially been identified as a cause of (e.g., Duka et al., 2004). Accordingly, Crego binge drinking. These antecedents have and colleagues (2012) proposed that the been mainly observed in neurophysiological Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 137 research and would explain the engagement group comparisons), and thus did not allow in excessive alcohol consumption in youth exploration of hazardous binge drinking. (e.g., López-Caneda et al., 2012). More pre- Moreover, no information was collected cisely, studies have shown reduced fronto- about potential changes in the performance parietal activations in adolescents prior to of these participants at follow-up, thus pre- any alcohol consumption, and these cerebral venting definitive conclusions regarding the activities were identified as predictors of sub- causal link. sequent binge drinking (Norman et al., 2011; Wetherill et al., 2013). Similarly, with partici- Behavioral and cerebral impairments as a pants who were already alcohol consumers, consequence of binge drinking overactivation in the insula, dorsal striatum, Some studies have also supported the inverse ventromedial prefrontal, anterior cingulate, relationship and have proposed that the and orbitofrontal cortex during viewing of impairments observed in binge drinkers are alcohol cues predicted the transition toward the direct consequence of alcohol consump- binge drinking 1 year later (Dager et al., 2014). tion. One study that targeted adolescent low At the behavioral level, some studies have drinkers indicated that alcohol consumption also addressed this question by recruiting 4 years later (mean = 54 g per week at fol- adolescents before the initiation of binge low-up when participants were 18 years old) drinking. The results observed are some- was not predicted by cognitive performance times unexpected; a study that targeted ado- (inhibitory control and shifting) or brain lescents between 11 and 19 years old and activation (Jurk et al., 2016), suggesting that considered four follow-up times showed, both cognitive impairments and brain modi- for example, no difference regarding execu- fications are the consequences of alcohol tive maturation between participants who consumption rather than its cause. remained teetotalers and those who initi- First, this proposal is supported by neu- ated binge drinking habits (Boelema et al., roimaging studies that showed that binge 2016). These findings can be related to the drinking predicted cerebral alterations. In difficulty in detecting behavioral differences particular, a higher number of drinks con- at this early stage, combined with a need to sumed predicted smaller left hemisphere use basic tasks for the longitudinal obser- cerebellar white and gray matter, as well as vation of executive maturation. In working reduced right hemisphere cerebellar gray with adolescents, Gil-Hernandez et al. (2017) matter volume (Lisdahl et al., 2013). Research suggested that compensatory mechanisms also implicated gender, describing differen- may exist in the adolescent brain that allow tial brain modifications in men and women young people to achieve a performance simi- (e.g., Squeglia et al., 2012). This proposal that lar to that of their non-binge-drinking peers impairments are the consequences of binge at the behavioral level. This study showed drinking is supported more clearly by longi- executive difficulties in binge drinkers com- tudinal research. The study of Maurage and pared with controls only in a group of older colleagues (2009) identified a slowing down adolescents and young adults (19–22 years), of cerebral activity during the processing thus proposing that behavioral impairments of affective voices after 9 months of binge emerge only at this later stage of binge drink- drinking among participants who had similar ing habits. Among university students who brain functioning to that of controls at base- had already initiated alcohol consumption, line. Moreover, in a follow-up study of 8 years only risky decision making and not inhibitory from adolescence to adulthood, it appeared control predicted the binge drinking score that both binge drinking and a family history 18 months later (Bø et al., 2017). However, of severe alcohol use disorders were associ- this study adopted a continuous approach ated with alterations in the developmental to alcohol consumption (i.e., targeted the trajectory of impulsivity, reflected as diffi- binge drinking score and did not propose culty in delaying a reward in binge drinkers 138 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth with a family history of alcohol-related dis- or people with genetic risk factors (see Crews, orders (Jones, Steele & Nagel 2017). This 2008, for a review). study emphasized a similar performance at In summary, on the basis of animal and baseline between future binge drinkers and human studies, it can be proposed that controls. Only adolescents with a family his- impairments observed in young drinkers tory of alcoholism were impaired in impul- might simultaneously result from binge sive choices at first assessment. Interestingly, drinking and also be involved in the emer- adolescents with a family history of alcohol gence of chronic alcohol abuse. Investigators use disorders who did not engage in binge clearly identified that frontal impairments drinking did not present impairments at facilitate the subsequent loss of control in follow-up, whereas those who engaged in alcohol consumption and underlined the binge drinking showed stronger impair- possible difficulties in processing emotional ments. While targeting an at-risk population, events because of amygdala dysfunctions. namely, individuals with a family history Finally, this assumption of specific impair- of severe alcohol use disorders, this study ments due to the alternation between intoxi- confirms the proposal of previous studies cations and withdrawals is supported by a by indicating that the difficulty in delaying study by Dingwall, Maruff, and Cairney (2011) a reward is in particular strongly associated that showed that binge drinking was related with binge drinking and is related to the to impairments and patterns of recovery sim- number of alcohol doses consumed. ilar to those found in individuals with severe Second, the assumption that alterations alcohol use disorder. This study targeted constitute the consequences of binge drink- people involved in therapeutic programs for ing is also in accordance with the proposal excessive alcohol use and compared binge of Stephens and Duka (2008), who conveyed drinkers (drinking at least six alcohol doses that specific alternations between alcohol per occasion, less than four times a week), intoxication and withdrawal in binge drink- individuals with severe alcohol use disor- ing induce changes in neuronal plasticity der (drinking at least six alcohol doses per and result in cognitive and emotional impair- occasion, more than four times a week), and ments. This research encompasses several controls. Results showed that both groups studies conducted in patients with severe of alcohol users presented impairments in alcohol use disorders and in social drinkers visuo-motor and learning skills, as well as who had binge drinking episodes (see Duka in memory and executive functions. While et al., 2004, for more details). It showed visuo-motor difficulties persisted in the long both executive impairments and altered term (i.e., at 11 months follow-up) in the two conditioned responses, potentially related groups of drinkers, recovery was observed for to dysfunctions in the frontal regions and other processes within the four detoxifica- amygdala, and directly related to the number tion weeks. Although it did not focus on the of withdrawals. Notably, to test the proposal specific relationship with withdrawal epi- that behavioral and brain impairments were sodes, this study suggests that alcohol alters associated with alcohol consumption, stud- cognitive and motor functioning in a similar ies were conducted that involved animals way to that in excessive episodic or chronic exposed to specific alternations between drinking patterns. intense drinking and withdrawal. Findings As a whole, it is clear that the neurotoxic supported that binge drinking leads to effects of alcohol, and potentially the spe- impaired functioning in the frontal corti- cific alternation between intoxication and ces and amygdala (Stephens & Duka 2008), withdrawal, induce brain damage, resulting leading to neurodegeneration similar to in impairments among binge drinkers. Most that seen in severe alcohol use disorders. In studies in the current literature support such human populations, this deleterious effect a causal direction. However, it also appears seems particularly important in adolescents that some factors, present before the start Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 139 of alcohol consumption, can predispose an (Wechsler Memory Scale) in stable binge individual to engage in excessive alcohol drinkers, non-binge drinkers, and ex-binge consumption (e.g., modification in execu- drinkers. Results showed that, compared with tive brain networks). This effect was mainly non-binge drinkers, binge drinkers presented investigated in neuroscience studies, but impaired immediate and delayed recall. future work should specify these possible Interestingly, in the midterm (after about 2 predispositions with combined behavioral years), ex-binge drinkers showed difficulties and cerebral measures and target the mecha- in immediate and delayed recall but these nisms involved with sufficiently complex impairments disappeared in the long term paradigms. Complementary investigations (Carbia et al., 2017a). This study is interesting of the underlying mechanisms appear to be because it extends the time frame of evalua- crucial for a better understanding of the dis- tion described by previous studies. However, rupted functioning and causal relationships as frequently found in this type of longitu- in binge drinking. dinal evaluation, there was a strong experi- mental mortality in the successive steps, Do the deficits persist following changes resulting in a poor final sample size in some in alcohol consumption? subgroups at follow-up (e.g., n = 4 for the sta- An important question relates to the per- ble binge drinkers’ group at the third assess- sistence of these impairments when binge ment). Replications of these results are thus drinking becomes less frequent, as it is usu- necessary to support the absence of impair- ally observed in adulthood. Animal stud- ments in ex-binge drinkers in the long term. ies suggest potential brain recovery after Moreover, within a 4-year period, a study that binge drinking (Crews, 2008), but studies compared the same subgroups but evaluated with young human drinkers are lacking and decision making through the Iowa Gambling remain uncertain regarding the temporal Task showed no decision-making impair- framework and differential recovery across ment in stable binge drinkers or ex-binge cognitive processes. Longitudinal studies that drinkers (Carbia et al., 2017b). Therefore, focus on university students have shown that research on the persistence of impairments most binge drinkers maintain their excessive associated with binge drinking should be drinking habits throughout their university extended. Moreover, although in this sec- years, despite the associated negative con- tion we focused on behavioral performance, sequences (e.g., unwanted sexual relation- it has been shown that some impairments ships or violent behaviors; Martinez, Sher & are not detectable at the behavioral level and Wood 2014). However, it has been reported that they could be partially compensated for that, generally, binge drinking decreases at the cerebral level. Accordingly, it can be after university years, as supported by a hypothesized that the perpetuation of binge 9-year follow-up study (Gómez et al., 2017). drinking could lead to more pronounced People who were engaged in binge drinking behavioral impairments that can no longer but who return to stable alcohol consump- be compensated for. Conversely, it can also tion can still present behavioral impairments be suggested that, if alcohol consumption is in specific cognitive abilities such as verbal regulated with time, these processes could memory (Mota et al., 2013), but recover recover, as observed in the study of López- some brain processes such as those involved Caneda and colleagues (2012). Notably, the in inhibition performance (López-Caneda et recovery hypothesis is supported by research al., 2014b). Recent studies have also provided conducted in severe alcohol use disorders information about the evolution of memory that showed recovery in cognitive abilities and decision-making processes over time. A with the maintenance of early abstinence 6-year longitudinal study on binge drinking (Munro, Saxton, & Butters, 2000) but, sur- in late adolescence measured logical memory prisingly, with no complementary beneficial 140 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth effect of long-term abstinence (Fein et al., drinkers were far more likely (i.e., 19 times 2006). Nevertheless, recovery does not higher odds) to develop severe alcohol use appear to be total, as patients with long- disorders later in life than were non-binge term abstinence still show persistent impair- drinkers (Knight et al., 2002). This proposal ments in inhibitory and attentional control has moreover been tested in cohort studies (Naim-Feil et al., 2014), although, consist- over 6, 10, and 14 years, showing that binge ent with the findings reported by Fein et al. drinking in adolescents preceded (Bonomo (2006), abstinence duration was not related et al., 2004) and predicted (Jennison, 2004; to cognitive performance. These findings in Viner & Taylor 2007) severe alcohol use the context of severe alcohol use disorders disorders in young adulthood. In addition, thus align nicely with the preliminary results research with alcohol-dependent patients observed in binge drinking, showing partial revealed that almost half of them were binge recovery with reduced alcohol consumption drinkers in late adolescence (Enoch, 2006). but persistence of some impairments in the The continuum hypothesis thus postulates midterm. that binge drinking and severe alcohol use disorders are two successive steps of the Is there a transition between binge same phenomenon, possibly characterized drinking and alcohol-related disorders? by analogous qualitative impairments at The continuum hypothesis, as is often behavioral and brain levels. Therefore, these described in the literature for severe alcohol two disorders could be described as a linear use disorders, has been used to characterize worsening of cognitive and affective abilities the links between binge drinking and other that promote the maintenance of excessive alcohol consumption patterns in two distinct drinking habits and the possible transition ways. The first concerns the continuum of alco- toward severe alcohol use disorders. hol consumption patterns and proposes that binge drinkers are more at risk for developing The continuum of impairments severe alcohol use disorders than are light or The proposal of similar qualitative impair- moderate drinkers (e.g., Bonomo et al., 2004). ments between binge drinking and severe The second refers to the continuum of the alcohol use disorders was supported by stud- impairments observed in the two patterns of ies that suggested that the specific alterna- alcohol consumption and suggests that binge tion between intense intake and withdrawal, drinkers present qualitative impairments simi- which characterizes binge drinking, could lar to those of patients with severe alcohol lead to consequences similar to those of use disorders (e.g., Sanhueza, García-Moreno severe alcohol use disorders at cognitive and & Expósito 2011), regardless of the possible emotional levels (Stephens & Duka 2008). evolution of the drinking pattern (i.e., devel- Some studies have observed similarities in opment of severe alcohol use disorders). the impairments found among binge drink- ers and individuals with severe alcohol use The continuum between consumption disorders for cognitive processes such as patterns attention, memory, and executive func- From the very start of research on binge tions (Goudriaan et al., 2007; Hartley et al., drinking, several authors observed that 2004), as well as for cerebral functioning binge drinking is related to important (e.g., López-Caneda et al., 2017; Maurage et negative consequences (e.g., Wechsler et al., 2013b). While this hypothesis has not al., 1994), potentially leading binge drink- received direct experimental support from ers to be more at risk for severe alcohol use comparisons between binge drinkers and disorders. This was later confirmed by a patients with severe alcohol use disorders, large exploration of students from 119 col- an investigation of executive functioning leges and universities,­ indicating that binge showed that young adult binge drinkers Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 141 had a similar performance to that of elderly (Maurage et al., 2007) and cerebral (Maurage adults (Sanhueza et al., 2011), thus conveying et al., 2013c; Maurage et al., 2008a) markers the proposal of premature aging in individu- of impaired emotional cross-modal integra- als engaged in binge drinking. These find- tion, and altered inhibition, notably during ings reinforce the continuum hypothesis by the processing of alcohol cues (e.g., Noël et showing that the specific binge drinking pat- al., 2007). tern leads to strong impairments in critical Possible similarities between binge drinkers processes implicated in addiction, namely, and patients with severe alcohol use disorders executive functions (Crews & Boettiger were thus observed for lower level cognitive 2009). Globally, these findings confirm that abilities, electrophysiological processing of binge drinking has deleterious consequences error detection (performance monitoring), at several levels and could belong to the and some emotional abilities. Regarding whole spectrum of alcohol-related disorders, attentional networks, the same paradigm in particular because of the alternations has been used in binge drinking and severe between intoxication and withdrawal. alcohol use disorders, and the results were To develop further insights into this ques- similar, showing specific difficulty in execu- tion, some studies have been conducted tive control of attention (Lannoy et al., 2017a; on binge drinking with paradigms that had Maurage et al., 2014). However, binge drink- already been used among patients who had ing was also characterized by an impaired severe alcohol use disorders, thus allow- alerting network (Lannoy et al., 2017a). ing indirect but interesting comparisons. Regarding this result, whereas binge drinkers Findings globally underline that binge drink- were asked to abstain from alcohol during the ers are characterized by various impairments, 3 days before the experiment, participants supporting the presence of alterations that were all engaged in a stable binge drinking are comparable to those observed in severe pattern and patients with severe alcohol use alcohol use disorders. Nevertheless, these disorders were recruited during their third findings emphasize that the difficulties week of detoxification (Maurage et al., 2014), found in binge drinkers are related to spe- which could potentially explain the difference cific processes: in the alerting component. At the electro- physiological level, comparable results were • Performance monitoring difficulties but observed through an enhanced Error-Related no global inhibition alterations (Bø et al., Negativity in abstinent patients with severe 2016a; Lannoy et al., 2017b; Lannoy et alcohol use disorders (Padilla et al., 2011) al., 2018a; Smith & Mattick, 2013). and binge drinkers (Lannoy et al., 2017b), • Alerting and executive control of atten- indexed as compensatory activity. Finally, tion but no general attentional impair- regarding emotional processing, poorer emo- ment (Hartley et al., 2004; Lannoy et al., tional abilities were found for the processing 2017a; Sanchez-Roige et al., 2014). of various emotions, both in severe alcohol • Emotional recognition only for complex use disorders (e.g., Kornreich, 2002; Maurage morphed stimuli (Lannoy et al., 2018b). et al., 2011) and binge drinking (Lannoy et • Cerebral modifications during emo- al., 2018b). Moreover, while binge drink- tional processing, but no strong behav- ers presented cerebral reorganization rather ioral impairment (Huang et al., 2017; than clear impairments (e.g., Huang et al., Maurage et al., 2009), notably for cross- 2017; Lannoy et al., 2018c), comparable dif- modal integration (Lannoy et al., 2018c). ficulties were found in binge drinking and severe alcohol use disorders: disrupted cross- In severe alcohol use disorders, more global modal integration, differential processing for deficits were found, such as general executive anger (Maurage et al., 2008a; Maurage et al., impairment (Brion et al., 2017a), behavioral 2008b), and specific difficulty in processing 142 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth incongruent cross-modal trials (Brion et al., taking into account the recent findings that 2017b). Table 3 summarizes the similarities show heterogeneity in binge drinking profiles and dissimilarities between binge drinking (Gierski et al., 2017; Lannoy et al., 2017d). and severe alcohol use disorders regarding These results underline that binge drinkers the cognitive functions explored in this paper. are not a unitary group, showing that some As a whole, mixed results are currently students are instead involved in a recrea- reported regarding the continuum hypothe- tional pattern of consumption, while others sis, several studies showing qualitatively simi- are clearly identified as being implicated in lar impairments in the targeted processes, but a more dangerous alcohol consumption pat- also indicating differential and more specific tern. Accordingly, it could be hypothesized underlying mechanisms among binge drink- that intense binge drinkers persist in exces- ers. First, the presence of more pronounced sive alcohol consumption and develop cog- impairments in severe alcohol use disorders nitive and emotional difficulties, which lead can be explained by the repeated impact them to poorly regulate their drinking behav- of alcohol consumption (Crews, 2008), as iors and therefore evolve toward severe alco- patients were drinking alcohol excessively for hol use disorder, as has been underlined in a long period and were potentially ex-binge previous longitudinal findings (e.g., Bonomo drinkers (Enoch, 2006). Moreover, the contin- et al., 2004). Three main research perspectives uum hypothesis cannot be discussed without might thus be developed for future research:

Table 3: Comparison between binge drinking and severe alcohol use disorders.

Cognitive function Sub-components Binge drinking Severe alcohol Comparison use disorders Attentional abilities Alerting Impaired Preserved x Orienting Preserved Preserved V Executive control Impaired Impaired V Executive abilities Shifting Preserved Impaired X Updating Preserved Impaired X Inhibition Impaired Impaired v Error-monitoring Modified Modified V Emotional abilities Emotional decoding Impaired Impaired v Anger processing Modified Impaired v Happiness processing Preserved Preserved V Crossmodal abilities Crossmodal integration Preserved Impaired X Congruent stimuli processing Modified Impaired v Incongruent stimuli processing Modified Impaired v Legend: V = comparable, v = potentially comparable, needs further investigation, X = different, x = potentially different, needs further investigation. Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 143

1. The exploration of cognitive and affec- increase the intrinsic motivation to change tive impairments in different subgroups through ambivalence exploration and reso- of binge drinkers, differing in alcohol lution (Yurasek et al., 2015). This tool is par- consumption patterns. This subgroup ticularly useful with binge drinkers, as they comparison could be based on variation usually perceive few negative consequences in binge drinking criteria from cluster associated with their consumption. Second, analysis and would allow the targeting intention implementation aims to help indi- of profiles of at-risk binge drinkers. viduals to learn a new and adapted response 2. A direct exploration of similarities when confronted with situations previously and differences between binge drink- associated with a maladaptive one, such ing and severe alcohol use disorders as excessive alcohol consumption. Results to compare, beyond the continuum of showed that students who took part in an consumption patterns, the variation of intention implementation program reported existing impairments. This exploration reduced alcohol consumption and less binge could be made through the comparison drinking behavior 1 week later (Norman & between binge drinkers, recently detox- Wrona-Clarke, 2016). Expectancy challenge ified patients, and matched control is mainly used with adolescents and aims to participants. This design would allow modify dysfunctional expectancies toward determination of the position of binge alcohol by proposing that participants drinkers compared with a control group drink a beverage (alcohol or placebo) with- of young moderate drinkers, a control out knowing its content and then engage group of older but healthy participants in social activities with other adolescents. A with moderate alcohol consumption, meta-analysis showed effects of expectancy and a group of patients with severe challenge but mainly in the short term, alcohol use disorders. with no maintenance at 4-week follow-up 3. In line with previous studies (e.g., (Scott-Sheldon et al., 2012). These strategies Bonomo et al., 2004; Jennison, 2004), have therefore demonstrated their potential longitudinal studies with multiple efficiency, but results should be confirmed testing sessions starting during early through longer follow-up periods. adolescence to explore the mutual In addition to preventive intervention, influences between binge drinking impaired cognitive processes can be targeted habits, cognitive impairments, and the in rehabilitation programs. Inhibition train- potential appearance of severe alcohol ing for alcohol-related cues has been pro- use disorders. posed, mostly through a Go/No-Go task with a No-Go alcohol condition in which partici- What strategies can prevent and reduce pants learn to inhibit their motor response binge drinking habits? when confronted with alcohol-related cues Several interventions have been proposed to (Houben et al., 2011). The study evaluated prevent binge drinking and, more globally, the impact of such training on alcohol con- excessive alcohol consumption among young sumption immediately after the task in a real people. In this section, we briefly describe situation and with self-reported measures in the interventions that aim to reduce alcohol the following week. After inhibition training consumption and to avoid the emergence of for beer cues, hazardous drinkers presented binge drinking habits. Specific tools to reha- decreased alcohol consumption (both in bilitate the cognitive processes impaired in free drinking following the task and in their binge drinking, particularly inhibitory con- weekly use). Moreover, conversely, partici- trol, are then addressed. pants in the control condition (“Go” alcohol) Different strategies to reduce alcohol con- reported increased alcohol consumption in sumption have shown promising results. the following week. Nevertheless, propos- First, motivational intervention aims to ing the same paradigm in two sessions, and 144 Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth comparing results with those of an active applied to the right inferior frontal cortex control group (i.e., online personalized during inhibition of prepotent response feedback based on alcohol consumption), (Campanella et al., 2017). The same inhibi- Bowley and colleagues (2013) were not able tion task and another control task (facial to confirm these results. They indicated that detection) was then performed with an elec- participants in both active training groups troencephalogram recording, allowing the (feedback intervention and inhibition train- observation of N2 and P3 components from ing) drank less, but only in the test presented the subtraction between Go and No-Go trials. after the training, with no significant differ- Results indicated no significant difference at ence in follow-up self-reported alcohol con- the behavioral level between tDCS and sham sumption (Bowley et al., 2013). These results conditions. However, a reduction in elec- were also reported in a recent study that com- trophysiological activity related to the P3 pared inhibition training for alcohol cues component was found, suggesting that tDCS and alcohol approach modification training allowed a decrease in the resources recruited (Di Lemma & Field, 2017). Both interven- to efficiently perform the task (Campanella tions appeared to have the same efficacy in et al., 2017). laboratory settings, but these effects did not extend to real-life situations. These findings Conclusion thus show preliminary interesting results, This review paper offered an overview of the but there is a clear need for future work literature on the executive and emotional before a conclusion can be drawn regarding impairments found in binge drinkers by the clinical efficiency of such programs in describing behavioral, electrophysiological, binge drinking. and neuroimaging studies, as well as by criti- Finally, our review paper underlines some cally discussing five key issues identified in brain modifications and the presence of dif- this research field. In particular, we empha- ficulties even in the absence of behavioral sized that the impairments observed in binge impairments. From this perspective, there is drinkers are mainly related to inhibition and also a new line of research that focuses on sometimes not indexed at the behavioral neuroscience-based intervention techniques level but detectable through cerebral modi- such as neuromodulation [e.g., repeated fications. Moreover, difficulties in process- transcranial magnetic stimulation and tran- ing emotional content are also detected at scranial direct current stimulation (tDCS)]. both the behavioral and the neurophysi- These noninvasive techniques allow stimu- ological level. From these findings, we have lation of specific brain areas to improve attempted to offer a better understanding of targeted cognitive abilities and promote the cerebral deficits observed in binge drink- compensation for some difficulties. Studies ers by comprehensively describing the com- with binge drinkers showed craving reduc- pensatory hypothesis and the kindling effect. tion after tDCS stimulation of the left dor- We have also questioned the causal relation- solateral prefrontal cortex during simple ship between excessive alcohol use and reading (den Uyl, Gladwin, & Wiers, 2015), cognitive/affective impairments or cerebral but no effect was found on implicit asso- modifications, as well as highlighting that ciations and alcohol approach tendencies. the binge drinking pattern might constitute This research thus represents an interesting a specific risk factor for these impairments. avenue, but the specific effects still need to On the other hand, some predispositions be determined. To this end, ERP could be could exist and should be taken into account useful in enabling the exploration, with high in future studies. We then reviewed the few temporal resolution, of the specific mecha- studies that have explored whether deficits nisms modulated following transcranial persist after binge drinking cessation and stimulation (Miniussi, Brignani, & Pellicciari, proposed that, although encouraging results 2012). With healthy participants, tDCS was have been observed, there is an urgent need Lannoy et al: Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth 145 to comprehensively investigate this ques- binge drinking and depression among tion. Next, we discussed the continuum Canadian youth: Prevalence, patterns, hypothesis, suggesting a link between binge and suicidality. Alcohol, 46(2), 165–172. drinking and severe alcohol use disorders. DOI: https://doi.org/10.1016/j.alco- We have shown that, while these two alcohol hol.2011.07.001 consumption patterns share several com- Banca, P., Lange, I., Worbe, Y., Howell, N. mon features, binge drinking is associated A., Irvine, M., Harrison, N. A., Voon, with more limited and specific impairments. V., et al. (2016). Reflection impulsivity in Concrete proposals to further answer this binge drinking: Behavioural and volumet- question, which constitutes an important ric correlates: Impulsivity in binge drink- topic for both fundamental and clinical pur- ing. Addiction Biology, 21(2), 504–515. poses, have also been suggested. Finally, we DOI: https://doi.org/10.1111/adb.12227 described clinical perspectives addressed Becker, H. C. (1998). Kindling in Alcohol through prevention and intervention strat- Withdrawal. Research World, 22(1), 9. egies. Overall, promising results have been Bø, R., Aker, M., Billieux, J., & Landrø, N. shown, but they should be further specified, I. (2016a). Binge Drinkers Are Fast, Able explored in greater depth, and evaluated by to Stop – but They Fail to Adjust. Journal using longer follow-up periods. of the International Neuropsychological Society, 22(01), 38–46. DOI: https://doi. Acknowledgements org/10.1017/S1355617715001204 This project was supported by the Belgian Bø, R., Billieux, J., Gjerde, L. C., Eilertsen, Fund for Scientific Research (F.R.S.-FNRS, E. M., & Landrø, N. I. (2017). Do Execu- Belgium) and a grant from the Fondation tive Functions Predict Binge-Drinking pour la Recherche en Alcoologie (FRA), but Patterns? Evidence from a Longitudi- these funds did not exert any editorial direc- nal Study in Young Adulthood. Fron- tion or censorship on any part of this article. tiers in Psychology, 08. DOI: https://doi. This review paper was written on the basis of org/10.3389/fpsyg.2017.00489 several chapters of the PhD thesis of the first Bø, R., Billieux, J., & Landrø, N. I. (2016b). author. 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How to cite this article: Lannoy, S., Billieux, J., Dormal, V., & Maurage, P. (2019). Behavioral and Cerebral Impairments Associated with Binge Drinking in Youth: A Critical Review. Psychologica Belgica, 59(1), 116–155. DOI: https://doi.org/10.5334/pb.476

Submitted: 07 September 2018 Accepted: 19 February 2019 Published: 29 March 2019

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