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Alcohol Use Disorder Displays Trait-Related Reductions in Prosocial Decision-Making

Open AccessPublished:May 18, 2022DOI:https://doi.org/10.1016/j.bpsc.2022.05.002

      Abstract

      Background

      Alcohol use disorder (AUD) is associated with deficits in social cognition, but the relationship between harmful alcohol use and the processes underlying interactive social behavior is still unknown. We hypothesized that prosocial decision-making is reduced in AUD and that individual differences in the underlying processes are key to better understand these reductions.

      Method

      In one laboratory study (Swedish participants, n=240) and one confirmatory online study (American participants, n=260), we compared young adults with AUD to age-, gender-, and education-matched healthy controls on six facets of prosocial decision-making. We used standardized behavioral economic tasks, namely: Dictator Game, Ultimatum Game, Trust Game, and Third-Party Game. To better understand the expected differences in prosociality, we evaluated attention by tracking eye-gaze, decision response time, clinical symptoms and social cognition.

      Results

      Altruism (Lab study: p = .007; Online study: p < .001), Fairness (Lab study: p = .003; Online study: p = .007), and Reciprocal trust decisions (Lab study: p = .007; Online study: p = .039) were reduced in AUD compared to healthy controls whereas Trust, and Third-party punishment and compensation were comparable in both studies. Reduced prosociality was associated with attending to the selfish response option, faster response time, and moral attitudes, while dissociated from both psychiatric symptoms and drinking history in AUD.

      Conclusions

      Individuals with AUD have trait-related reductions in prosocial decision-making that do not vary with drinking history or psychiatric symptom load. These reductions were confined to one-to-one interaction accompanied by differences in attention, decision-time and moral attitudes.

      Keywords

      Introduction

      The study of social interaction in the initiation and maintenance of alcohol use disorder (AUD) has been highlighted as one of the most pressing concerns in current addiction research (
      • Heilig M.
      • Epstein D.H.
      • Nader M.A.
      • Shaham Y.
      Time to connect: bringing social context into addiction neuroscience.
      ). Despite this, research on social cognition in AUD (
      • Quednow B.B.
      Social cognition in addiction.
      ,
      • Bora E.
      • Zorlu N.
      Social cognition in alcohol use disorder : a meta-analysis.
      ) has largely omitted the study of prosocial behavior which is key to a healthy social life (
      • Cotter J.
      • Granger K.
      • Backx R.
      • Hobbs M.
      • Looi C.Y.
      • Barnett J.H.
      Social cognitive dysfunction as a clinical marker: A systematic review of meta-analyses across 30 clinical conditions.
      ), and could aid in contributing to the reduction of harmful alcohol use (
      • Heilig M.
      • Epstein D.H.
      • Nader M.A.
      • Shaham Y.
      Time to connect: bringing social context into addiction neuroscience.
      ). We addressed this gap in existing research by applying a social decision-making framework to understand the processes underlying trade-offs between prosocial and selfish choices in AUD.
      To date, the majority of research on social behavior in AUD has used self-report measures, and studies using objective measures during experimental social interactions are scarce (
      • Quednow B.B.
      Social cognition in addiction.
      ,
      • Bora E.
      • Zorlu N.
      Social cognition in alcohol use disorder : a meta-analysis.
      ). This is a limitation, because self-report measures fail to capture important aspects of actual social behavior, such as real-time markers of attention, response time, and decision outcomes with relevance to others and self (
      • Yamagishi T.
      • Matsumoto Y.
      • Kiyonari T.
      • Takagishi H.
      • Li Y.
      • Kanai R.
      • Sakagami M.
      Response time in economic games reflects different types of decision conflict for prosocial and proself individuals.
      ,
      • Rand D.G.
      • Greene J.D.
      • Nowak M a
      Spontaneous giving and calculated greed.
      ,
      • Teoh Y.Y.
      • Yao Z.
      • Cunningham W.A.
      • Hutcherson C.A.
      Attentional priorities drive effects of time pressure on altruistic choice.
      ). Objective measures of social decision-making (e.g. tasks in behavioral economics) examine social behaviors by quantifying the ability to evaluate and select a prosocial course of action from multiple alternatives during social interaction (e.g. altruistic, fairness and trust behavior) (

      Camerer CF, Fehr E (2005): Measuring Social Norms and Preferences Using Experimental Games: A Guide for Social Scientists. Found Hum Soc Econ Exp Ethnogr Evid from Fifteen Small-Scale Soc. https://doi.org/10.1093/0199262055.003.0003

      ,
      • Böckler A.
      • Tusche A.
      • Singer T.
      The Structure of Human Prosociality : Differentiating Altruistically Motivated , Norm Motivated , Strategically Motivated , and Self-Reported Prosocial Behavior.
      ). To our knowledge, only three studies to date have used a social decision-making task in individuals with AUD (
      • Brevers D.
      • Noël X.
      • Ermer E.
      • Dabiri D.
      • Verbanck P.
      • Kornreich C.
      Unfairness sensitivity and social decision-making in individuals with alcohol dependence: A preliminary study.
      ,
      • Brevers D.
      • Noël X.
      • Hanak C.
      • Verbanck P.
      • Kornreich C.
      On the relationship between emotional state and abnormal unfairness sensitivity in alcohol dependence.
      ,
      • Tsukue R.
      • Okamoto Y.
      • Yoshino A.
      • Kunisato Y.
      • Takagaki K.
      • Takebayashi Y.
      • et al.
      Do Individuals with Alcohol Dependence Show Higher Unfairness Sensitivity? The Relationship Between Impulsivity and Unfairness Sensitivity in Alcohol-Dependent Adults.
      ). These studies showed that individuals with AUD compared to healthy controls (HC) more often rejected unfair offers from others. However, no prior work has extended these findings to examine whether individuals with AUD are more unfair themselves.
      Social decision-making tasks have previously been successfully applied to understand deficits in other psychiatric disorders, such as cocaine use disorder (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ) and attention deficit hyperactivity disorder (ADHD) (
      • Ma I.
      • Lambregts-Rommelse N.N.J.
      • Buitelaar J.K.
      • Cillessen A.H.N.
      • Scheres A.P.J.
      Decision-making in social contexts in youth with ADHD.
      ), which display similar characteristics to AUD in terms of increased impulsivity. These studies have shown reduced altruistic behavior in comparison to healthy individuals using the Dictator Game (
      • Ma I.
      • Lambregts-Rommelse N.N.J.
      • Buitelaar J.K.
      • Cillessen A.H.N.
      • Scheres A.P.J.
      Decision-making in social contexts in youth with ADHD.
      ) or a combined Dictator/Distribution Game (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ). In contrast, studies on other psychiatric disorders, such as autism (
      • Sally D.
      • Hill E.
      The development of interpersonal strategy: Autism, theory-of-mind, cooperation and fairness.
      ) and schizophrenia (
      • Van’t Wout M.
      • Sanfey A.G.
      NIH Public Access.
      ) found no alterations using the Dictator Game. These applications across different psychiatric diagnostic groups reveal the relevance of deficits on prosocial tasks beyond conventional diagnostic boundaries, suggesting their usefulness also in AUD. Moreover, this approach resonates well with the Research Domain Criteria (RDoC) initiative, recommending the application of behavioral economic tasks in the search for more ecological valid social biomarkers in psychiatric disorders (

      National Institute of Mental Health (2016): Behavioral Assessment Methods for RDoC Constructs: A Report by the National Advisory Mental Health Council Workgroup on Tasks and Measures for Research Domain Criteria (RDoC). 167.

      ). In light of these considerations, we used a set of standardized behavioral economic tasks to investigate prosocial decision-making in individuals with AUD.
      Given that prosocial behavior is influenced by numerous state- and trait-related factors at the individual level, it is of key importance to go beyond simple group differences (e.g. AUD vs. healthy individuals) to understand underlying individual differences within the groups themselves (
      • Penner L.A.
      • Dovidio J.F.
      • Piliavin J.A.
      • Schroeder D.A.
      Prosocial Behavior: Multilevel Perspectives.
      ). For instance, visual attention is informative for prosocial decisions in being associated with an increased attendance towards stimuli representing prosocial (compared to selfish) choices (
      • Teoh Y.Y.
      • Yao Z.
      • Cunningham W.A.
      • Hutcherson C.A.
      Attentional priorities drive effects of time pressure on altruistic choice.
      ,
      • Pärnamets P.
      • Shuster A.
      • Reinero D.A.
      • Van Bavel J.J.
      A Value-Based Framework for Understanding Cooperation.
      ). Visual attention has also been shown to be trait-related in consistently influencing individual choice behavior across social and non-social task domains (
      • Smith S.M.
      • Krajbich I.
      Attention and choice across domains.
      ,
      • Thomas A.W.
      • Molter F.
      • Krajbich I.
      • Heekeren H.R.
      • Mohr P.N.C.
      Gaze bias differences capture individual choice behaviour.
      ). Response time is another individual level factor with relevance to prosocial decisions where a slower decision in general results in a more prosocial choice (
      • Teoh Y.Y.
      • Yao Z.
      • Cunningham W.A.
      • Hutcherson C.A.
      Attentional priorities drive effects of time pressure on altruistic choice.
      ,
      • Krajbich I.
      • Bartling B.
      • Hare T.
      • Fehr E.
      Rethinking fast and slow based on a critique of reaction-time reverse inference.
      ). Collectively, the influence of increased attention and response time on altered prosociality have both been suggested to operate through modulating the subjective value attributed to prosociality at the individual level (
      • Pärnamets P.
      • Shuster A.
      • Reinero D.A.
      • Van Bavel J.J.
      A Value-Based Framework for Understanding Cooperation.
      ,
      • Krajbich I.
      • Bartling B.
      • Hare T.
      • Fehr E.
      Rethinking fast and slow based on a critique of reaction-time reverse inference.
      ).
      Individual variability in drinking history for AUD individuals (e.g. days of abstinence, recent consumption level and duration of harmful drinking) may also inform whether there is a relationship between alcohol use patterns and altered prosociality. Such a relationship would suggest that altered prosociality in AUD individuals primarily depends on state-related fluctuations in drinking history. Conversely, a non-relation would suggest that the prosocial alterations are mainly trait-related in being independent of differences in drinking history, but rather indicative of some other underlying process (e.g. processes of social cognition or impulsivity). In sum, information on drinking history in individuals with AUD might help us to understand the role of prosocial deficits as state- or trait-related factor of the disorder.
      In the present study, we investigate six key facets of prosocial decision-making (altruism, fairness, trust, reciprocal trust, third-party punishment and third-party compensation) in young adults with AUD compared to a matched population of HC. To achieve this goal, we conducted two separate experiments (n=240 and n=260), including standardized behavioral economic tasks in two separate samples. Additionally, we investigated individual differences by assessing measures of attention, response time, clinical, and sociocognitive variables. We proposed two main hypotheses: Firstly, we hypothesized that young adults with AUD would exhibit reduced prosociality across all six facets of prosocial decision-making. Secondly, we hypothesized that reduced prosociality in AUD would be associated with (a) increased attention towards selfish stimuli and faster response time, (b) reduced empathy and moral attitudes, but dissociated from (c) drinking history in AUD.

      Methods and Materials

      Participants

      Participants were young adults (aged 18-24) with AUD, and age, gender and education matched HC for comparison. They were recruited as part of two separate studies: A Swedish laboratory study conducted at the Karolinska Institutet, comprising 120 AUD participants (50% females), and 120 HC participants (50% females), and an American online study comprising 124 AUD participants (47% females), and 136 HC participants (59% females) using the Prolific Research Platform (www.prolific.co). Details regarding power estimation, recruitment, and selection process are provided in Supplementary Methods.
      We screened individuals in both study samples by carefully assessing a range of inclusion and exclusion criteria’s (including exclusion of other substance use disorder, neuropsychiatric disorder, and severe psychiatric disorder, see Supplementary Methods for details). The AUD group fulfilled a minimum of 4 DSM-5 criteria of AUD (corresponding to a moderate or severe AUD) while the HC group fulfilled a maximum of 1 DSM-5 criteria of AUD (corresponding to no AUD). For the laboratory study, assessment of the clinical criteria was done by a licensed psychologist or a medical doctor using the MINI Neuropsychiatric Interview (
      • Sheehan D.V.
      • Lecrubier Y.
      • Sheehan K.H.
      • Amorim P.
      • Janavs J.
      • Weiller E.
      • et al.
      The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10.
      ), while for the online study assessment was self-rated by the participants using an established questionnaire (
      • Hagman B.T.
      Development and psychometric analysis of the Brief DSM-5 Alcohol Use Disorder Diagnostic Assessment: Towards effective diagnosis in college students.
      ).
      All participants were compensated for their participation with 3 movie vouchers (lab study) or $16 (online study), and an additional bonus compensation based on their decisions (see Supplementary Methods and Discussion for details).
      All participants provided informed consent and the procedures were in accordance with the Declaration of Helsinki. The laboratory study was approved by the Swedish Ethical Review Authority (Dnr: 2019-05123). No ethical approval was required for the online study as the Swedish Act concerning the Ethical Review of Research Involving Humans (2003:460) states that approval is needed only when personal data is handled. A pre-registration of the study including a general plan for analysis and collected measures that will be reported elsewhere can be found at: https://osf.io/uvhmq.

      Social Decision-Making Tasks

      Participants’ prosocial behavior were estimated by six behavioral economic tasks of social decision-making, namely: altruism using the Dictator Game (
      • Böckler A.
      • Tusche A.
      • Singer T.
      The Structure of Human Prosociality : Differentiating Altruistically Motivated , Norm Motivated , Strategically Motivated , and Self-Reported Prosocial Behavior.
      ,

      Camerer C (2003): Behavioral Game Theory: Experiments in Strategic Interaction. Princeton University Press.

      ); fairness using the Ultimatum Game (
      • Ma I.
      • Lambregts-Rommelse N.N.J.
      • Buitelaar J.K.
      • Cillessen A.H.N.
      • Scheres A.P.J.
      Decision-making in social contexts in youth with ADHD.
      ,
      • Kahneman D.
      • Knetsch J.L.
      • Thaler R.H.
      Fairness and the Assumptions of Economics.
      ); trust, and reciprocal trust using the Trust Game (
      • Böckler A.
      • Tusche A.
      • Singer T.
      The Structure of Human Prosociality : Differentiating Altruistically Motivated , Norm Motivated , Strategically Motivated , and Self-Reported Prosocial Behavior.
      ,
      • Peysakhovich A.
      • Rand D.G.
      Habits of Virtue : Creating Norms of Cooperation and Defection in the Laboratory.
      ); third-party punishment and compensation using the Third-Party Game (
      • Böckler A.
      • Tusche A.
      • Singer T.
      The Structure of Human Prosociality : Differentiating Altruistically Motivated , Norm Motivated , Strategically Motivated , and Self-Reported Prosocial Behavior.
      ,
      • Peysakhovich A.
      • Rand D.G.
      Habits of Virtue : Creating Norms of Cooperation and Defection in the Laboratory.
      ). Each task consisted of 2-5 trials, and were implemented in PsychoPy (lab study), and jsPsych (online study) (
      • de Leeuw J.R.
      jsPsych: a JavaScript library for creating behavioral experiments in a Web browser.
      ,
      • Peirce J.
      • Gray J.R.
      • Simpson S.
      • MacAskill M.
      • Höchenberger R.
      • Sogo H.
      • et al.
      PsychoPy2: Experiments in behavior made easy.
      ). Participants were informed that they would play online with a different and allegedly real interaction partner for each trial in each of the tasks (i.e., a series of independent “one-shot” games (

      Camerer CF, Fehr E (2005): Measuring Social Norms and Preferences Using Experimental Games: A Guide for Social Scientists. Found Hum Soc Econ Exp Ethnogr Evid from Fifteen Small-Scale Soc. https://doi.org/10.1093/0199262055.003.0003

      ), see Supplementary Methods for instructions and details). The tasks had a similar design and setup where individuals decided regarding the distribution of points for oneself and/or another participant (see Figure 1 and Supplementary Methods for illustrations). Prosocial behavior was for each task, operationalized as the per-trial number of points transferred to the other participant.
      Figure thumbnail gr1
      Figure 1Trust Game assessing reciprocal trust. Experimental timeline showing: A) connection established to other (new) participant, B-C) other participant chooses how many points to give (multiplied by 3) to playing participant, D-E) playing participant chooses how many points to give back to other participant. Areas-of-interest for the measurement of eye-gaze was recorded in D (i.e. the end-points on the response-scale, and the silhouettes representing the participants). Response time was recorded in D.

      Attention

      Attention was assessed during the social decision-making tasks in the lab study by recording eye-gaze using a SMI RED 250 tracking at 250Hz running on a dedicated computer system (
      • Pärnamets P.
      • Shuster A.
      • Reinero D.A.
      • Van Bavel J.J.
      A Value-Based Framework for Understanding Cooperation.
      ). We used the proportion of fixations during choice, and defined areas of interest in relation to the social stimuli of the screen, namely: the selfish and prosocial response option (i.e. ‘min’ and ‘max’ on the response bar, see Figure 1), and the silhouettes representing each respondent (i.e. ‘self’ and ‘other’). For details regarding data preprocessing and operational procedure, see Supplementary Methods.

      Response Time

      As a measure of deliberation during choice we recorded trial-by-trial response time data during the six tasks in both studies (
      • Krajbich I.
      • Bartling B.
      • Hare T.
      • Fehr E.
      Rethinking fast and slow based on a critique of reaction-time reverse inference.
      ). The recording occurred from the start of choice where the response bar was shown, to the end of choice, when the participant clicked the “continue” button following a desired response (see Figure 1).

      Self-Report Measures

      Alcohol and drug use were assessed with the Alcohol Use Disorder Identification Test (AUDIT) (
      • Bergman H.
      • Källmén H.
      Alcohol use among Swedes and a psychometric evaluation of the alcohol use disorders identification test.
      ) and Drug Use Disorder Identification Test (DUDIT) (
      • Berman A.H.
      • Bergman H.
      • Palmstierna T.
      • Schlyter F.
      Evaluation of the Drug Use Disorders Identification Test (DUDIT) in criminal justice and detoxification settings and in a Swedish population sample.
      ) respectively. Abstinence duration and alcohol use past 30 days were assessed using the timeline follow-back method (

      Sobell LC, Sobell MB (1992): Timeline follow-back: A technique for assessing self-reported alcohol consumption. In: Litten RZ, Allen JG, editors. Measuring Alcohol Consumption: Psychosocial and Biochemical Methods. Humana Press, pp 41–72.

      ) while alcohol craving was assessed using a single-item visual analogue scale (ranging from 0 to 100 asking “How much craving for alcohol do you experience right now?”) (
      • Khemiri L.
      • Steensland P.
      • Guterstam J.
      • Beck O.
      • Carlsson A.
      • Franck J.
      • Jayaram-Lindström N.
      The effects of the monoamine stabilizer (-)-OSU6162 on craving in alcohol dependent individuals: A human laboratory study.
      ) presented in conjunction to starting the first behavioral task (i.e. Dictator Game). Duration of harmful drinking was assessed using the single-item “For how long (years; months) would you consider that you have been drinking too much?”. Neuropsychiatric symptoms were assessed with the Adult ADHD Self-Report Scale-6 (
      • Kessler R.C.
      • Adler L.
      • Ames M.
      • Demler O.
      • Faraone S.
      • Hiripi E.
      • et al.
      The World Health Organization adult ADHD self-report scale (ASRS): A short screening scale for use in the general population.
      ) and the Autism Spectrum Quotient-10 (
      • Allison C.
      • Auyeung B.
      • Baron-Cohen S.
      Toward brief “red flags” for autism screening: The short Autism Spectrum Quotient and the short Quantitative Checklist in 1,000 cases and 3,000 controls.
      ). Psychiatric symptom load past week was assessed with the Depression Anxiety Stress Scales-21 (
      • Antony M.M.
      • Cox B.J.
      • Enns M.W.
      • Bieling P.J.
      • Swinson R.P.
      Psychometric properties of the 42-item and 21-item versions of the Depression Anxiety Stress Scales in clinical groups and a community sample.
      ).
      Empathy was assessed with the Questionnaire of Cognitive and Affective Empathy including separate subscales for its affective- (i.e. vicariously experience the emotional experience of others), and cognitive components (i.e. comprehending the emotional experience of others) (
      • Reniers R.L.E.P.
      • Corcoran R.
      • Drake R.
      • Shryane N.M.
      • Völlm B.A.
      The QCAE: A questionnaire of cognitive and affective empathy.
      ). Moral attitudes were assessed using the Oxford Utilitarianism Scale including the subscales of instrumental harm (i.e. impartially maximizing well-being by harming others), and impartial beneficence (i.e. impartially maximizing well-being at the cost of oneself) (

      Kahane G, C Everett JA, Earp BD, Caviola L, Faber NS, Crockett MJ, et al. (2017): Beyond Sacrificial Harm: A Two-Dimensional Model of Utilitarian Psychology Beyond Sacrificial Harm: A Two-Dimensional Model of Utilitarian Psychology. 0. https://doi.org/10.1037/rev0000093

      ).

      Statistical Analysis

      All models were estimated in R (version 4.04) using the lme4-package (version 1.1-26) (

      Bates D, Mächler M, Bolker B, Walker S (2014): Fitting Linear Mixed-Effects Models using lme4. eprint arXiv:14065823 67: 51.

      ), see Supplementary Methods for details. In our main analyses, we investigated group differences by conducting separate multilevel linear regression analyses for each of the six social decision-making tasks. For all tasks, the task response was our outcome variable which we modeled as a function of group (AUD vs Control, fixed effect) while variation across trials for each participant was modeled using a random intercept:
      TaskResponse ∼ Group + (1 | Participant)
      Moreover, in the tasks measuring Reciprocal trust, Third-party punishment and compensation an initial response was given by the other participant before the participant responded. We therefore included the other participants response in the models as an additional fixed effect and as a random slope (since the magnitude of the response varied across trials):
      TaskResponse ∼ Group + OtherResponse + (1 + OtherResponse | Participant)
      All models were fitted separately for the lab and online samples since our main interest was to identify group differences that were replicated in both samples. Given group differences in task performance across-samples, we assessed individual differences by investigating the unique contribution of attention, response time, clinical and sociocognitive variables by conducting one additional multilevel linear regression analysis per relevant task.

      Results

      Demographics

      The demographics and clinical characteristics of the AUD and HC individuals are presented in Table 1. The groups did not differ regarding matching variables of age, sex, and education with an exception for the online study where participants with AUD were slightly older and more educated but these differences had no effect on the main results (Supplementary Results S2-S3). The lab- and online study samples were similar in terms of mean number of fulfilled AUD criteria as well as the self-reported AUDIT score. That alcohol had been the main drug of choice during the past year was (apart from the clinical evaluation in the lab study) also confirmed by the low DUDIT scores in both samples (
      • Basedow L.A.
      • Kuitunen-Paul S.
      • Eichler A.
      • Roessner V.
      • Golub Y.
      Diagnostic Accuracy of the Drug Use Disorder Identification Test and Its Short Form, the DUDIT-C, in German Adolescent Psychiatric Patients.
      ).
      Table 1Demographics and Clinical Characteristics
      Lab StudyOnline Study
      Alcohol Use Disorder (n = 120)Healthy Control (n = 120)Alcohol Use Disorder (n = 124)Healthy Control (n = 136)
      Characteristicsp
      Analysis of variance for continuous variables, or χ2 for categorical variables
      p
      Analysis of variance for continuous variables, or χ2 for categorical variables
      Age, Mean (SD)21.4 (2.0)21.0 (2.0).08321.8 (1.7)20.8 (2.1)<.001
      Gender, Male, No. (%)60 (50.4)60 (50.0)1.00064 (52.9)55 (41.4).086
      Socioeconomic Status, Education
       Undergraduate Degree or Higher, No. (%)43 (35.8)30 (25.0).09287 (70.2)60 (44.1)<.001
      Socioeconomic Status, Income.828.073
       Don't Meet Basic Expenses, No. (%)4 (4.5)3 (2.5)9 (7.3)12 (8.8)
       Just Meet Basic Expenses, No. (%)8 (9.1)9 (7.5)36 (29.0)23 (16.9)
       Meet Needs with a Little Left, No. (%)48 (54.5)67 (55.8)48 (38.7)52 (38.2)
       Live Comfortably, No. (%)28 (31.8)41 (34.2)31 (25.0)49 (36.0)
      Nonverbal IQ Score
      IQ Score were assessed using the WAIS-IV vocabulary and working memory/digit span subtests respectively (40)
      , Mean (SD)
      26.4 (4.4)25.9 (4.0).435NANA
      Verbal IQ Score
      IQ Score were assessed using the WAIS-IV vocabulary and working memory/digit span subtests respectively (40)
      , Mean (SD)
      21.7 (7.6)21.8 (7.5).939NANA
      Psychiatric Attributes and Substance UseMean (SD)Mean (SD)p
      Analysis of variance for continuous variables, or χ2 for categorical variables
      Mean (SD)Mean (SD)p
      Analysis of variance for continuous variables, or χ2 for categorical variables
      Adult ADHD Self-Report Scale-612.0 (3.9)9.4 (3.6)<0.0019.3 (4.1)7.5 (3.8)<.001
      Autism Spectrum Quotient-102.8 (1.6)3.0 (1.8).3133.2 (1.8)3.6 (2.0).086
      Depression Anxiety Stress Scales-21
       Anxiety3.5 (3.3)1.2 (1.6)<.0014.7 (3.7)2.1 (2.6)<.001
       Depression6.6 (4.5)2.7 (2.4)<.0017.9 (5.3)4.4 (4.3)<.001
       Stress6.6 (4.0)3.7 (3.0)<.0017.1 (4.5)4.0 (4.1)<.001
      Alcohol Use Disorder Identification Test17.3 (4.5)1.7 (1.8)<.00117.9 (6.2)1.0 (1.4)<.001
      Alcohol Use Disorder Criterias, No.6.2 (1.8)NA
      Max 1 criterion for alcohol use disorder required for participation
      6.5 (2.1).1 (.3)<.001
      Drinking Too Much, No. Months29.4 (26.6)1.0 (3.9)<.00127.5 (25.3).8 (6.7)<.001
      Alcohol Binges, Past 6-months22.8 (19.1)NA
      Max 1 binge episode required for participation
      19.1 (21.6).1 (.3)<.001
      Alcohol Consumption, Past 30-days, No.51.5 (25.4)1.4 (3.0)<.00165.1 (40.1)2.3 (4.6)<.001
      Alcohol Abstinence, No. Days3.4 (2.3)23.4 (10.0)<.0013.1 (4.4)23.1 (12.4)<.001
      Alcohol Craving at Time of Testing18.5 (18.5)1.0 (7.2)<.00145.3 (26.8)2.1 (6.9)<.001
      Drug Use Disorder Identification Test3.6 (4.5).2 (.8)<.0011.6 (2.2)
      Max 1 binge episode required for participation
      .3 (.9)
      The online study used the short-form version of the Drug Use Disorder Identification Test
      <.001
      Cognitive Attributes
      Oxford Utilitarianism Scale
       Impartial Beneficence20.2 (6.0)20.2 (6.2).95819.4 (6.2)20.0 (5.8).441
       Instrumental Harm16.1 (4.7)14.9 (4.9).05714.9 (4.6)14.7 (4.9).695
      Questionnaire of Cognitive and Affective Empathy
       Affective Empathy34.8 (5.3)35.3 (5.4).49735.6 (5.8)35.4 (5.8).800
       Cognitive Empathy54.8 (6.2)56.5 (6.6).04159.9 (8.2)57.6 (8.5).023
      a Analysis of variance for continuous variables, or χ2 for categorical variables
      b Max 1 criterion for alcohol use disorder required for participation
      c Max 1 binge episode required for participation
      d The online study used the short-form version of the Drug Use Disorder Identification Test
      e IQ Score were assessed using the WAIS-IV vocabulary and working memory/digit span subtests respectively (
      • Benson N.
      • Hulac D.M.
      • Kranzler J.H.
      Independent Examination of the Wechsler Adult Intelligence Scale-Fourth Edition (WAIS-IV): What Does the WAIS-IV Measure?.
      )

      Group Differences in Prosocial Decision-Making

      We found, across samples, evidence for a significant reduction of prosocial decision-making in AUD (see Table 2 for effect estimations, and Figure 2 and Supplementary Results S1 for details). Specifically, the AUD group exhibited reduced altruistic (Lab study: β = 3.17, p = .007; Online study: β = 4.53, p < .001), fairness (Lab study: β = 1.61, p = .003; Online study: β = 2.30, p = .007), and reciprocal trust decisions (Lab study: β = 2.00, p = .007; Online study: β = 2.50, p = .039). However, we did not find any across-sample reduction in trust, third-party punishment, or third-party compensation. Given that the distribution of the response variable across tasks was not normal (Figure 2), we verified the robustness of our results in an additional set of analyses using square root and logarithmic transformations of the response variables (Supplementary Results S8). Moreover, we validated the group differences in each task by controlling for the responses in the other tasks which replicated the key results (Supplementary Results S9). Individuals were also consistently faster in making decisions on subsequent trials within the same task, but crucially this had no effect on decision outcomes (Supplementary Results S10). Finally, we exchanged the group variable in the main models to a continuous self-report measure on harmful alcohol use: AUDIT (
      • Bergman H.
      • Källmén H.
      Alcohol use among Swedes and a psychometric evaluation of the alcohol use disorders identification test.
      ), which showed comparable reduction in the same decisions indicating robustness across measurements (Supplementary Results S13).
      Table 2Multilevel Linear Regression Models for the Social Decision-Making Tasks
      Lab StudyOnline Study
      B (95% CI)pDB (95% CI)pD
      Altruistic Decisions
      Intercept17.81 (16.19-19.44)<2e-1615.00 (13.14-16.86)<2e-16
      HC3.17 (.88-5.47).007.354.53 (1.97-7.08)<.001.44
      Fairness Decisions
      Intercept22.54 (21.52-23.57)<2e-1621.05 (19.85-22.25)<2e-16
      HC1.61 (.15-3.06).031.292.30 (.65-3.94).007.35
      Trust Decisions
      Intercept24.49 (21.78-27.20)<2e-1618.34 (15.69-21.00)<2e-16
      HC-.90 (-4.73-2.93).646-.061.99 (-1.65-5.64).284.14
      Reciprocal Trust Decisions
      Intercept18.21 (17.05-19.37)<2e-1623.21 (21.19-25.24)<2e-16
      HC2.00 (.55-3.45).007.352.50 (.13-4.86).039.26
      Third-Party Punishment Decisions
      Intercept7.75 (6.38-9.11)<2e-166.17 (4.50-7.84)5.37e-12
      HC-.00 (-1.55-1.54).996<.01.28 (-2.00-2.57).809.03
      Third-Party Compensation Decisions
      Intercept17.62 (14.71-20.53)<2e-1614.00 (11.59-16.40)<2e-16
      HC3.77 (-2.23-(-).84).069.241.67 (-1.58-4.92).316.13
      Results are extracted from separate multilevel regression models and shows across the tasks of altruism, fairness, and reciprocal trust higher prosociality for the healthy control (HC) group compared to the alcohol use disorder group. In contrast, there is no group differences across the tasks measuring Trust, Third-party punishment and compensation, see Supplementary Results S1 for details.
      B, Beta estimate; CI, Confidence interval; D, Cohen’s d effect size
      Figure thumbnail gr2
      Figure 2Group differences on task measures of altruistic (A; B), fairness (C; D), and reciprocal trust decisions (E; F) showing a reduction in prosocial decision-making for the alcohol use disorder individuals. * p < .05, ** p < .01, *** p < .001
      Neuropsychiatric symptoms (e.g. ADHD), gender or education level had no consistent effect on our main results whereas higher household income had a positive effect on fairness decisions (Lab study: β = 5.58, p = .002; Online study: β = 4.92, p = .002), and symptoms of antisocial personality disorder a negative effect on reciprocal trust decisions (Lab study: β = -.90, p = .006), see Supplementary Results S3 and S6. Crucially, these results had no effect on the relationship between AUD and prosocial decision-making.

      Explaining Reduced Prosociality in AUD

      We performed a set of additional analyses on altruism, fairness, and reciprocal trust, given that we identified consistent group differences in these task measures. Apart from the measure of attention, the analyses were performed in both study samples.

      Attention

      The role of attentional processes in prosocial behavior were investigated by measuring the eye-gaze pattern in relation to the social stimuli of the screen (Supplementary Results S14, S17, S20). Attending the selfish response option was negatively associated with altruism (β = -48.81, p < .001), fairness (β = -25.79, p < .001), and reciprocal trust (β = -25.71, p < .001), Figure 3, also when separating the eye-gaze pattern made during the initial and final stage of each trial. For the measure of fairness, this effect was stronger in the AUD group as shown by an interaction effect (β = 19.95, p = .018). Interestingly, attending the silhouette representing oneself was positively associated with fairness (β = 8.51, p = .015), and reciprocal trust (β = 8.24, p = .039). No consistent effects were found for attending the prosocial response option, nor the silhouette representing the other participant.
      Figure thumbnail gr3
      Figure 3Eye-tracking results for alcohol use disorder and healthy control individuals respectively. Associations between prosocial decision-making and visually attending the selfish (i.e. ’minimal’) response option for altruistic (A), fairness (B), and reciprocal trust (C) decision-making showing reduced prosociality for individuals attending the selfish response option. *** p < .001

      Response Time

      Response time showed a negative effect on prosocial decisions across all three tasks such that individuals with faster response time trials had a stronger reduction in prosociality (Figure 4, (Supplementary Results S15, S18, S21). In particular, this reduction was for the lab study stronger for individuals in the AUD group compared to the HC group as shown by interaction effects (Altruism: β = -1.49, p = .076; Fairness: β = -1.79, p = .012; Reciprocal trust: β = -1.95, p = .002), whereas the negative effect was comparable for both groups as shown by main effects in the online study (Altruism: β = 1.39, p = .052; Fairness: β = 1.51, p = .051; Reciprocal trust: β = 1.95, p = .023).
      Figure thumbnail gr4
      Figure 4Individual differences in response time and moral attitudes for alcohol use disorder (AUD) and healthy control individuals respectively. A; C; E: Associations between prosocial decision-making and response time (1Z = approx. 5 seconds) showing reduced prosociality for fast decisions in the AUD group. B; D; F: Associations between prosocial decision-making and moral attitudes showing reduced prosociality for individuals disfavoring impartiality. For online study, see Supplementary Results S23. p < .1, * p < .05, ** p < .01, *** p < .001==========

      Clinical Variables

      Drinking history had no effect on prosocial decisions in terms of abstinence duration, alcohol use past 30 days, and duration of harmful drinking in the AUD group (Supplementary Results S16, S19, S22). Neither did we find any effect of alcohol craving at time of testing, symptoms of anxiety, depression and stress past week.

      Sociocognitive Variables

      We found a negative effect for moral attitudes of impartiality for others in the lab study (Altruism: β = 2.86, p < .001; Fairness: β = 1.16, p = .034; Reciprocal trust: β = 1.33, p = .014, Figure 2, Supplementary Results S15, S18, S21), such that individuals disfavoring impartiality also showed a stronger reduction in prosocial decisions. Although all measures in the online study pointed in the same direction (Altruism: β = 1.52, p = .11; Fairness: β = .16, p = .80), only Reciprocal trust were marginally significant (β = 1.67, p = .061). In contrast, neither moral attitudes of instrumental harm or empathy had any effect on prosociality.

      Discussion

      In the present study, we report differences in prosocial decision-making in young adults with AUD in comparison with HC in two separate samples: one laboratory sample in Sweden and one US confirmatory online sample. Our study yielded three major findings. First, using standardized behavioral economical tasks, we found that altruistic, fairness and reciprocal trust decisions were reduced in AUD as compared to HC. In contrast, trust, third-party punishment and third-party compensation decisions did not differ between the two groups. Specifically, individuals with AUD kept more economically incentivized points for themselves in a Dictator Game, Ultimatum Game, and a Reciprocal Trust Game. The findings demonstrated a medium effect size which is comparable to previous findings on prosocial decision-making in cocaine use disorder (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ). Second, we found that individual performance varied on three important dimensions: attention, decision-response time, and moral attitudes. Third, individual differences in prosociality could not be explained by drinking level history in the AUD group or recent psychiatric symptom load indicating trait-related prosocial deficits. To our knowledge, this is the first study to systematically identify reductions in components of interactive behaviors in young adults with AUD and describe the processes underlying these reductions.
      Altruistic behavior is reduced in individuals with other substance use disorders when measured as self-report (
      • Carter R.R.
      • Johnson S.M.
      • Exline J.J.
      • Post S.G.
      • Pagano M.E.
      Addiction and “Generation Me:” Narcissistic and Prosocial Behaviors of Adolescents with Substance Dependency Disorder in Comparison to Normative Adolescents.
      ) or decision responses in a combined Dictator/Distribution Game (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ). Other psychiatric disorders such as ADHD also show reduced altruistic decisions in the Dictator Game (
      • Ma I.
      • Lambregts-Rommelse N.N.J.
      • Buitelaar J.K.
      • Cillessen A.H.N.
      • Scheres A.P.J.
      Decision-making in social contexts in youth with ADHD.
      ), whereas individuals with Autism and Schizophrenia perform on par with healthy controls (
      • Sally D.
      • Hill E.
      The development of interpersonal strategy: Autism, theory-of-mind, cooperation and fairness.
      ,
      • Van’t Wout M.
      • Sanfey A.G.
      NIH Public Access.
      ). Our results support the advantage of using the Dictator Game for identifying reduced altruism in AUD. Taken together, our and previous results highlight the importance of altruistic behavior as a transdiagnostic phenotype (i.e., effects not differentiating along the conventional diagnostic categories) in psychiatric disorders.
      The processes underlying fair behavior are important for understanding social norm transgressions, and previous studies show that individuals with AUD compared to HC individuals, are more likely to inflict punishment following unfair behavior from others (
      • Brevers D.
      • Noël X.
      • Ermer E.
      • Dabiri D.
      • Verbanck P.
      • Kornreich C.
      Unfairness sensitivity and social decision-making in individuals with alcohol dependence: A preliminary study.
      ,
      • Brevers D.
      • Noël X.
      • Hanak C.
      • Verbanck P.
      • Kornreich C.
      On the relationship between emotional state and abnormal unfairness sensitivity in alcohol dependence.
      ,
      • Tsukue R.
      • Okamoto Y.
      • Yoshino A.
      • Kunisato Y.
      • Takagaki K.
      • Takebayashi Y.
      • et al.
      Do Individuals with Alcohol Dependence Show Higher Unfairness Sensitivity? The Relationship Between Impulsivity and Unfairness Sensitivity in Alcohol-Dependent Adults.
      ). We extended this finding by showing that individuals with AUD also behave more unfair toward others themselves, in spite of displaying no differences in the tendency to regulate unfairness between third-party others (i.e. third-party punishment or compensation). One interpretation of this discrepancy might be that only direct interaction is emotionally salient enough to trigger response deficits in AUD (
      • Brevers D.
      • Noël X.
      • Hanak C.
      • Verbanck P.
      • Kornreich C.
      On the relationship between emotional state and abnormal unfairness sensitivity in alcohol dependence.
      ).
      Reciprocal trust behavior was reduced in individuals with AUD which aligns with findings in other psychiatric disorders (e.g., social anxiety disorder (
      • Anderl C.
      • Steil R.
      • Hahn T.
      • Hitzeroth P.
      • Reif A.
      • Windmann S.
      Reduced reciprocal giving in social anxiety – Evidence from the Trust Game.
      )). Moreover, our results support that whereas reciprocating trust from others is reduced in AUD, the initiation of trust in others is intact. Thus, it seems that individuals with AUD have deficits when a response to another individual’s trust behavior is required. Alternatively, the reductions might be related to more general emotional deficits in recognizing and responding to the perspective of others. For an example, self-reported interpersonal difficulties in AUD have been related to general emotional deficits in voice and face recognition (
      • Kornreich C.
      • Philippot P.
      • Foisy M.-L.
      • Blairy S.
      • Raynaud E.
      • Dan B.
      • et al.
      Impaired emotional facial expression recognition is associated with interpersonal problems in alcoholism.
      ). Future studies should examine how reciprocity deficits is related to the fact that individuals with AUD often break the trust of others resulting in difficulties in maintaining relations, as well as the relative role of reciprocity deficits in the maintenance of drinking behaviors and relapse (
      • Keller P.S.
      • Gilbert L.R.
      • Koss K.J.
      • Cummings E.M.
      • Davies P.T.
      Parental problem drinking, marital aggression, and child emotional insecurity: A longitudinal investigation.
      ).
      Collectively, our results showing reduced prosocial decisions in AUD may echo previous research on the comorbidity of antisocial personality and AUD, which shared some genetic loading (
      • Cloninger C.R.
      • Reich T.
      Genetic heterogeneity in alcoholism and sociopathy.
      ), and have been shown to interact in producing more severe clinical symptoms, as well as reducing empathy and distress from interpersonal relationships (
      • Morgenstern J.
      • Langenbucher J.
      • Labouvie E.
      • Miller K.J.
      The comorbidity of alcoholism and personality disorders in a clinical population: Prevalence rates and relation to alcohol typology variables.
      ). Hence, it possible that reduced prosocial behavior in AUD, at least partly, shares variance with increased antisocial behavioral traits.
      Individual differences are to be expected in AUD due to the large symptom heterogeneity of the disorder in the population (i.e. any 4 out of 11 criteria required for a moderate AUD diagnosis according to the DSM-5). The wide response distribution in altruistic, fairness, and reciprocal trust decision making within the AUD group is therefore not surprising (Figure 2). The prosocial deficits were associated with several variables. First, attending the selfish response options was associated with subsequent choice even after controlling for early and late attentional deployment which indicates the role of some valuation process and not merely tracking the mouse cursor prior to response. These findings preliminary support a selfish attentional bias for individuals with AUD. In fact, previous research shows that attentional deployment towards selfish as compared to social stimuli might be an expression for individual preferences, but also, due to the causal role of attention on choices (
      • Teoh Y.Y.
      • Yao Z.
      • Cunningham W.A.
      • Hutcherson C.A.
      Attentional priorities drive effects of time pressure on altruistic choice.
      ,
      • Pärnamets P.
      • Shuster A.
      • Reinero D.A.
      • Van Bavel J.J.
      A Value-Based Framework for Understanding Cooperation.
      ). Second, faster decision responses were associated with reduced prosociality across altruism, fairness, and reciprocal trust. This might indicate that individuals with AUD value prosociality less (
      • Pärnamets P.
      • Shuster A.
      • Reinero D.A.
      • Van Bavel J.J.
      A Value-Based Framework for Understanding Cooperation.
      ,
      • Krajbich I.
      • Bartling B.
      • Hare T.
      • Fehr E.
      Rethinking fast and slow based on a critique of reaction-time reverse inference.
      ) and therefore require more time for deliberation compared to HC in order to overcome selfish impulses. These findings also suggest a linkage to studies on other psychiatric disorders marked by impulsivity and reduced altruistic decision-making, namely: cocaine use disorder, and ADHD (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ,
      • Ma I.
      • Lambregts-Rommelse N.N.J.
      • Buitelaar J.K.
      • Cillessen A.H.N.
      • Scheres A.P.J.
      Decision-making in social contexts in youth with ADHD.
      ). Thus, impulsivity and reduced prosociality might be overlapping phenotypes due to the instant reward from selfish behavior (
      • Soutschek A.
      • Ruff C.C.
      • Strombach T.
      • Kalenscher T.
      • Tobler P.N.
      Brain stimulation reveals crucial role of overcoming self-centeredness in self-control.
      ), and should be further investigated in AUD and other psychiatric disorders. Third, moral attitudes disfavoring impartiality were associated with reduced prosociality. Although this effect was not equally clear in the online study, this provides a preliminary linkage between reduced prosocial decision-making in AUD and explicit moral judgment which aligns with research highlighting the role of moral reasoning in the change of behavior (
      • Bloom P.
      How do morals change?.
      ,
      • Li J.
      • Hao J.
      • Shi B.
      From moral judgments to prosocial behavior: Multiple pathways in adolescents and different pathways in boys and girls.
      ,
      • Reynolds S.J.
      • Ceranic T.L.
      The Effects of Moral Judgment and Moral Identity on Moral Behavior: An Empirical Examination of the Moral Individual.
      ).
      Variables not associated with reduced prosociality in AUD included individual differences in recent psychiatric symptom load and drinking history. This indicates that reduced prosociality in AUD has a trait-like stability, which neatly aligns with similar findings in individuals with cocaine use disorder (
      • Hulka L.M.
      • Eisenegger C.
      • Preller K.H.
      • Vonmoos M.
      • Jenni D.
      • Bendrick K.
      • et al.
      Altered social and non-social decision-making in recreational and dependent cocaine users.
      ).
      Our study has limitations in need of discussion. Given the cross-sectional study design, the stated evidence for reduced prosociality as a trait-related factor in AUD should be interpreted with caution. In fact, a strong reduction in actual drug consumption can lead to some recovery of prosocial behavior in cocaine use disorder (
      • Vonmoos M.
      • Eisenegger C.
      • Bosch O.G.
      • Preller K.H.
      • Hulka L.M.
      • Baumgartner M.
      • et al.
      Improvement of emotional empathy and cluster B personality disorder symptoms associated with decreased cocaine use severity.
      ), providing support for a bidirectional effect and highlights the importance of longitudinal study designs for more reliably assessing how prosocial behavior might change as a result of altered drug consumption over time. Also, we did not examine the relation to real-world behavior, such as social network size or social activities in daily life, which may explain parts of the group differences found in this study.
      In conclusion, the current study is to the best of our knowledge the first to show that individuals with AUD exhibit reduced prosocial decision-making related to altruism, fairness, and reciprocal trust. We found that these reductions could be explained by individual differences in attention, decision response time and moral attitudes. Neither drinking level history in AUD, nor current psychiatric symptoms, explained these reductions indicating stability over time. Future directions include refinement of the prosocial task measures for better integration of the mechanisms underlying individual differences in AUD. For example, refinements could be made based on related task measures, e.g. a social gaze task administered in individuals with cocaine use disorder demonstrated differences in attention during social interaction which was related to reduced activation of the brain’s reward system (
      • Preller K.H.
      • Herdener M.
      • Schilbach L.
      • Stämpfli P.
      • Hulka L.M.
      • Vonmoos M.
      • et al.
      Functional changes of the reward system underlie blunted response to social gaze in cocaine users.
      ). Taken together, our study shows that young adults with AUD have stable reductions in prosocial decision-making during one-to-one interaction suggesting a trait-related deficit in the early-onset of the disorder.

      Acknowledgments

      This study was supported by a Consolidator Grant (2018-00877) from the Swedish Research Foundation to Andreas Olsson, project grants from Stockholm County Council (20170512), Stiftelsen Söderström-Königska Sjukhemmet (SLS-750801), and The Swedish Society of Medicine (SLS-780001) to Nitya Jayaram-Lindström, and a project grant from the Swedish Research Council to Philip Pärnamets (2020-02584). Preliminary versions of these results have been shown as poster presentations at the Society of Biological Psychiatry (April 30, 2021) (
      • Jangard S.
      • Lindström B.
      • Khemiri L.
      • Olsson A.
      • Jayaram-Lindström N.
      Prosocial Learning and Decision-Making in Young Adults With Alcohol Use Disorder.
      ) and the Social & Affective Neuroscience Society (April 30, 2021). We thank Jonas Karlsson and Kristin Nordenberg for assistance with data collection. Moreover, we thank Joar Guterstam and Predrag Petrovic for comments on an earlier draft of this manuscript.
      Disclosures
      The authors report no biomedical financial interests or potential conflicts of interest.

      Supplementary Material

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