Affective decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in 10th grade Chinese adolescent binge drinkers
Introduction
Although some studies have investigated the role of the Prefrontal Cortex (PFC) in the vulnerability to experimentation with alcohol, and the acquisition of alcohol disorders in adolescents, most of these studies have focused on the role of the “cold” cognitive aspects of executive functions (EF) in alcohol use, which have been linked to the dorsolateral sector of the prefrontal cortex (DLPC) (Finn, Mazas, Justus, & Steinmetz, 2002; Hartley, Elsabagh, & File, 2004; Sher, 2006; Thush & Wiers, 2007; Zeigler et al., 2005; Zetteler, Stollery, Weinstein, & Lingford-Hughes, 2006). Relatively few studies have addressed the “hot” cognitive aspects of EF in alcohol and other substance use, which have been more linked to the orbital/ventromedial sector of the prefrontal cortex (OFC/VMPC) (Overman et al., 2004). In this study, we examined the affective decision-making ability measured by the Iowa Gambling Test (IGT) in adolescent drinkers. The IGT has been shown to tax aspects of decision-making that are guided by affect and emotions (Bechara, 2003; Turnbull, Evans, Bunce, Carzolio, & O’Connor, 2005). We hypothesized that binge drinkers would show relatively poor measures of affective decision-making relative to other drinkers and/or never drinkers. The rationale was that poor affective decision-making, as measured by the IGT, would predispose individuals to poorly controlled substance use, as they become more likely to be lured by immediate reward, or more oblivious to the negative future consequences of their choice.
Much evidence shows that there are protracted maturational changes in top-down PFC systems relative to subcortical systems during the transitional period of adolescence (Giedd, 2004, Gogtay et al., 2004, Spear, 2000; Toga, Thompson, & Sowell, 2006). However, the PFC is relatively large, and its functions are heterogeneous (Faw, 2003; Kolb, Pellis, & Robinson, 2004). These “supervisory” functions of PFC can be further categorized into cognitive control or “cold” EF, which flexibly regulates thoughts and actions in the presence of competing goals (Durston & Casey, 2006; Miller & Cohen, 2001), and affective control or “hot” EF, which strategically controls feelings in the service of a goal (Dahl, 2003; Kerr & Zelazo, 2004). Studies in neuroimaging and neuropsychology have shown that cognitive and affective control associate with different but interacting subregions of the PFC—the DLPC and the OFC/VMPC, respectively (Kringelbach, 2005; Miller & Cohen, 2001; O’Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001; Oya et al., 2005). Development studies have indicated that maturation of the OFC/VMPC, and especially the frontal pole (e.g., Brodmann's Area 10) might be a developmentally distinct process from maturation of other regions of the frontal lobe, and cognitive control functions might mature earlier than do affective control functions (Crone & van der Molen, 2004; Hooper, Luciana, Conklin, & Yarger, 2004). This immature period of the OFC/VMPC perhaps explains why adolescents are often capable of understanding the risks and consequences of their actions, despite making disadvantageous decisions (Cauffman & Steinberg, 2000), which suggests that cognitive control functions are already in place, whereas affective control is still developing (Steinberg, 2005). Thus, examining the affective control functions in adolescents might be important to understanding their reward-seeking behavior, such as alcohol consumption.
Affective control is essential for adequate functioning and is likely to have an effect on a number of behaviors in which positive and negative affective consequences must be acted on adaptively. Among several useful measures to assess affective control functions (Bechara, Damasio, Damasio, & Anderson, 1994; Elliott, Friston, & Dolan, 2000; Ernst et al., 2004, Rogers et al., 1999), we employed a widely used measure— Iowa Gambling Test (IGT) (Bechara et al., 1994) —to assess the affective decision-making ability of a group of Chinese adolescents. Compared to other tasks, which assess brain functions related to the calculation of probability or expected value, IGT requires participants to learn and infer from their past experience (such as reward and punishment encountered during the task) about outcome probabilities (Bechara, 2004a, Bechara, 2004b). Affective and emotional systems play a critical role in such learning processes. The decision-making of neurologically developed and intact participants is guided by an emotional signal that assigns negative value for the disadvantageous choices and positive value for advantageous choices, thereby leading behavior towards long term favorable options. Several developmental studies have demonstrated that there is significant and steady improvement on the IGT or IGT analogous tasks during early adolescence to adulthood (Crone & van der Molen, 2004; Hooper et al., 2004, Overman, 2004). These findings parallel other studies, which show that the prefrontal cortex may not develop fully until the age of 21 (Giedd, 2004, Gogtay et al., 2004). Although all adolescents might still be undergoing developmental changes in the prefrontal region (i.e., having a “premature” prefrontal cortex), and by and large be mostly susceptible to making suboptimal or “risky” decisions compared to adults, we investigated in this study the individual variability among the adolescents at similar age. We attempted to identify those who might be at a higher risk for making bad decisions, which potentially may translate into real life risky behaviors, such as alcoholism and drug dependence. It remains to be determined whether a relatively abnormal poor decision-making capacity as measured by the IGT will serve as an early neurocognitive marker that may help identify at-risk adolescent individuals. This early identification could be useful for prevention.
The IGT has two versions: the original and the variant. In the original version, the disadvantageous decks of cards yield higher immediate rewards but unpredictable and larger delayed punishments, while the advantageous decks provide lower immediate gains but unexpected and smaller future losses. In the variant version, the schedules of reward and punishment contingencies are reversed, so that the advantageous decks yield immediate losses but even higher future rewards, and the disadvantageous decks offer lower immediate punishments but even lower long-term rewards. The variant version was developed to address the question of whether hypersensitivity to immediate reward and/or insensitivity to long-term consequences might account for the choice of the disadvantageous decks on the original version (Bechara, Tranel, & Damasio, 2000; Bechara, Dolan, & Hindes, 2002). For example, although patients with VMPC brain damage and the Substance Dependence Individuals (SDI) showed similar disadvantageous choices on the original version, they performed very differently on the variant version. VMPC patients still performed badly but one large subgroup of SDI performed normally (Bechara, Tranel et al., 2000; Bechara et al., 2002). These results were interpreted to suggest that although both VMPC patients and SDI were “myopic” for the future, the underlying mechanisms were different: VMPC patients were insensitive for future consequences, positive or negative (Bechara, Tranel et al., 2000; Bechara et al., 1994) while some SDI were hypersensitive to immediate reward (Bechara et al., 2002).
Because hot and cold executive functions diverge in their maturational trends and may have different implications for binge-drinking, cognitive performance associated with cold cognition is also important to consider. One of the specific and most well-researched cognitive functions in this domain is working memory. Good working memory helps individuals keep competing considerations “online” (Kane & Engle, 2002), even when faced with other demands on cognitive resources (e.g., carrying on a conversation, considering peer's opinions). Without good working memory, multiple considerations are not as likely to be kept active or “online” for any decisions, and explicit memory retrieval is less effective (De Neys et al., 2005a, De Neys et al., 2005b; Kane & Engle, 2000). Therefore, a smaller subset of learned effects (only the most spontaneously activated ones) is available to influence behavior.
In this study, we used the Self-ordered Pointing Test (SOPT) (Peterson, Pihl, Higgins, & Lee, 2002) to assess working memory capacity, utilizing a task developed by Petrides and Milner (Petrides & Milner, 1982). The task is feasible for use in field research with adolescent participants. This task requires in each trial, an individual to memorize a maximum number of 12 items, either visually or phonologically encoded, and hold them “online” for further operations. Because there are 6 trials of the SOPT, the maximum capacity is not required in the first trial but the amount of information increases cumulatively over the course of each trial. This process resembles that of transient online storage (Perry et al., 2001), or active monitoring and retrieving of the increasing amount of information (Petrides, 1995) in the concept of working memory. This task has been linked to neural activity within the Dorsolateral Prefrontal Cortex (DLPC) (Petrides, Alivisatos, Meyer, & Evans, 1993) and has been used to assess working memory capacity in several studies (Chaytor & Schmitter-Edgecombe, 2004; Chey, Lee, Kim, Kwon, & Shin, 2002; Pukrop et al., 2003; Ward, Shum, McKinlay, Baker-Tweney, & Wallace, 2005). Moreover, studies have shown that working memory is highly related to general cognitive functions such as reading, mathematics, and reasoning (Colom, Rebello, Palacios, Juan-Espinosa, & Kyllonen, 2004; Engle, Cantor, & Carullo, 1992; Jarrold & Towse, 2006). Therefore, we also ask the participants to report their school academic performance.
In this study, we focus on binge-drinking behavior because binge-drinking in youth represents poorly controlled alcohol consumption and is highly predictive of alcohol abuse and dependence in the future (Bonomo, Bowes, Coffey, Carlin, & Patton, 2004; Jennison, 2004). Our primary hypothesis is that binge drinkers will demonstrate signs of worse decision-making than never-drinkers, as reflected by lower scores on the original version of the IGT. Since hyperactivity of the reward system in the adolescent brain has been implicated in their risky behaviors (Ernst et al., 2005, May et al., 2004), we predict that the binge drinkers will perform normally on the variant version of the IGT, which indicates that the “myopia” for the future among binge drinkers is due to their hypersensitivity to reward. Furthermore, studies have reported that decision-making and working memory functions have an asymmetrical relationship (Bechara, Damasio, Tranel, & Anderson, 1998; Bechara, Damasio, & Damasio, 2000), i.e., poor working memory related to dorsolateral prefrontal cortex damage can compromise decision-making, but poor decision-making related to OFC/VMPC damage can occur independent of any working memory deficits. Developmental studies have suggested that maturation of the OFC/VMPC, might be a developmentally distinct process from maturation of other regions of the frontal lobe (Crone & van der Molen, 2004; Hooper et al., 2004). Other studies have shown that adolescents make disadvantageous decisions, yet they seem to have a mature capacity to reason and to explain reward probabilities (Crone, Jennings, & Van der Molen, 2004; Crone, Somsen, Van Beek, & Van Der Molen, 2004). Therefore, we anticipate that poor decision-making in binge drinkers is not due to deficits in their “cold” dorsolaterally mediated executive functions, and thus we expect normal scores on working memory and school academic performance, but poor performance on the original version of the IGT.
Section snippets
Sample
The data collected in this study support the Pacific Rim Transdisciplinary Tobacco and Alcohol Use Research Center investigation of the determinants of tobacco and alcohol use and abuse among youth in China. All research protocols and instruments were approved by the USC and Chengdu, China CDC IRB's. With the assistance of the municipal Education Committee and the Chengdu Center for Disease Control and Prevention (CCDCP), in Chengdu City, Sichuan Province, four schools were recruited for the
Results
Demographic and drinking characteristics of the sample are presented in Table 1. Both gender and school type were almost equally represented. The proportions of youth with drinking experience (ever + 30-day + binge) were not significantly different between males (64.1%) and females (51.9%) or between vocational (59.2%) and academic (56.7%) students in the whole sample (P > 0.1). Gender and school type also did not reveal any significant difference in drinkers (at any level) relative to never-drinkers
Discussion
To our knowledge, there has been only one previous study to show that deficits in affective decision-making (as measured by an analogous IGT task) are associated with heavy alcohol use in adolescents (Overman et al., 2004). The current study presents a more detailed analysis than Overman and is in part an extension of that study. By avoiding heavy, prolonged substance abuse, the study provides support for a potential pre-existing neural basis for development of substance abuse in adolescence.
Acknowledgements
This research was supported by the University of Southern California Pacific Rim Transdisciplinary Tobacco and Alcohol Use Research Center TTAURC funded by the National Institutes of Health (grant #1 P50 CA84735 to C. Anderson Johnson) and the National Institute on Drug Abuse (grant #DA16708 to Antoine Bechara and DA 16094 to Alan Stacy). The authors thank Peggy Gallaher, Steven Cen, Joel Milam, Qian Guo, Kari-Lyn Kobayakawa Sakuma, and Janet Okamoto for their contribution to this project. We
References (91)
Trajectories of brain development: Point of vulnerability or window of opportunity?
Neuroscience and Biobehavioral Reviews
(2003)Disturbances of emotion regulation after focal brain lesions
International Review of Neurobiology
(2004)The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage
Brain Cognition
(2004)- et al.
Insensitivity to future consequences following damage to human prefrontal cortex
Cognition
(1994) - et al.
Decision-making and addiction (part II): Myopia for the future or hypersensitivity to reward?
Neuropsychologia
(2002) - et al.
Brain systems mediating aversive conditioning: An event-related fMRI study
Neuron
(1998) - et al.
Spatial working memory span, delayed response and executive function in schizophrenia
Psychiatry Research
(2002) - et al.
Working memory is (almost) perfectly predicted by g
Intelligence
(2004) - et al.
Decision-making in disinhibited adolescents and adults:insensitivity to future consequences or driven by immediate reward?
Personality and Individual Differences
(2003) - et al.
What have we learned about cognitive development from neuroimaging?
Neuropsychologia
(2006)
Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents
Neuroimage
Choice selection and reward anticipation: An fMRI study
Neuropsychologia
Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: A tutorial review
Consciousness and Cognition
Complex decision-making in early childhood
Brain Cognition
Binge drinking and sex: Effects on mood and cognitive function in healthy young volunteers
Pharmacology Biochemistry and Behavior
Individual differences in working memory
Neuroscience
Development of “hot” executive function: The children's gambling task
Brain Cognition
Decision-making impairments in adolescents with early-onset schizophrenia
Schizophrenia Research
Plasticity and functions of the orbital frontal cortex
Brain Cognition
Sensation seeking, puberty, and nicotine, alcohol, and marijuana use in adolescence
Journal of the American Academy of Child and Adolescent Psychiatry
Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents
Biological Psychiatry
Sex differences in early childhood, adolescence, and adulthood on cognitive tasks that rely on orbital prefrontal cortex
Brain Cognition
Performance on the IOWA card task by adolescents and adults
Neuropsychologia
Mapping brain maturation and cognitive development during adolescence
Trends in Cognitive Sciences
Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man
Neuropsychologia
Dimensions of working memory dysfunction in schizophrenia
Schizophrenia Research
Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: Evidence for monoaminergic mechanisms
Neuropsychopharmacology
The adolescent brain and age-related behavioral manifestations
Neuroscience and Biobehavioral Reviews
Cognitive and affective development in adolescence
Trends in Cognitive Sciences
Explicit and implicit alcohol-related cognitions and the prediction of future drinking in adolescents
Addictive Behaviors
Mapping brain maturation
Trends in Neurosciences
Emotion-based learning and central executive resources: An investigation of intuition and the Iowa Gambling Task
Brain Cognition
Relationship of binge drinking and other health-compromising behaviors among urban adolescents in China
Journal of Adolescent Health
The neurocognitive effects of alcohol on adolescents and college students
Preventive Medicine
Impairments of emotion and real-world complex behavior following childhood- or adult-onset damage to ventromedial prefrontal cortex
Journal of the International Neuropsychological Society
Adolescence: Vulnerable period for stress-induced prefrontal cortical function? Introduction to part IV
Annals of the New York Academy of Sciences
Risky business: Emotion, decision-making, and addiction
Journal of Gambling Studies
The anatomy of emotional intelligence and the implications for educating people to be emotionally intelligent
Emotion, decision making and the orbitofrontal cortex
Cerebral Cortex
Role of the amygdala in decision-making
Annals of the New York Academy of Sciences
Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Journal of Neuroscience
Dissociation of working memory from decision making within the human prefrontal cortex
Journal of Neuroscience
Impaired decision making related to working memory deficits in individuals with substance addictions
Neuropsychology
Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions
Brain
Orbitofrontal cortex and social behavior: Integrating self-monitoring and emotion-cognition interactions
Journal of Cognitive Neuroscience
Cited by (103)
A systematic review of neuropsychological studies involving young binge drinkers
2018, Neuroscience and Biobehavioral ReviewsElectrophysiological correlates of performance monitoring in binge drinking: Impaired error-related but preserved feedback processing
2017, Clinical NeurophysiologyCitation Excerpt :A recent study also specifies that binge drinking is associated with altered response monitoring, indexed by a weak post-error slowing effect (Bø et al., 2016a). On the other hand, regarding the motivational system, binge drinking is characterized by disadvantageous decision-making, the ability to accurately react to sensory stimulations (e.g., Goudriaan et al., 2007; Johnson et al., 2008). These impairments are driven by high reward seeking (see Stautz and Cooper, 2013 for a meta-analysis) and more risky choices (Bø et al., 2016b; Worbe et al., 2014).
Risk Decision Making and Executive Function among Adolescents and Young Adults
2023, Behavioral SciencesSex-specific decision-making impairments and striatal dopaminergic changes after binge drinking history in rats
2023, Frontiers in Pharmacology