Smaller feedback ERN amplitudes during the BART are associated with a greater family history density of alcohol problems in treatment-naïve alcoholics

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Abstract

Background

Alcoholism is characterized by impaired decision-making (i.e., choosing intoxication in the face of mounting negative consequences). This impairment may involve a reduced brain response to the negative consequences of behavior, which supports an inclination to engage in risky behaviors. The feedback error-related negativity (F-ERN) is hypothesized to reflect the valence attached to the negative consequences of behavior. Performance on the Balloon Analogue Risk Task (BART) measures risk-taking propensity. We recorded F-ERNs during the BART and during a BART simulation, where individuals observed the rewards and consequences of (someone else's) BART performance.

Methods

EEGs were recorded on 22 actively drinking, treatment-naïve alcoholics during the BART and BART simulation. F-ERNs were measured and their association with psychological and alcohol use measures was examined.

Results

F-ERNs over fronto-central electrode sites were observed to balloon pops in the BART and BART simulation. F-ERNs during the BART were more than twice the amplitude of F-ERNs during the BART simulation. Smaller F-ERN amplitudes from the BART (but not the BART simulation) were associated with a greater family history density of alcohol problems.

Conclusion

The results suggest a possible link between the genetic vulnerability toward developing alcoholism and the brain's response to the negative consequences of behavior.

Introduction

A hallmark of substance abuse is impaired decision-making that favors short-term rewards (e.g., intoxication) in the face of mounting negative long-term consequences in one's personal, emotional, professional and social life (Rahman et al., 2001). These decision-making impairments are associated with a number of factors, including impulsivity, a reduced emotional valence attached to the negative consequences of behavior, impaired contingency learning, and an excessive dominance of the effects on behavior of immediate versus delayed rewards (Clark and Robbins, 2002). Ultimately, impaired decision-making can lead to abuse of other substances (or other risky behaviors) and can hamper the ability to cease substance abuse and resist relapse. Thus, understanding the mechanisms behind decision-making impairments is an important aspect to promoting effective treatment strategies and positive recovery outcomes.

Pairing decision-making laboratory experiments with EEG recordings enables simultaneous investigation of the behavioral and electrophysiological correlates of impaired decision-making. In particular, event-related potentials generated by the human error processing system could elucidate how neural responses to negative events relate to poor decision-making in alcoholics. The primary electrophysiological marker of the error processing system is the error-related negativity (ERN)—a negative potential that occurs in response to errors, detectable over fronto-central regions of the scalp. In tasks that involve prior knowledge of correct stimulus-response mappings (e.g. a Stroop or flanker task), the participant does not necessarily require feedback to know that he has made a mistake. In this case, an ERN occurs about 50–150 ms after the erroneous response and is called a response-locked error-related negativity (R-ERN) (for example: Dikman and Allen, 2000, Falkenstein et al., 2001, Hajcak and Simons, 2002). The R-ERN reflects low-level error recognition, as it is present even when individuals are not consciously aware of their errors (Nieuwenhuis et al., 2001). Another type of ERN is observed during tasks with unexpected outcomes (e.g. pseudo-random gambling games) that require participants to use positive and negative feedback to evaluate their response as correct or incorrect. These tasks elicit an ERN that occurs about 200–300 ms after negative feedback, now commonly referred to as the feedback error-related negativity (F-ERN) (Hajcak et al., 2006, Holroyd et al., 2004a, Nieuwenhuis et al., 2002, Nieuwenhuis et al., 2004, van Meel et al., 2005). F-ERN amplitude appears to be sensitive to changes along an abstract good–bad dimension, which depends on the most salient task objective (Nieuwenhuis et al., 2004). Consistent with a general good–bad evaluation, Hajcak and others demonstrated that F-ERNs reflected reward valence rather than reward magnitude (Hajcak et al., 2006). Recent studies have shown that the F-ERN is also present during error observation, suggesting that error monitoring is active even when errors are caused by someone else (van Schie et al., 2004, Yu and Zhou, 2006).

According to the reinforcement learning theory and error-processing model proposed by Holroyd and Coles, the R-ERN and F-ERN reflect the disinhibition of apical dendrites in the anterior cingulate cortex (ACC), which is caused by phasic decreases in mesencephalic dopaminergic activity from the basal ganglia to the ACC. This negative reinforcement signal occurs when the system realizes that ongoing events are worse than expected. Acting as a motor control filter, the ACC uses the reinforcement signals to determine the most suitable behavior for the task at hand (Holroyd and Coles, 2002). An alternative explanation is that the R-ERN represents the activation of a conflict-monitoring system after an error is committed. When conflict is present, centers for cognitive control are notified that attention needs to be redirected in order to avoid negative outcomes. The negative feedback that elicits the F-ERN also activates the conflict-monitoring system, and in turn, calls for behavioral changes (Botvinick et al., 2001). In either case, evidence suggests that normal F-ERN responses are crucial in the processing of negative events and consequently, central to effective decision-making.

Evidence for the impact of alcoholism on the ERN is currently limited. Two studies found acute reductions in R-ERN amplitude with moderate doses of alcohol (Easdon et al., 2005, Ridderinkhof et al., 2002). Impulsivity, which is strongly related to alcoholism, was shown to be associated with weakened R-ERNs in a flanker task (Ruchsow et al., 2005). When rewards and punishments are added to the flanker task, impulsive individuals have reduced R-ERNs only when errors result in punishment, which indicates hyposensitivity specific to punishment rather than a generalized desensitization to reward and punishment (Potts et al., 2006). R-ERN deficits were also reported in patients with cocaine dependence (Franken et al., 2006). These studies open the possibility that compromised error processing and/or reduced sensitivity to punishment is related to substance abuse; however, we have yet to find a study that specifically examines the relationship between the ERN and chronic alcoholism.

In addition to understanding the F-ERN, observing risk-taking behavior on the Balloon Analogue Risk Task (BART) can provide insights into the underlying mechanisms of poor decision-making (Lejuez et al., 2002). In the experiment, an individual is presented with an empty balloon that can be inflated incrementally with money. After each balloon pump, the individual can choose to stop and collect the money inside the balloon or he can choose to add more money by pumping again. If he causes the balloon to pop, the money inside is lost and experiment continues with another empty balloon. The probability of the balloon bursting increases with each pump. Thus, each pump is a risky decision that can result in a gain in temporary earnings or a loss of all balloon earnings up to that point. This approach models real-world risk-taking and provides a novel measure of an individual's tendency to engage in risky behaviors (i.e. make risky decisions). BART performance has been associated with self-report measures of safety and health risk behaviors (e.g. drug use, gambling, stealing, unprotected sexual intercourse), which are real-world manifestations of poor decision-making (Lejuez et al., 2002). The same study also found BART performance to be associated with deficiencies in behavioral constraint in adults (Lejuez et al., 2002). In a sample of young adults, antisocial behavior measures were positively correlated with risk-taking on the BART (Hunt et al., 2005). In a study differentiating smokers from nonsmokers, the BART was more effective than the Iowa Gambling Task (Lejuez et al., 2003a). Performance on the BART is related to real-world risk-taking in adolescent samples as well (Aklin et al., 2005, Lejuez et al., 2003b). Increased risk-taking on the BART was observed in adolescents with serious conduct and substance problems, including alcohol dependence and abuse (Crowley et al., 2006). Lejuez and colleagues have now developed a youth version of the BART to further investigate risk-taking propensity in adolescents (Lejuez et al., 2007). In the initial evaluation, BART performance was associated with measures of impulsivity but no associations were found in follow up studies (Aklin et al., 2005, Hunt et al., 2005, Lejuez et al., 2003a, Lejuez et al., 2003b). Lejuez and others suggest that the lack of association indicates that the BART measures a form of behavioral disinhibition that is distinct from self-report measures of impulsivity. Therefore, the BART is said to tap into a unique aspect of risk-taking, unaccounted for by self-report measures (Lejuez et al., 2003a, Lejuez et al., 2003b). This property offers a different look into the proclivity for risk-taking in samples with alcohol problems that is not captured by written questionnaires. We are unaware of any studies on electrophysiological activity during administration of the BART. F-ERN recording could help elucidate the brain mechanisms involved in processing the negative consequences of behavior during the BART. Furthermore, we have not encountered any implementations of a BART simulation that could replicate the ERN findings during error observation (van Schie et al., 2004, Yu and Zhou, 2006).

In this study, we examined decision-making on the BART and F-ERNs during the BART and BART simulation in actively drinking, treatment-naïve alcoholics (TxNA). Evidence for the relationship between substance abuse and poor decision-making suggests that our sample would make risky, disadvantageous decisions during the BART. We hypothesized that poor decision-making would be driven by hyposensitivity to negative feedback. The degree of hyposensitivity could be measured by the F-ERN, with weaker F-ERN responses indicating decreased sensitivity and stronger F-ERN responses indicating increased sensitivity. Consequently, we expected risk-taking during the BART to be negatively related to the F-ERN. Furthermore, we also expected to find that individuals with severe alcoholism (as measured by alcohol consumption, family history and personality profiles) would exhibit an even lesser sensitivity to negative feedback than those with less severe alcoholism.

Section snippets

Subjects

The participants consisted of 22 TxNA individuals (9 females, 13 males) between the ages of 20 and 45 (mean = 29.35, S.D. = 7.96). All participants were recruited from respondents to flyer postings, mailings, newspaper advertisements, internet postings and referrals from other research participants. TxNA participants were accepted into the study if they met DSM-IV (American Psychiatric Association, 1994) criteria for alcohol dependence, were currently drinking, and never sought treatment for

Results

The F-ERN was present for both the BART and the BART simulation (Table 1), and was strongest at FCz. F-ERN amplitudes were more than twice as large during the BART compared to the BART simulation. Repeated-measures ANOVA revealed that the within-subject task effect accounted for 50.4% of the variance in F-ERN amplitude (F(1,19) = 6.435, p = 0.003).

These results are illustrated by average waveforms following positive and negative feedback by channel and task (Fig. 2). Waveforms following balloon

Discussion

We have clearly demonstrated that the F-ERN is present in response to popped balloons during the BART. In agreement with previous studies, the F-ERN was present at fronto-central electrodes after feedback indicated an error. Also, in agreement with previous studies, the F-ERN was detected when individuals observed negative feedback that was not caused by their own actions. If the ERN reflects the reinforcement signals utilized in reinforcement learning (Holroyd and Coles, 2002), then this

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