Neurobiological correlates of problem gambling in a quasi-realistic blackjack scenario as revealed by fMRI

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Abstract

In the present study we obtained functional magnetic resonance imaging (fMRI) data in occasional gamblers (OG) and problem gamblers (PG) during a quasi-realistic blackjack game. We focused on neuronal correlates of risk assessment and reward processing. Participants had to decide whether to draw or not to draw a card in a high-risk or low-risk blackjack situation. We assumed PG would show differences in prefrontal and ventral striatal brain regions in comparison to OG during risk assessment and due to the winning or losing of money. Although both groups did not differ in behavioral data, blood oxygen level dependent (BOLD) signals in PG and OG significantly differed in thalamic, inferior frontal, and superior temporal regions. Whereas PG demonstrated a consistent signal increase during high-risk situations and a decrease in low-risk situations, OG presented the opposite pattern. During reward processing as derived from contrasting winning vs. losing situations, both PG and OG groups showed an enhancement of ventral striatal and posterior cingulate activity. Furthermore, PG demonstrated a distinct fronto-parietal activation pattern which has been discussed to reflect a cue-induced addiction memory network which was triggered by gambling-related cues.

Introduction

Pathological gambling is characterized by a craving for gambling, loss of control, and continuing gambling despite associated adverse consequences. It is classified as an impulse control disorder in the Diagnostic and Statistical Manual of Mental Disorders IV (DSM IV) with a lifetime prevalence of 0.5–1% (Petry et al., 2005). From a clinical point of view, pathological gambling is related to addictive behavior (Potenza, 2006), and there is emerging evidence that the underlying pathology on a neuronal level compares to cue-related behavior in drug addiction (Franklin et al., 2007). Gambling takes place in a complex social and context-specific environment, which cannot easily be transferred into an experimental setting. Furthermore, the gambling situation consists of a variety of cognitive (problem solving, risk assessment) and emotional (reward processing) behaviors, which may be prevalent in problem gamblers. In the present study we introduced an experimental design with a quasi-realistic blackjack game scenario to enhance ecological validity, and to allow for the analysis of different episodes of the game. We were particularly interested in separating the risk assessment and reward processing periods of the game because both have been shown to be impaired in pathological gambling (Reuter et al., 2005, Goudriaan et al., 2006).

Growing evidence suggests that risk assessment/decision making might be affected in pathological gambling, especially when gamblers have to choose between risky and safe options (Bechara, 2005). So far, most experimental data have been derived from the Iowa Gambling Task (IGT), as developed by Bechara et al. (1994), and introduced as a tool to measure “risk-anticipation”. Patients with ventromedial frontal lobe (VMF) damage (Cavedini et al., 2002), patients with disinhibition behavior (substance dependencies, psychopathy and attention deficit/hyperactivity disorder; Blair, 2001), and pathological gamblers (Goudriaan et al., 2005) showed impaired performance on the IGT (Bechara et al., 1997). Tanabe et al. (2007) showed a reduced activation in the right prefrontal cortex during decision making in substance-dependent gamblers, as compared with substance-dependent controls on the IGT. These authors related gambling-associated problems to impaired working memory, stimulus reward evaluation, or cue reactivity. Furthermore, Brand et al., 2005, Brand et al., 2006 suggested dorsolateral prefrontal and orbitofrontal dysfunctions in pathological gamblers — both regions are discussed to be involved in decision making. In particular, the orbitofrontal cortex was reported to be sensitive to the amount of conflict inherent to decisions (Rogers et al., 1999).

In addition to impaired risk evaluation and risk taking, it has been shown that reward processing and the activity of the mesolimbic dopaminergic reward system (Self and Nestler, 1998, Volkow et al., 2002) may be affected in pathological gambling. Additionally, there is evidence for a reduction in the sensitivity of the reward system. Reuter et al. (2005) compared pathological gamblers with healthy controls in a simple card-guessing game and demonstrated a ventral striatal and ventromedial prefrontal hypoactivation in pathological gamblers, which was positively correlated with gambling severity. d-Amphetamine, a non-specific dopamine agonist, was shown to prime gambling motivation in problem gamblers (Zack and Poulos, 2004). This points to a dysregulation of specific dopamine-related neuronal reward processes in problem gamblers. More recently, the same group (Zack and Poulos, 2007) demonstrated an enhancement of reward and priming effects of a gambling episode (playing slot machines) in pathological gamblers as compared with non-gamblers after D2 antagonist intake.

The majority of studies investigating neuronal correlates in pathological gambling are based on experimental settings which simplify the complex gambling environment. There are only a few studies which have introduced a more ecologically valid experimental gambling design to examine neuronal or neuroendocrinological responses while playing. Hewig et al. (2009) measured blood oxygen level dependent (BOLD) signal while playing blackjack in healthy participants. During the evaluative phase of decision making under risk conditions, the authors demonstrated that excessively risky and cautious decisions were associated with increased dorsal anterior cingulate cortex activity, similar to observed correlations of the error-related negativity (ERN) amplitude with both risk-taking and decision-making behavior (Gehring and Fencsik, 2001, Gehring and Willoughby, 2002) in a previous electroencephalography (EEG) study using the same design (Hewig et al., 2007). Evidence for the influence of gambling for real money (Ladouceur et al., 2003, Wulfert et al., 2005) was provided by Meyer et al. (2004), who compared the neuroendocrine responses of problem gamblers and healthy controls in two different situations: a real blackjack casino situation, where gamblers invested their own money, and an experimental control condition, where participants were playing for points in a laboratory environment. The results showed higher levels of norepinephrine and dopamine in problem gamblers compared with healthy participants in a “real money” casino environment, which became not significant in the control condition. Additional support for the crucial role of the applied stimulus material in relation to a specific addiction or disorder came from Volkow et al. (2003). The authors reported an orbitofrontal hypoactivation in addicted persons when confronted with natural reinforcers in contrast to an activation of the same area to substance-related cues. A similar finding was reported by Crockford et al. (2005), who showed cue-induced dorsolateral prefrontal activity in pathological gamblers during viewing of gambling-related cues. Thus, we decided to design the present experimental blackjack game scenario to be as realistic as possible, while considering necessary experimental efforts for methodologically correct parameterization.

The present functional magnetic resonance imaging (fMRI) study aimed at analyzing two major parts of the blackjack game, the periods of risk assessment and reward processing, using an ecologically valid quasi-realistic gambling scenario with comparatively high wagers in both problem gamblers and occasional gamblers. Based on the above-mentioned studies, we hypothesized that in problem gamblers both risk assessment and reward processing might be modulated by the gambling-related nature of the applied task: 1) For the period of risk assessment, we expect a signal increase in inferior frontal/orbitofrontal and thalamic brain regions, and particularly in problem gamblers during high-risk situations. 2) During reward processing, we expect a signal increase in the nucleus accumbens in both groups after win conditions. The quasi-realistic task, including gambling for real money, is supposed to counteract or override a generally observed hypoactivation in pathological gamblers associated with risk assessment and reward processing which is reported in experimental setups with a lower gambling-authenticity (Reuter et al., 2005, Tanabe et al., 2007).

Section snippets

Study participants

The study group consisted of 12 healthy male OG (range 25–49 years) and 12 male PG (range 29–57 years). All participants were right-handed according to a modified version of the Edinburgh Handedness Questionnaire (Oldfield, 1971). Both groups did not differ in age (F[1,22] = 2.97, P = 0.1), smoking behavior (z =  1.7, P = 0.1), and frequency of blackjack gambling (z =  0.6, P = 0.6; see also Table 1). We decided to investigate only male participants, as the prevalence of pathological gambling in men is

Behavioral data

Response times (RT) and risk assessment (hit vs. stand) in PG and OG did not differ significantly. A repeated measures ANOVA for RTs with the factors group (PG vs. OG) × risk (high-risk vs. low-risk) showed no significant main effect of group (F[1,22] = 0.9; P = 0.3), and group × risk interaction (F[1,22] = 0.02; P = 0.9). Both groups showed significantly longer RTs in high-risk compared with low-risk conditions (main effect of the factor risk; 1882 ± 629 ms vs. 1461 ± 452 ms; F[1,22] = 42.9, P < 0.001).

A repeated

Discussion

Using fMRI, we investigated neuronal correlates in PG and OG during a quasi-realistic blackjack scenario with respect to both risk assessment and reward processing. The present data suggest that risk assessment was associated with comparable arousal-related neuronal networks in PG and OG. During high-risk situations, fronto-thalamic brain activity was enhanced in PG, whereas OG showed a significant signal increase in low-risk conditions. Winning contrasted with losing money activated brain

Acknowledgements

The present study was supported by a research grant (11/174/05) of the Bremen University Research Commission to Gerhard Meyer and Manfred Herrmann and by the BMBF Neuroimaging Program (01GO0202) from the Center for Advanced Imaging (CAI) to Manfred Herrmann). We would like to thank Dorit Kliemann and Juliana Wiechert for assistance during data acquisition.

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