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Distorted Expectancy Coding in Problem Gambling: Is the Addictive in the Anticipation? Ruth J

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Distorted Expectancy Coding in Problem Gambling: Is the Addictive in the Anticipation? Ruth J Distorted Expectancy Coding in Problem Gambling: Is the Addictive in the Anticipation? Ruth J. van Holst, Dick J. Veltman, Christian Büchel, Wim van den Brink, and Anna E. Goudriaan Background: Pathologic gamblers are known to have abnormal neural responses associated with experiencing monetary wins and losses. However, neural responsiveness during reward and loss expectations in pathologic gamblers has not yet been investigated. Methods: We used a functional magnetic resonance imaging paradigm that allowed us to investigate the dissociable reward- and loss-related expectancies with various probabilities of winning or losing different amounts of money in 15 patients with problem gambling (PRGs) and 16 healthy control subjects (HCs). Results: Compared with HCs, PRGs showed stronger activation in the bilateral ventral striatum to 5 euro than to 1 euro trials. PRGs also showed more activation of the bilateral ventral striatum and left orbitofrontal cortex associated with gain-related expected value than HCs. In addition, regression analyses indicated a highly significant negative correlation between gambling severity scores and right amygdala activation associated with gain-related expected value coding. There were no group differences in brain activation for loss-related expected value. Conclusions: PRGs show higher activity in the reward system during reward expectation than HCs, whereas we observed no difference between PRGs and HC in the loss value system. Furthermore, the negative relation between gambling severity and amygdala activation in gain expected value coding suggests that more severe PRGs are less likely to be risk aversive during gambling. Our study provides evidence that PRGs are characterized by abnormally increased reward expectancy coding, which may render them overoptimistic with regard to gambling outcomes. Key Words: Expectancy, fMRI, loss, neuroimaging, pathological rewarding outcomes (for a review, see Peters and Buchel) (15). The gambling, reward amygdala, on the other hand, has a role in processing predictions of loss and/or aversive events (9,16–18) and was indeed shown to Ϫ ost pathologic gamblers (PGs) have erroneous beliefs respond to EV in a guessing task with varying loss magnitudes about gambling (1). For example, they overestimate the and probabilities (9). M probability of winning on a slot machine or in a poker Studying these dissociable value systems for gain and loss pre- game or have the idea that they can influence their chances, al- dictions could provide better insight into the systems that drive though these are fixed (2–7). These cognitive distortions are maladaptive choice behavior in PGs (19,20). For example, Frank et thought to underlie continued gambling by PGs despite incurring al. (21) found that Parkinson patients, who are characterized by a high losses. midbrain dopaminergic deficit, are better at learning to avoid To make advantageous decisions, people must estimate ex- choices that lead to negative outcomes than learning from positive pected reward values related to certain behaviors and continually outcomes. Interestingly, dopamine medication reversed this bias, update these reward expectations according to the encountered rendering Parkinson patients more sensitive to positive than to consequences. The expected value of certain behaviors can be negative predictions. Pathologic gamblers who experience higher divided in gain- (EVϩ) and loss (EVϪ)-related expectancy values, excitement levels during gambling showed higher dopamine re- EVϩ being reward magnitude times the probability of obtaining lease, whereas this relationship was absent in healthy control sub- the reward, and EVϪ being loss magnitude times the probability of jects (HCs) (22), and PGs had higher dopamine release when losing obtaining the loss. Using this gain and loss expectancy value model, money in a gambling game compared with HCs (23), thereby re- EVϩ and EVϪ have been found to be processed in different brain sembling medicated Parkinson patients (24). These higher dopa- areas. In humans, activity of the ventral striatum (8–12), a region mine levels during gambling could reflect increased sensitivity to known to receive afferent input from midbrain dopaminergic neu- gain-related (EVϩ) predictions in pathologic gambling. However, rons (12), has been shown to respond to conditioned stimuli pre- no neuroimaging data are currently available on how this expec- dicting reward delivery (13,14) according to the EVϩ model (9). In tancy of potential rewards manifests itself at a neurophysiologic addition, the orbitofrontal cortex has been implicated in EVϩ cod- level in PGs. However, it has been suggested that PGs are less loss ing (9) and is known to represent subjective hedonic experience for aversive than HCs (25,26). A neurocognitive study showed that PGs showed less heart rate changes compared to HCs during a card game when losing money (26). Furthermore, a functional magnetic From the Academic Medical Center (RJvH, DJV, WvdB, AEG), University of resonance imaging (fMRI) study showed impaired performance on Amsterdam; Department of Psychiatry, Amsterdam Institute for Addic- a reversal learning task coupled with an attenuated ventral medial tion Research (RJvH, DJV, WvdB, AEG); and Department of Psychiatry prefrontal cortex response in problem gamblers (PRGs) compared (DJV), VU University Medical Center, Amsterdam, the Netherlands; and the Department of Neurology (CB), University Medical Center, NeuroIm- with HCs when losing money (25). Thus, PGs could also be suffering age Nord, Hamburg, Germany. from an insensitivity to losses, rendering them less loss aversive Address correspondence to Ruth J. van Holst, Ph.D., Academic Medical than HCs. Center, Department of Psychiatry, P.O. Box 22660, 1100 DD Amsterdam, In view of the cognitive distortions discussed here and findings The Netherlands; E-mail: [email protected]. of aberrant choice behavior in PRGs (25–27), we hypothesized that Received Mar 28, 2011; revised Dec 24, 2011; accepted Dec 28, 2011. expectancy of potential gains (EVϩ) would result in a higher neural 0006-3223/$36.00 BIOL PSYCHIATRY 2012;71:741–748 doi:10.1016/j.biopsych.2011.12.030 © 2012 Society of Biological Psychiatry 742 BIOL PSYCHIATRY 2012;71:741–748 R.J. van Holst et al. response in the ventral striatum, ventral medial prefrontal cortex, in the top right-hand corner of the screen. Two seconds later, the 3- and orbitofrontal cortex in PRGs than in HCs. On the basis of studies to 10-sec intertrial interval started. indicating that PRGs could be less loss aversive and/or less sensitive Trial order was pseudo-randomized and predetermined (i.e., the for monetary losses (25, 26), we hypothesized that neural responses volunteer had no influence on the probability and the magnitude of associated with loss expectancy would be decreased in PRGs com- each individual trial and outcome). Altogether, subjects played 192 pared with HCs. To test these hypotheses, we used an fMRI para- trials (96 low-probability and 96 high-probability trials). In 30% of digm that allowed us to investigate gain and loss expected value the low-probability trials and in 70% of the high-probability trials, coding during various probabilities of winning different amounts of the participants won the displayed amount of money. money in PRGs compared with HCs. In summary, the task consisted of a 2 ϫ 2 ϫ 2 factorial design with factors probability (70% or 30%), magnitude (1 or 5 euro) and outcome (gain or loss), resulting in eight anticipation conditions Methods and Materials and eight outcome conditions. Before entering the scanner, subjects received a standardized Participants verbal description of the task and completed a practice session. It Fifteen PRGs and 16 HCs participated in this study. The PRGs was clearly explained to the subjects that they could not influence were recruited from Dutch addiction treatment centers, and the the outcome of the trials by their performance and that wins and HCs were recruited through advertisements in local newspapers. losses would be random, but that the highlighted area indicated Because most treatment-seeking PRGs are men, only male partici- their chance of winning. The participants started with 0 euros in the pants were included. The ethical review board of the Academic bank. In addition, participants were told that they would receive the Medical Centre approved the study, and all participants provided amount of money in the bank at the end of the task as part of their written informed consent. participant reimbursement. The PRGs were interviewed with section T of the Diagnostic Interview Schedule (28) to assess the diagnostic criteria for DSM- IV-TR Pathological Gambling. In addition, the South Oaks Gambling Imaging Acquisition and Preprocessing Screen (SOGS) (29) was administered as a general indication of Imaging data were obtained using a 3-Tesla Intera full-body MRI gambling problems and to facilitate comparisons with other stud- scanner (Philips Medical Systems, Best, The Netherlands) with a ies in PRGs and pathologic gamblers. phased array SENSE RF eight-channel receiver head coil. Thirty-five Exclusion criteria for all groups were as follows: lifetime diagno- axial slices (voxel size 2.29 ϫ 2.29 ϫ 3mm, matrix size 96*96 mm, sis of schizophrenia or psychotic episodes; 12-month diagnosis of repetition time/echo time ϭ 2.3 sec/30 msec) of T2*-weighted echo manic disorder (Composite International Diagnostic Interview planar images, sensitive to blood oxygenation level–dependent
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