Dopamine modulates reward expectancy during performance of a slot machine task in rats: evidence for a 'near-miss' effect

Abstract

Cognitive accounts of gambling suggest that the experience of almost winning-so-called 'near-misses'-encourage continued play and accelerate the development of pathological gambling (PG) in vulnerable individuals. One explanation for this effect is that near-misses signal imminent winning outcomes and heighten reward expectancy, galvanizing further play. Determining the neurochemical processes underlying the drive to gamble could facilitate the development of more effective treatments for PG. With this aim in mind, we evaluated rats' performance on a novel model of slot machine play, a form of gambling in which near-miss events are particularly salient. Subjects responded to a series of three flashing lights, loosely analogous to the wheels of a slot machine, causing the lights to set to 'on' or 'off'. A winning outcome was signaled if all three lights were illuminated. At the end of each trial, rats chose between responding on the 'collect' lever, resulting in reward on win trials, but a time penalty on loss trials, or starting a new trial. Rats showed a marked preference for the collect lever when both two and three lights were illuminated, indicating heightened reward expectancy following near-misses similar to wins. Erroneous collect responses were increased by amphetamine and the D(2) receptor agonist quinpirole, but not by the D(1) receptor agonist SKF 81297 or receptor subtype selective antagonists. These data suggest that dopamine modulates reward expectancy following the experience of almost winning during slot machine play, via activity at D(2) receptors, and this may result in an enhancement of the near-miss effect and facilitate further gambling.

Figure 1

Schematic diagram showing the trial structure for the slot machine task. A response on the roll lever starts the first light flashing (a). Once the animal responds in each flashing aperture, the light inside sets to on or off and the neighboring hole starts to flash (b, c). Once all three lights have been set, the rat has the choice to start a new trial, by responding on the roll lever, or responding on the collect lever. On win trials, where all the lights have set to on, a collect response delivers 10 sugar pellets (d). If any of the lights have set to off, a response on the collect lever instead results in a 10 s time-out period (e). There are eight possible light patterns (f). A win is clearly signaled by all three lights setting to on, and a clear loss is evident when all of the lights are set to off.

Figure 2

Baseline performance of the slot machine task. On win trials, when all three lights had set to on ((1,1,1)), animals chose the collect lever 100% of the time (a, b). As the number of lights illuminated decreased, so did the preference for the collect lever (a). Animals consistently showed a strong preference for the collect lever on 2-light losses, or near-miss trials. The proportion of collect responses made on both 2-light and 1-light losses also varied according to the precise pattern of lights illuminated (b). In the first week of training, rats were slower to respond in the subsequent hole if the previous hole had set to off (c). However, this differential effect was no longer observed once stable choice behaviour has been established. This pattern was observed for both the middle and last holes, therefore, the graph reflects the combined data from both holes. All data shown are the mean across five sessions±SEM.

Figure 3

Effects of amphetamine on performance of the slot machine task. Amphetamine dose-dependently increased the proportion of collect errors on clear loss and 1-light loss trials (a). More specifically, amphetamine significantly increased collect responses on on (0,0,0) and (0,0,1) trial types (b). The lowest and highest dose of amphetamine also made animals more sensitive to the illumination status of the holes, in that they were once more faster to respond if the previous hole had set to on rather than off (c). Data are shown as the mean±SEM.

Figure 4

Effects of quinpirole on performance of the slot machine task. Quinpirole dose-dependently increased collect errors on all loss trials (a, b). This effect was particularly pronounced on 1-light and 2-light losses at the lowest dose tested. Quinpirole also increased the latency to respond at the array regardless of the illumination status of the holes (c). Data are shown as the mean±SEM.

Figure 5

Effect of removing near-miss trials during extinction on both the rate of extinction and subsequent reinstatement of task performance. The presence or absence of near-miss trials did not affect the rate of extinction as indicated by the number of trials completed per session (a). However, rats which had not experienced near-miss trials during extinction were faster to pick up the task again once win trials were rewarded. During this reinstatement phase, near-miss trials were again present for both groups. Despite the difference in the number of trials completed, the proportion of collect responses made across the different trial types was similar in both groups, even within the first three sessions of reinstatement (b). Although rats that did not experience near-miss trials during extinction were initially faster to response in the subsequent hole if the previous hole had set to on (c), both groups of rats were sensitive to the illumination status of the holes by the end of reinstatement (c, d).