In this study, eye-tracking measurements were performed during a gambling task to compare gaze allocation and pupillary dynamics between PGs and NPGs. Gaze allocation was generally more concentrated around the peaks in PGs than in NPGs. In addition, more narrowly focused gaze was observed for the left-hand pictures in the decision phase in NPGs than in PGs. Furthermore, in the decision and feedback phases, gaze allocation was greater to the right picture than to the left picture in PGs, but not in NPGs. Only PGs showed significant differences in pupillary dynamics between the reward and control conditions, and between the punishment and control conditions. To our knowledge, this study is the first to demonstrate distinctive gaze allocation and pupillary dynamics characteristics in PGs while engaged in gambling.
Consistent with our hypothesis regarding attentional allocation, higher ratios of gaze allocation time were observed in PGs than in NPGs around the peaks in the decision, feedback, and fixation phases. Previous studies indicated that PGs had attentional bias to gambling-related stimuli compared to neutral stimuli.9,26 Unlike previous studies that used non-gambling tasks (e.g., Stroop, flicker, and lexical salience tasks) (Brevers et al. 2011; McCusker and Gettings 1997; Zack and Poulos 2004), the PGs received rewards and avoided punishments based on their choice of neutral stimuli in this study. They may, therefore, have concentrated not only on the stimuli but also on the overall task. This would be consistent with the finding that their attentional allocation was greater even in the fixation phase. While PGs gazed at the left-hand pictures more than the NPGs during the decision phase, peripheral gaze was “higher” for NPGs than PGs. This was presumably because PGs inspected the pictures more carefully, in an attempt to identify winning strategies that did not actually exist, while the NPGs explored a wider range of pictures. However, this difference was not observed for the right-hand pictures, possibly due to the masking effect of an attentional preference for the right-hand pictures in PGs. Left unilateral spatial neglect due to right hemispheric injury has been reported in neuropsychological studies.30 Heilman et al. proposed a theoretical model of unilateral spatial neglect, in which the left hemisphere directs attention to the right side, and the right hemisphere to both sides.31 Based on this model, increased activity in the left hemisphere or decreased activity in the right hemisphere may result in an attentional bias to the right side in PGs. Davidson et al. proposed a model of cerebral asymmetry and approach-withdrawal, in which the left hemisphere exhibited greater activation during approach and the right hemisphere exhibited greater activation during withdrawal. This model has been supported by numerous studies.32–34 Some studies have indicated that this hemispheric asymmetry influences BIS/BAS scores,35–37 whereby activation of the left hemisphere was greater in participants with higher BAS scores and they made more disadvantageous choices in the Iowa Gambling Task.38,39 In the present study, PGs had significantly higher BAS, SR, and SSS-AE thrill and adventure seeking and experience seeking subscale scores. In another study, higher novelty-seeking scores were associated with greater rightward attentional bias, and it was suggested that this bias was related to dopamine asymmetry favoring the left hemisphere.40 Thus, excessive activity in the left hemisphere may lead to an attentional preference to the right side in PGs.
Consistent with our hypothesis regarding pupillary dynamics, the differences in z-values between the congruent and incongruent conditions reflected significant differences between the reward and control conditions, and between the punishment and control conditions, only in PGs. Because pupillary dilation reflects activity in noradrenergic locus coeruleus neurons,10,11 the sympathetic nervous system in PGs may be excited by rewards and punishments. Previous studies reported pupillary dilation during reward anticipation and violation of expectation.12–17 Significant differences in responses to punishment were observed mainly in the feedback phase, while differences in responses to reward were observed in the fixation phase. Therefore, punishments may surprise PGs, and rewards may enhance reward anticipation for the next trial. However, significant differences in responses to punishment were also observed in the decision phase, although there were no discernible differences between the conditions. Previous studies have reported irrational behavior during gambling (i.e., chasing losses), whereby people make riskier decisions after a loss than after a win, and decide to continue gambling despite considerable losses (Brevers et al. 2017; Campbell-Meiklejohn et al. 2008; Gainsbury et al. 2014). It is possible that prior trials may influence the neural activity of PGs in the decision phase.
Our investigations of attentional allocation and pupillary dynamics during gambling tasks indicate that there are two distinctive cognitive processing pathways in PGs. First, PGs allocate more attention to the right side because of asymmetrical activation favoring the left hemisphere. Second, PGs show pupillary dilation in association with noradrenergic locus coeruleus activity because of punishment-mediated surprise and expectations of future rewards. These results also demonstrate the advantages of sample-specific analysis in terms of both attentional allocation and pupillary dynamics to avoid canceling out significant differences by data integration. In fact, the significantly greater attentional allocation to the left-hand pictures by PGs in the sample-specific analysis was not observed in the analysis of gaze allocation toward the whole picture. However, problematic behaviors in PGs could not be identified because the outcomes of gambling were completely controlled. Future studies should examine how these differences in attentional allocation and pupillary dynamics are related to cognitive abnormalities and behaviors in problem gambling and gambling disorder.