Self-Controlled Choice Arises from Dynamic Prefrontal Signals That Enable Future Anticipation

Abstract

Self-control allows humans the patience necessary to maximize reward attainment in the future. Yet it remains elusive when and how the preference to self-controlled choice is formed. We measured brain activity while female and male humans performed an intertemporal choice task in which they first received delayed real liquid rewards (forced-choice trial), and then made a choice between the reward options based on the experiences (free-choice trial). We found that, while subjects were awaiting an upcoming reward in the forced-choice trial, the anterior prefrontal cortex (aPFC) tracked a dynamic signal reflecting the pleasure of anticipating the future reward. Importantly, this prefrontal signal was specifically observed in selfcontrolled individuals, and moreover, interregional negative coupling between the prefrontal region and the ventral striatum (VS) became stronger in those individuals. During consumption of the liquid rewards, reduced ventral striatal activity predicted self-controlled choices in the subsequent free-choice trials. These results suggest that a well-coordinated prefrontalstriatal mechanism during the reward experience shapes preferences regarding the future self-controlled choice.

Prefrontal-Striatal Mechanisms of Behavioral Impulsivity During Consumption of Delayed Real Liquid Rewards

“…Interestingly, in the previous studies, the aPFC regions exhibited an anticipatory utility effect during the delay period and the effect was enhanced in shallow discounters (Jimura et al, 2013;Tanaka et al, 2020), whereas in the current study, the consumption period activity was reduced in shallow discounters (Figure 5 left; see ''Discussion'' section for details).…”

“…aPFC ROIs were defined as spheres with an 8-mm radius that were centered at bilateral aPFC coordinates showing an anticipatory utility effect during the delay period, as reported in our previous study analyzing the identical data set [coordinates: (28, 54, −7), (−31, 55, −7); Table 1 in Jimura et al, 2013]. These bilateral aPFC regions also showed the anticipatory utility effect in our recent study (Tanaka et al, 2020). For exploratory analysis, a small-volume correction approach was used, and statistical significance levels of the peak were corrected for multiple comparisons within the aPFC ROIs using voxel-level family-wise error rates.…”

“…The ventral striatum (VS) is implicated as a core neural site involved in impulsive decision-making (McClure et al, 2004(McClure et al, , 2007Tanaka et al, 2004Tanaka et al, , 2020Jimura et al, 2013), whereas the prefrontal cortex (PFC) is associated with less impulsive (or self-controlled) decision-making (McClure et al, 2004(McClure et al, , 2007Shamosh et al, 2008;Hare et al, 2009;Jimura et al, 2013Jimura et al, , 2018Tanaka et al, 2020). These involvements of the PFC and VS raise the possibility that a PFC-VS mechanism plays an important role in determining impulsivity in value-based decision-making.…”

“…Intertemporal choice paradigms using delayed real liquid rewards (Jimura et al, 2009(Jimura et al, , 2011(Jimura et al, , 2013Tanaka et al, 2020) could provide a unique opportunity to examine brain mechanisms involved in the direct experiences of delayed rewards. In these paradigms, humans make choices between two alternatives, one larger amount of liquid reward delayed by tens of seconds, and a smaller amount of liquid reward available immediately (Figure 1A).…”

“…Prior human studies examining the neural mechanisms of intertemporal choice behavior have mainly focused on the choice period (McClure et al, 2004 , 2007 ; Tanaka et al, 2004 ; Hariri et al, 2006 ; Kable and Glimcher, 2007 ; Peters and Buechel, 2010 ), with a few exceptions examining temporal changes in brain activity while future outcomes were anticipated (Berns et al, 2006 ; Jimura et al, 2013 ; McGuire and Kable, 2015 ; Tanaka et al, 2020 ). However, it remains unclear how the PFC-VS mechanism is involved while a behavioral agent is receiving a reward after having waited for it, despite the collective evidence that the VS and PFC are associated with behavioral impulsivity and self-control.…”