Abstract

The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to be compared continuously with potential rewards that could be obtained by traveling elsewhere (background reward rate), to determine the opportunity cost of staying versus leaving. We hypothesized that dopamine specifically modulates the influence of background, but not foreground, reward information when making a dynamic comparison of these variables for optimal behavior. On a novel foraging task based on an ecological account of animal behavior (marginal value theorem), human participants of either sex decided when to leave locations in situations where foreground rewards depleted at different rates, either in rich or poor environments with high or low background reward rates. In line with theoretical accounts, people's decisions to move from current locations were independently modulated by changes in both foreground and background reward rates. Pharmacological manipulation of dopamine D2 receptor activity using the agonist cabergoline significantly affected decisions to move on, specifically modulating the effect of background reward rates. In particular, when on cabergoline, people left patches in poor environments much earlier. These results demonstrate a role of dopamine in signaling the opportunity cost of rewards, not value per se. Using this ecologically derived framework, we uncover a specific mechanism by which D2 dopamine receptor activity modulates decision-making when foreground and background reward rates are dynamically compared.SIGNIFICANCE STATEMENT Many decisions, across economic, political, and social spheres, involve choices to “leave”. Such decisions depend on a continuous comparison of a current location's value, with that of other locations you could move on to. However, how the brain makes such decisions is poorly understood. Here, we developed a computerized task, based around theories of how animals make decisions to move on when foraging for food. Healthy human participants had to decide when to leave collecting financial rewards in a location, and travel to collect rewards elsewhere. Using a pharmacological manipulation, we show that the activity of dopamine in the brain modulates decisions to move on, with people valuing other locations differently depending on their dopaminergic state.

Highlights

  • The mesolimbic dopaminergic system plays a crucial role in motivating behavior and has been closely linked to neural circuits which convey information about incentives (Schultz and Dickinson, 2000; Haber and Knutson, 2010; Salamone and Correa, 2012; Hamid et al, 2016)

  • Healthy human foragers are guided by Marginal Value Theorem (MVT) principles Within MVT, foreground and background reward rates should have independent effects on how long an individual remains in a patch

  • Are healthy people optimal foragers? participants showed effects in the directions predicted by MVT, we wanted to know whether the magnitude of these effects conform to foraging theories, which stipulate the optimal time to leave each patch

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Summary

Introduction

The mesolimbic dopaminergic system plays a crucial role in motivating behavior and has been closely linked to neural circuits which convey information about incentives (Schultz and Dickinson, 2000; Haber and Knutson, 2010; Salamone and Correa, 2012; Hamid et al, 2016). Le Heron et al · Dopamine Modulates Dynamics of Foraging overcoming costs to obtain rewards (Salamone and Correa, 2012; Le Bouc et al, 2016; Syed et al, 2016; Le Heron et al, 2018b) and for learning about rewarding outcomes to update future behavior (Pessiglione et al, 2006; Schultz, 2016). Animal models increasingly highlight that dopamine signals change gradually as the rate of obtaining rewards changes, suggesting a need to examine dopamine’s role in settings where rewards are dynamically accrued (Howe et al, 2013; Hamid et al, 2016; Mohebi et al, 2019)

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