Mesolimbic dopamine transmission during decisions involving cost-benefit tradeoffs

Abstract

Real-world decisions frequently involve tradeoffs between multiple economic dimensions, and the integration of benefits and costs into a common currency of subjective value is fundamental to action selection. Phasic dopamine is widely regarded as a critical teaching signal for learning the values assigned to actions, and these stored ("cached") values can be read out from the dopamine response to the unexpected presentation of reward-predictive cues. In Chapter 1, I introduce current theories of the neural basis of economic decision making and focus on how phasic dopamine is thought to contribute to these processes. In Chapter 2, I present data testing the critical question of whether dopamine-associated cached values align with animals' subjective preferences in a decision-making task involving cost-benefit tradeoffs. Here, I observed a significant inversion between animals' behavioral preferences and the rank ordering of dopamine-reported cached values, indicating that these cached values cannot be the sole determinant of choices in simple economic decision making. These data challenge the fundamental tenet of contemporary theories of decision making which posit that dopamine-associated cached values are sufficient to serve as the basis for action selection. In Chapter 3, I examine the question of which variant of reinforcement learning algorithms is instantiated by phasic dopamine transmission, as previous reports in the literature have arrived at conflicting conclusions. Using the cost-benefit tradeoff task described in Chapter 2, I analyzed what cue-evoked dopamine encodes when animals face choices between concurrently available options, finding that cue-evoked dopamine signals the cached value of the chosen option. Consistent with the notion that phasic dopamine transmission enacts an "on-policy" reinforcement learning algorithm that updates based on chosen state-action values, these results indicate that cue-evoked dopamine reflects post-decision information about the expected value of the outcome of an action that has already been selected via other neural substrates. In Chapter 4, I conclude by summarizing and integrating these results, discussing how the contributions of phasic dopamine to cost-benefit decision making are more limited and perhaps more nuanced than previously thought. I extend this discussion to describe other neural substrates which might contribute to the aspects of decision making not accommodated by phasic dopamine transmission.