The dopamine dip amplitude is a quantitative measure of disappointment

Abstract

AbstractGreat expectations can lead to greater disappointment when the desired results are not achieved. Although it is well-documented that a better-than-expected reward is encoded quantitatively via midbrain dopaminergic (DA) activity, it has been less addressed experimentally whether disappointment, a worse-than-expected outcome is also expressed quantitatively by the DA signal. We show that the degree of disappointment is quantified by the magnitude of a transient decrease in the extracellular DA concentration (DA dip) in the ventral striatum of mice. We set up a lever press task on a fixed ratio (FR) schedule requiring five lever presses as an effort for a food reward (FR5). Mice occasionally checked the food magazine without a reward before completing the task. The percentage of this premature magazine entry (PME) increased as the number of lever presses approached five. This behavioral readout shows rising expectations with increasing proximity to task completion, leading to greater disappointment in the mice. Fiber photometry of the extracellular DA dynamics in the ventral striatum using a fluorescent protein (genetically encoded GPCR-activation-based-DA sensor: GRABDA2m) revealed that the amplitude of the DA dip following a PME was correlated with the percentage of the PME, demonstrating a monotonic relationship between the DA dip amplitude and the degree of disappointment. Computational modeling of the lever press task implementing temporal difference errors and state transitions replicated the positive correlation between the PME frequency and DA dip amplitude during improvement of the FR5 task. Taken together, these findings indicate that the degree of disappointment while making an effort toward a goal is represented monotonically by the magnitude of the DA dip in the ventral striatum, which may guide behavioral adjustment.