Phasic nucleus accumbens dopamine release encodes effort- and delay-related costs

Abstract

Background: Optimal decision-making requires that organisms correctly evaluate both the costs and benefits of potential choices. Dopamine transmission within the nucleus accumbens (NAc) has been heavily implicated in reward-learning and decision-making, but it is unclear how dopamine release might contribute to decisions that involve costs.

Methods: Cost-based decision-making was examined in rats trained to associate visual cues with either immediate or delayed rewards (delay manipulation) or low-effort or high-effort rewards (effort manipulation). After training, dopamine concentration within the NAc was monitored on a rapid time scale with fast-scan cyclic voltammetry.

Results: Animals exhibited a preference for immediate or low-effort rewards over delayed or high-effort rewards of equal magnitude. Reward-predictive cues but not response execution or reward delivery evoked increases in NAc dopamine concentration. When only one response option was available, cue-evoked dopamine release reflected the value of the future reward, with larger increases in dopamine signaling higher-value rewards. In contrast, when both options were presented simultaneously, dopamine signaled the better of two options, regardless of the future choice.

Conclusions: Phasic dopamine signals in the NAc reflect two different types of reward cost and encode potential rather than chosen value under choice situations.

Figure 1

Behavioral preference tracks reward cost. (A) Schematic representing effort-based or delay-based behavioral tasks. On forced-choice low cost/immediate reward trials (left panel), a cue light was presented for 5s and was followed by extension of two response levers into the behavioral chamber. A single lever press (FR1) on the lever corresponding to the cue light led to immediate reward (45 mg sucrose) delivery in a centrally located food receptacle. Responding on the other lever did not produce reward delivery and terminated the trial. On forced choice high cost/delayed reward trials, the other cue light was presented for 5s before lever extension. On these trials, a reward was delivered after either sixteen responses (FR16, effort based decision task) or a delay (FR1 + 5s delay, delay based decision task). Responses on the opposite lever terminated the trial and no reward was delivered. On free choice trials, both cues were presented, and animals could select either response option. After training, dopamine concentration in the NAc was measured using fast-scan cyclic voltammetry during a single 90-trial behavioral session. Behavioral performance in effort (B–D) and delay (E–G) based decision tasks during electrochemical recording. All data are mean ± SEM. (B,E) Percentage of possible rewards obtained on forced-choice trials. Animals overcame high effort requirements and reward delays to maximize rewards. (C,F) Percentage of errors on forced-choice trials in both tasks were significantly below chance levels (50%; p < 0.0001 for all comparisons), indicating behavioral discrimination between cues. (D,G) Response allocation on free-choice trials, as percentage of choices. Dashed line indicates indifference point. Animals robustly preferred the low cost and immediate reward options (* p < 0.01). (H,I) Behavior-related changes in dopamine across multiple trials for representative animals on effort (H) and delay (I) tasks. Heat plots represents individual trial data, rank ordered by distance from lever extension (black triangle) to reward delivery (black circles), whereas bottom trace represents average from all trials. Data are aligned to cue onset (horizontal bars). For all trial types, dopamine release peaks after cue presentation, but high value cues evoke larger increases in dopamine concentration.

Figure 2

Dopamine release in the NAc core encodes the value of the best available response. (A,B) Left panels: Change in dopamine concentration on forced-choice trials, aligned to cue onset (black bar). Right panels: Peak cue-evoked dopamine signal on forced choice trials. Cue presentation on low cost and immediate reward trials led to significantly larger increases in dopamine concentration than cue presentation on high cost and delayed reward trials, respectively. (C,D) Change in dopamine concentration (left panels) and peak dopamine signals (right panels) on free-choice trials. Conventions follow from A,B. On free-choice trials, cue-evoked dopamine signals did not reflect the value of the chosen option. All data are mean ± SEM. *p < 0.01. DA, dopamine; n.s., not significant.