Elsevier

Biological Psychiatry

Volume 71, Issue 3, 1 February 2012, Pages 199-205
Biological Psychiatry

Archival Report
Phasic Nucleus Accumbens Dopamine Encodes Risk-Based Decision-Making Behavior

https://doi.org/10.1016/j.biopsych.2011.09.029Get rights and content

Background

To optimize behavior, organisms evaluate the risks and benefits of available choices. The mesolimbic dopamine (DA) system encodes information about response costs and reward delays that bias choices. However, it remains unclear whether subjective value associated with risk-taking behavior is encoded by DA release.

Methods

Rats (n = 11) were trained on a risk-based decision-making task in which visual cues predicted the opportunity to respond for smaller certain (safer) or larger uncertain (riskier) rewards. Following training, DA release within the nucleus accumbens (NAc) was monitored on a rapid time scale using fast-scan cyclic voltammetry during the risk-based decision-making task.

Results

Individual differences in risk-taking behavior were observed as animals displayed a preference for either safe or risky rewards. When only one response option was available, reward predictive cues evoked increases in DA concentration in the NAc core that scaled with each animal's preferred reward contingency. However, when both options were presented simultaneously, cue-evoked DA release signaled the animals preferred reward contingency, regardless of the future choice. Furthermore, DA signaling in the NAc core also tracked unexpected presentations or omissions of rewards following prediction error theory.

Conclusions

These results suggest that the dopaminergic projections to the NAc core encode the subjective value of future rewards that may function to influence future decisions to take risks.

Section snippets

Behavioral Training

Male Sprague–Dawley rats aged 90 to 120 days (weighing 275–350 g) were used (see Supplement 1 for additional information). Sessions were conducted in 43 × 43 × 53 cm Plexiglas chambers housed in a sound-attenuated cubicle (Med Associates, St. Albans, Vermont). One side of the chamber had two retractable levers (Coulbourn Instruments, Allentown, Pennsylvania) 17 cm apart, with a stimulus light 6 cm above each lever. A white-noise speaker (80 dB) was located 12 cm above the floor on the opposite

Individual Differences in Risk-Taking Behavior

Rats (n = 8 rats with 11 recording locations in the NAc core) were able to learn the risky decision-making task and discriminate between the cue types as evidenced by a significant reduction in the percentage of errors on forced-choice safe and risk trials compared to session 1 [F(24,168) = 5.985, p < .00001; Figure 1B]. Furthermore, animals displayed a significant increase in the number of sucrose pellets received across all sessions compared to session 1 [F(24,168) = 3.585, p < .00001; Figure

Discussion

We show here that when rats were given the option to play it safe for a certain small reward or take a risk for a larger, uncertain reward, individual preferences were tracked by DA release in the NAc core. Thus, DA release does not simply encode extrinsic factors of reward value but also reflects intrinsic representations that can function to bias future decision-making behavior. Furthermore, consistent with its role as a reward prediction error signal (9), we also show that unexpected reward

References (37)

  • M.R. Roesch et al.

    Ventral striatal neurons encode the value of the chosen action in rats deciding between differently delayed or sized rewards

    J Neurosci

    (2009)
  • W. Schultz et al.

    A neural substrate of prediction and reward

    Science

    (1997)
  • J.J. Day et al.

    Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens

    Nat Neurosci

    (2007)
  • G.D. Stuber et al.

    Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons

    Science

    (2008)
  • L.A. Sombers et al.

    Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area

    J Neurosci

    (2009)
  • C.D. Fiorillo et al.

    Discrete coding of reward probability and uncertainty by dopamine neurons

    Science

    (2003)
  • P.N. Tobler et al.

    Adaptive coding of reward value by dopamine neurons

    Science

    (2005)
  • R.N. Cardinal et al.

    Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats

    BMC Neurosci

    (2005)
  • Cited by (104)

    • Neuronal activity associated with cocaine preference: Effects of differential cocaine intake

      2021, Neuropharmacology
      Citation Excerpt :

      Therefore, the possible mediational role of any neurobiological measure in reinforcer preference cannot be dissociated from the effects of reinforcer frequency and consequent intake under such conditions. Furthermore, given that most studies investigating the neurobiological mechanisms of decision-making using nondrug reinforcers (e.g., Padoa-Schioppa and Assad, 2006; Simon et al., 2011; Stopper et al., 2014; Sugam et al., 2012; Zeeb et al., 2009) rely on choice procedures that do not control for reinforcer frequency, the results of such studies are also, at least in principal, subject to the confound highlighted above. Relatedly, research into probabilistic nondrug outcomes has demonstrated that neuronal signaling is strongly related to the likelihood of reinforcement (Joshua et al., 2009; Morris et al, 2004, 2006).

    View all citing articles on Scopus
    View full text