Nucleus Accumbens Neurons Track Behavioral Preferences and Reward Outcomes During Risky Decision Making

Abstract

Background In order to make appropriate decisions, organisms must evaluate the risks and benefits of action selection. The nucleus accumbens (NAc) has been shown to be critical for this processing, and is necessary for appropriate risk-based decision making behavior. However, it is not clear how NAc neurons encode this information to promote appropriate behavioral responding. Methods Here, rats (n=17) were trained to perform a risky decision making task in which discrete visual cues predicted the availability to respond for a smaller certain (safer) or larger uncertain (riskier) reward. Electrophysiological recordings were made in the NAc core and shell to evaluate neural activity during task performance. Results At test, animals exhibited individual differences in risk-taking behavior; some displayed a preference for the risky option, some the safe option, and some did not have a preference. Electrophysiological analysis indicated that NAc neurons differentially encoded information related to risk versus safe outcomes. Further, during free choice trials, neural activity during reward-predictive cues reflected individual behavioral preferences. In addition, neural encoding of reward outcomes was correlated with risk taking behavior, with safe-preferring and risk-preferring rats showing differential activity in the NAc core and shell during reward omissions. Conclusions Consistent with previously demonstrated alterations in prospective reward value with effort and delay, NAc neurons encode information during reward-predictive cues and outcomes in a risk task that tracked the rats’ preferred responses. This processing appears to contribute to subjective encoding of anticipated outcomes, and thus may function to bias future risk-based decisions.

Nucleus accumbens core neurons encode value-independent associations necessary for sensory preconditioning.

“…One possible explanation for this observation is a lack of sensitivity to detect inhibitions due to the population averaging method employed here, particularly given that the noted low resting baseline activity of medium spiny neurons (MSNs) in the NAc. However, we found approximately equal proportions of inhibitions and excitations during Preconditioning, and in previous work, we have shown the ability to detect differences in inhibitory encoding based on task demands in the NAc (Sugam et al, 2014). An alternative interpretation is that excitatory encoding displayed here during Preconditioning and Test reflects important processing components for NAc and its limbic inputs.…”

“…Neural firing was assessed using similar methods as described previously from our lab (Sugam et al, 2014). For each cue ( A, B, X and Y ), we calculated the expected (i.e., average) firing rate in each 250ms bin averaged across all the trials for that cue in that session.…”

Neural activation during risky decision-making in youth at high risk for substance use disorders

“…Hence, the inverse pattern of activation observed between groups on the explosion outcomes in the ventral striatum raises the possibility of deficits in reward learning, particularly in the context of uncertain outcomes. Of note, in rats, the ventral striatal encoding of reward outcomes was correlated with later risk-taking behavior (Sugam et al, 2014), suggesting a neural mechanism underlying future risk-taking in HR youth (Pasupathy and Miller, 2005; Lau and Glimcher, 2007; Yamada et al, 2011). In the case of the BART, striatal activity was greater for unexpected explosions in the HC group, possibly because these trials required an “update” to learned patterns.…”

Modeling risky decision-making in nonhuman animals: shared core features

“…Nevertheless, some of the tasks used in rats match the blocked macaque paradigm, in that choices are between a risky and a safe option with equivalent expected values (rats: [19,20]; mice: [21])…”

“…When expected values are equalized, rats range from risk-seeking to risk-averse ([20,44], see [3] for an early review), with substantial individual differences within and between experiments. Unfortunately, the range of risk preferences in macaques is largely unknown, because the cost of each research subject makes testing large numbers prohibitive.…”