A selective role for dopamine in stimulus–reward learning

Abstract

Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, whereby they themselves become attractive and desirable incentive stimuli. But individuals differ in whether a cue acts solely as a predictor that evokes a conditional response, or also serves as an incentive stimulus, and this determines the degree to which a cue might bias choice or even promote maladaptive behavior. Here we use rats that differ in the incentive motivational properties they attribute to food cues to probe the role of the neurotransmitter dopamine in stimulus-reward learning. We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors. Rather, dopamine acts selectively in a form of reward learning in which “incentive salience” is assigned to reward cues. In individuals with a propensity for this form of learning, reward cues come to powerfully motivate and control behavior. This work provides insight into the neurobiology of a form of reward learning that confers increased susceptibility to disorders of impulse control.

The role of learning-related dopamine signals in addiction vulnerability

“…This has consequences for learning accounts of addiction as some learning tendencies appear to confer vulnerability towards developing addiction. In this part, we first present the data on individual differences in Pavlovian responding in some detail (mainly reiterating the findings of Flagel et al 2011b), then discuss its interpretation in terms of incentive salience (Berridge and Robinson, 1998;Berridge, 2004Berridge, , 2007Saunders and Robinson, 2012), and finally put forth a hypothesis that proposes a connection between the propensity to assign incentive salience and the propensity to employ model-free learning (McClure et al, 2003a;Huys et al, 2013b;Lesaint et al, 2013;Dayan and Berridge, 2013).…”

“…Flagel et al (2011b) used fast-scan cyclic voltammetry in the core of the nucleus accumbens to characterize cue-induced phasic dopamine signaling during Pavlovian training in selectively bred rats predisposed towards sign-or goal-tracking behavior. Similar to outbred rats, these selectively bred phenotypes both learned a conditioned response and did so at the same rate.…”

“…Next, Flagel et al (2011b) asked whether the development of either a goal-or sign-tracking responses was dependent on dopamine. They administered a nonspecific dopamine antagonist, flupenthixol systemically prior to the first of several Pavlovian training sessions.…”

“…These differences suggest that sign trackers acquire a cached value V MF (s) in accordance with the temporal prediction hypothesis, but that goal trackers do not. Data in B,C,E,F adapted from Flagel et al (2011b).…”

“…Phasic dopaminergic signals appear to serve as teaching signals (Montague et al, 1996;Schultz et al, 1997) and be central to the attribution of incentive salience (Flagel et al, 2011b). The development of substance abuse and addiction likely involves the usurpation of such dopaminergic learning or incentive salience attribution signals (Volkow et al, 2009;Dayan, 2009;Flagel et al, 2011b).…”