Toward isolating the role of dopamine in the acquisition of incentive salience attribution

Abstract

Stimulus-reward learning has been heavily linked to the reward-prediction error learning hypothesis and dopaminergic function. However, some evidence suggests dopaminergic function may not strictly underlie reward-prediction error learning, but may be specific to incentive salience attribution. Utilizing a Pavlovian conditioned approach procedure consisting of two stimuli that were equally reward-predictive (both undergoing reward-prediction error learning) but functionally distinct in regard to incentive salience (levers that elicited sign-tracking and tones that elicited goal-tracking), we tested the differential role of D1 and D2 dopamine receptors and nucleus accumbens dopamine in the acquisition of sign- and goal-tracking behavior and their associated conditioned reinforcing value within individuals. Overall, the results revealed that both D1 and D2 inhibition disrupted performance of sign- and goal-tracking. However, D1 inhibition specifically prevented the acquisition of sign-tracking to a lever, instead promoting goal-tracking and decreasing its conditioned reinforcing value, while neither D1 nor D2 signaling was required for goal-tracking in response to a tone. Likewise, nucleus accumbens dopaminergic lesions disrupted acquisition of sign-tracking to a lever, while leaving goal-tracking in response to a tone unaffected. Collectively, these results are the first evidence of an intraindividual dissociation of dopaminergic function in incentive salience attribution from reward-prediction error learning, indicating that incentive salience, reward-prediction error, and their associated dopaminergic signaling exist within individuals and are stimulus-specific. Thus, individual differences in incentive salience attribution may be reflective of a differential balance in dopaminergic function that may bias toward the attribution of incentive salience, relative to reward-prediction error learning only.

Stimulation of dopamine D 1 receptor improves learning capacity in cooperating cleaner fish

“…Recently, Darvas et al [70] found that animals are capable of associative learning with as little as 30% of baseline DA levels. Additionally, DA blockade may only impair associative learning in animals with a tendency to learn through a form of stimulus-reward learning where DA-mediated incentive salience is attributed to reward cues [10,71,72], but not of those forms that instead rely on the predictive value of such reward cues [70]. Here, none of the administered antagonists (D 1 and D 2 ) delayed the cleaners' learning ability in either of the two tasks, probably because DA signalling did not decrease to a degree where it would compromise the acquisition of a basal conditioned response.…”

Suboptimal choice in rats: Incentive salience attribution promotes maladaptive decision-making

“…Additionally, it has been demonstrated that CSs that elicit sign-tracking are indicative of greater conditioned reinforcing value in rats, relative to CSs that elicit goal-tracking, and can promote suboptimal behavior (e.g. Beckmann and Chow, 2015; Chow et al 2016). Hence, by using lever stimuli that elicit sign-tracking, equating stimulus function to that used with pigeons, terminal-link stimuli are capable of producing suboptimal choice in both rats and pigeons.…”

“…For example, when pitted against each other, rats have shown a preference for a CS attributed with incentive value over a CS without incentive value, even if the preference results in significantly reduced primary reinforcement (cf. Beckmann and Chow, 2015; Chow et al 2016). Collectively, these studies suggest that not all CSs function equivalently and, despite being equally predictive, CSs attributed with incentive value can significantly influence decision-making, leading to maladaptive decisions.…”

Cannabinoid receptor-1 signaling contributions to sign-tracking and conditioned reinforcement in rats

“…Here, we first determine whether systemic injections of the CB1 receptor inverse agonist, rimonabant, mimic the reduction in sign-tracking observed by antagonizing DA receptors (Flagel, Clark et al 2011, Saunders and Robinson 2012, Clark, Collins et al 2013, Chow, Nickell et al 2016, Fraser and Janak 2017). The endogenous mechanism of eCB modulation of dopamine release occurs in the ventral tegmental area (VTA), via CB1 receptor mediated inhibition of GABAergic neurotransmission onto DA neurons.…”