Differential dependence of Pavlovian incentive motivation and instrumental incentive learning processes on dopamine signaling

Abstract

Here we attempted to clarify the role of dopamine signaling in reward seeking. In Experiment 1, we assessed the effects of the dopamine D(1)/D(2) receptor antagonist flupenthixol (0.5 mg/kg i.p.) on Pavlovian incentive motivation and found that flupenthixol blocked the ability of a conditioned stimulus to enhance both goal approach and instrumental performance (Pavlovian-to-instrumental transfer). In Experiment 2 we assessed the effects of flupenthixol on reward palatability during post-training noncontingent re-exposure to the sucrose reward in either a control 3-h or novel 23-h food-deprived state. Flupenthixol, although effective in blocking the Pavlovian goal approach, was without effect on palatability or the increase in reward palatability induced by the upshift in motivational state. This noncontingent re-exposure provided an opportunity for instrumental incentive learning, the process by which rats encode the value of a reward for use in updating reward-seeking actions. Flupenthixol administered prior to the instrumental incentive learning opportunity did not affect the increase in subsequent off-drug reward-seeking actions induced by that experience. These data suggest that although dopamine signaling is necessary for Pavlovian incentive motivation, it is not necessary for changes in reward experience, or for the instrumental incentive learning process that translates this experience into the incentive value used to drive reward-seeking actions, and provide further evidence that Pavlovian and instrumental incentive learning processes are dissociable.

Nucleus Accumbens Acetylcholine Receptors Modulate Dopamine and Motivation

“…Each CS lasted 2 min with a 4-min fixed intertrial interval. PIT has been robustly demonstrated in both Long Evans (Corbit et al, 2007;Wassum et al, 2011) and Sprague Dawley (Saddoris et al, 2011;Wassum et al, 2013) rats with procedures similar to those here, and the PIT effect was shown here to be similar in magnitude in the control conditions in both species.…”

“…The PIT behavioral task procedures are similar to those described previously (Wassum et al, 2011(Wassum et al, , 2013. For Experiment 1, training and testing took place in a set of 16 Med Associates (East Fairfield, VT) operant chambers described previously (Malvaez et al, 2015).…”

Differential Effects of Systemic Cholinergic Receptor Blockade on Pavlovian Incentive Motivation and Goal-Directed Action Selection

“…Both families of receptors are highly expressed in brain areas implicated in instrumental learning and performance, including the striatum, prefrontal cortex, and amygdala (Goldberg et al, 2012;Leslie et al, 2013;Thiele, 2013). Acetylcholine is also known to be involved in regulating dopamine signaling (Cachope et al, 2012;Chapman et al, 1997;Di Giovanni and Shi, 2009;Threlfell et al, 2012), a neuromodulator that has been more directly implicated in motivated behavior and is known to underlie the response-invigorating influence of rewardpaired cues on reward-seeking behavior (Dickinson et al, 2000;Lex and Hauber, 2008;Ostlund and Maidment, 2012;Wassum et al, 2011Wassum et al, , 2013. While acetylcholine has been implicated in various aspects of reward-motivated behavior (Mendez et al, 2012;Pratt and Kelley, 2004;Ragozzino et al, 2009), much remains unknown about its specific contributions to action selection.…”

“…The influence of reward-paired cues on instrumental action selection is mediated by separate behavioral and neural processes from those underlying the selection of actions based on changes in reward value (Dickinson et al, 2000;Holland, 2004;Balleine, 2007a, 2008b;Wassum et al, 2011). This latter aspect of action selection can be assayed through outcome devaluation testing.…”

“…For instance, rats tend to increase their performance of a lever-press action that once produced food reward when non-contingently presented with a Pavlovian cue that independently signals food reward (Dickinson et al, 2000;Wassum et al, 2011). Importantly, when rats are trained on distinct pairs of stimulus-outcome (S1-O1 and S2-O2) and action-outcome (A1-O1 and A2-O2) contingencies, these stimuli also acquire the ability to bias action selection at test, such that rats selectively increase their performance of whichever instrumental action was trained with the same outcome as the eliciting stimulus (eg, S1-A1) (Corbit and Balleine, 2005;Kruse et al, 1983).…”