Optogenetic activation of basolateral amygdala projections to nucleus accumbens core promotes cue-induced expectation of reward but not instrumental pursuit of cues

Abstract

Reward-associated conditioned stimuli (CS) can acquire predictive value, evoking conditioned approach behaviors that prepare animals to engage with forthcoming rewards. Such CS can also acquire conditioned reinforcing value, becoming attractive and pursued. Through their predictive and conditioned reinforcing properties, CS can promote adaptive (e.g., locating food) but also maladaptive responses (e.g., drug use). Basolateral amygdala neurons projecting to the nucleus accumbens core (BLA[->]NAc core neurons) mediate the response to appetitive CS, but the extent to which this involves effects on the predictive and/or conditioned reinforcing properties of CS is unclear. Thus, we examined the effects of optogenetic stimulation of BLA[->]NAc core neurons on conditioned approach behavior and on the instrumental pursuit of a CS, the latter a measure of conditioned reinforcement. Water-restricted, adult male rats learned that a light-tone compound cue (CS) predicts water delivery. Pairing optogenetic stimulation of BLA[->]NAc core neurons with CS presentation potentiated conditioned approach behavior, and did so even under extinction conditions, when water was omitted. This suggests that BLA[->]NAc core neurons promote cue-induced expectation of rewards. Rats also received instrumental conditioning sessions during which they could lever press for CS presentations, without water delivery. Optogenetic stimulation of BLA[->]NAc core neurons either during these instrumental test sessions or during prior CS-water conditioning did not influence lever responding for the CS. This suggests that BLA[->]NAc core neurons do not influence the conditioned reinforcing effects of CS. We conclude that BLA[->]NAc core neurons promote cue-induced control over behavior by increasing cue-triggered anticipation of rewards, without influencing cue wanting. SIGNIFICANCE STATEMENTEnvironmental cues associated with rewards guide animals toward rewards essential for survival such as food. Reward-associated cues can also evoke maladaptive responses such as in addiction. Reward cues guide behavior in two major ways. First, they evoke approach toward imminent rewards, preparing animals to engage with these rewards. Second, cues can become attractive themselves, such that animals will learn new behaviors simply to obtain them. Here we show that activation of basolateral amygdala neurons projecting to the nucleus accumbens core increases cue-induced approach to the location of reward, without influencing the pursuit of reward cues. Thus, these amygdala-to-accumbens neurons promote cue-induced expectation of reward, without changing the attractiveness of cues.