Abstract

During Pavlovian conditioning, a conditioned stimulus (CS) may act as a predictor of a reward to be delivered in another location. Individuals vary widely in their propensity to engage with the CS (sign tracking) or with the site of eventual reward (goal tracking). It is often assumed that sign tracking involves the association of the CS with the motivational value of the reward, resulting in the CS acquiring incentive value independent of the outcome. However, experimental evidence for this assumption is lacking. In order to test the hypothesis that sign tracking behavior does not rely on a neural representation of the outcome, we employed a reward devaluation procedure. We trained rats on a classic Pavlovian paradigm in which a lever CS was paired with a sucrose reward, then devalued the reward by pairing sucrose with illness in the absence of the CS. We found that sign tracking behavior was enhanced, rather than diminished, following reward devaluation; thus, sign tracking is clearly independent of a representation of the outcome. In contrast, goal tracking behavior was decreased by reward devaluation. Furthermore, when we divided rats into those with high propensity to engage with the lever (sign trackers) and low propensity to engage with the lever (goal trackers), we found that nearly all of the effects of devaluation could be attributed to the goal trackers. These results show that sign tracking and goal tracking behavior may be the output of different associative structures in the brain, providing insight into the mechanisms by which reward-associated stimuli—such as drug cues—come to exert control over behavior in some individuals.

Highlights

  • Sign tracking describes the propensity of individuals to engage with a conditioned stimulus (CS) that has been paired with a rewarding unconditioned stimulus (US), even when the location of the eventual reward is not colocalized with the CS (Hearst and Jenkins, 1974; Flagel et al, 2009)

  • Sign trackers develop elevated levels of dopamine in the nucleus accumbens (NAc; Tomie et al, 2000), and sign tracking is profoundly sensitive to dopamine receptor antagonism within the NAc (Saunders and Robinson, 2012). These results suggest that sign tracking is the result of activity in the mesolimbic dopamine system, perhaps because dopamine serves to assign incentive salience to reward-associated objects (Berridge and Robinson, 1998; Berridge, 2004); in contrast, goal-tracking appears to be independent of mesolimbic dopamine

  • We trained 48 rats on a standard Pavlovian procedure in which the CS terminated with delivery of a liquid sucrose reward in a receptacle that was spatially distinct from the CS

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Summary

INTRODUCTION

Sign tracking describes the propensity of individuals to engage with a conditioned stimulus (CS) that has been paired with a rewarding unconditioned stimulus (US), even when the location of the eventual reward is not colocalized with the CS (Hearst and Jenkins, 1974; Flagel et al, 2009). Only in sign trackers, as opposed to goal trackers, will a reward-associated CS become an effective secondary reinforcer, such that rats will work to receive the CS even without the original rewarding outcome (Robinson and Flagel, 2009) These observations are thought to indicate that sign trackers have a higher propensity to transfer incentive salience to a CS. Sign trackers (but not goal trackers) develop elevated levels of dopamine in the nucleus accumbens (NAc; Tomie et al, 2000), and sign tracking (but not goal tracking) is profoundly sensitive to dopamine receptor antagonism within the NAc (Saunders and Robinson, 2012) Together, these results suggest that sign tracking is the result of activity in the mesolimbic dopamine system, perhaps because dopamine serves to assign incentive salience to reward-associated objects (Berridge and Robinson, 1998; Berridge, 2004); in contrast, goal-tracking appears to be independent of mesolimbic dopamine. We provide direct evidence that sign tracking behavior, as it is commonly studied, is resistant to changes in the value of the outcome, whereas goal tracking behavior—at least in rats that preferentially goal-track—is profoundly sensitive to the value of the outcome

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