Research report
Individual variation in the propensity to attribute incentive salience to an appetitive cue predicts the propensity to attribute motivational salience to an aversive cue

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Abstract

It has been proposed that animals that attribute high levels of incentive salience to reward-related cues may be especially vulnerable to addiction. Individual variation has also been observed in the motivational value attributed to aversive cues, which may confer vulnerability to anxiety disorders such as post-traumatic stress disorder (PTSD). There may be a core behavioral trait that contributes to individual variation in the motivational value assigned to predictive cues regardless of emotional valence. To test this hypothesis, we used a Pavlovian conditioned approach procedure to classify rats based on whether they learned to approach and interact with a cue predicting food reward (sign-trackers) or learned upon cue presentation to go to the location of impending food delivery (goal-trackers), and then examined Pavlovian fear conditioning in the same animals. It has recently been proposed that sign-trackers are more vulnerable to substance abuse because they attribute greater incentive motivational value to drug cues. Here we show that sign-trackers also have a tendency to be more fearful of discrete cues that predict footshock. In addition, we found that goal-trackers exhibited greater contextual fear when placed back into the original fear-conditioning context in the absence of temporally discrete cues. These results suggest that there may be a subset of individuals who tend to attribute high levels of motivational salience to predictive cues regardless of emotional valence, which may predispose them to a number of psychiatric comorbidities including PTSD and substance abuse. Other individuals use contexts to appropriately modify their reactions to such salient stimuli.

Introduction

Cues in the environment that have been associated with emotionally salient events often themselves come to trigger complex emotional and motivational states that can powerfully influence behavior. For example, eating behavior can be triggered in humans and other animals by exposure to cues associated with food (e.g., the sight of a fast-food restaurant), even when the subject is sated [1], [2], [3]. This basic psychological process can have undesirable consequences, for example, spurring excessive eating that can contribute to obesity. Similarly, in addicts, drug-associated cues can induce craving, which often leads to continued drug use or relapse [4], [5]. In other circumstances, relatively innocuous cues that were associated with a previous trauma can induce extreme fear and avoidance behaviors, e.g., a fireworks display inducing panic in a war veteran [6].

Preclinical studies have shown, however, that there is considerable individual variation in the degree to which animals attribute incentive motivational properties (“incentive salience”) to reward cues. For example, when a food reward is paired with a localizable cue the cue itself becomes attractive, eliciting approach towards it, only in some rats (“sign-trackers,” STs); other rats direct their behavior away from the cue towards to location of reward delivery (“goal-trackers,” GTs) [7], [8], [9]. Furthermore, a food cue is more “desired” in STs than GTs, in that they will work harder to get it [10]. Drug cues also acquire greater control over behavior in STs than GTs. For example, STs are more susceptible to cue-induced reinstatement of cocaine self-administration behavior, suggesting they may be more vulnerable to develop addiction-like behaviors than GTs [11]. Thus, the extent to which individuals attribute predictive reward cues with incentive motivational properties may confer vulnerability to disorders of impulse control.

There is also considerable individual variation in the extent to which cues associated with aversive stimuli acquire control over behavior [12], and this trait may contribute to vulnerability to anxiety disorders [13], [14]. For example, variation in the magnitude of conditioned fear responses in animals has been proposed as a model of vulnerability to post-traumatic stress disorder (PTSD) [12], [15]. Indeed, pathological hyper-reactivity to environmental cues is a central feature common to several psychiatric disorders. In the case of substance abuse, “cue reactivity” is well-documented and includes psychological cravings, physiological responses, and engagement in actual drug use behaviors in response to drug-related cues or contexts [16], [17]. Similarly, PTSD is defined in part by excessive emotional, physiological, and behavioral responses to trauma-related stimuli [18], [19]. From this perspective, one difference between substance abuse and PTSD is the emotional valence of the triggering stimulus, one being “positive” and eliciting approach, the other being “negative” and eliciting avoidance. It is possible that some individuals are prone to attribute excessive emotional and/or motivational significance to environmental cues regardless of valence, which could therefore make them more vulnerable to a number of different psychiatric disorders. We explore this idea here using preclinical animal models to estimate the emotional and/or motivational significance individual rats attribute to both an attractive food cue and to a fearful aversive cue.

Section snippets

Materials and methods

All procedures were approved by the University Committee on the Use and Care of Animals.

Exp. 1: Pavlovian conditioned approach

As described previously, rats varied in the topography of the conditioned response (CR) they acquired [7], [10]. Upon presentation of the lever-CS some rats (“sign-trackers”, STs) came to approach and contact the lever, whereas others came to approach and engage the food cup (“goal-trackers”, GTs), even though neither of these responses was necessary for receipt of the food reward. Based on an Approach Index that takes into account the probability and latency of each response type, 10 rats were

Discussion

We found that rats prone to attribute incentive salience to a reward (food) cue, as assessed by their tendency to approach it (i.e., STs), also tended to attribute greater emotional and/or motivational significance to a fear-provoking aversive cue, assessed by either conditioned freezing behavior or conditioned suppression of ongoing instrumental behavior. Variation in one trait accounted for between 11 and 16% of the variance in the other, depending on the measure of conditioned fear. In

Acknowledgements

We wish to thank Allison Gates for her technical assistance with the conditioned suppression experiment. This research was supported by NIH grants R37DA04294 to TER and grant R01MH065961 to SM.

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