Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence

Beckmann, Joshua S.; Chow, Jonathan J.

doi:10.1101/lm.037382.114

Cited by 66 publications

(81 citation statements)

References 57 publications

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“…For example, a sign-tracking individual may enter a "focal search mode," preparing the animal to handle food by promoting behaviors such as biting or gnawing (Timberlake 1994;Beckmann and Chow 2015). These CRs are routinely observed during sign-tracking interaction with the lever-CS.…”

Section: Discussionmentioning

confidence: 99%

“…A lever-CS is a complex multimodal cue as its presentation involves movement and generates visual (the lever itself and its illumination), auditory (the sound when extended and retracted, as well as when pressed), and tactile sensory components. This may be important because a number of studies have suggested that auditory stimuli (tones) are attributed with less incentive salience than a lever-CS (Meyer et al 2014;Beckmann and Chow 2015), even though rats can localize auditory stimuli (Harrison 1979;Cleland and Davey 1983). Thus, if an animal attended primarily to its auditory qualities, a lever-CS may generate a GT CR because of its predictive value, but the auditory component alone may not be sufficient to confer much incentive value to the lever-CS, reducing its potential to act as a potent incentive stimulus.…”

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confidence: 99%

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The sensory features of a food cue influence its ability to act as an incentive stimulus and evoke dopamine release in the nucleus accumbens core

et al. 2016

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The sensory properties of a reward-paired cue (a conditioned stimulus; CS) may impact the motivational value attributed to the cue, and in turn influence the form of the conditioned response (CR) that develops. A cue with multiple sensory qualities, such as a moving lever-CS, may activate numerous neural pathways that process auditory and visual information, resulting in CRs that vary both within and between individuals. For example, CRs include approach to the lever-CS itself (rats that "sign-track"; ST), approach to the location of reward delivery (rats that "goal-track"; GT), or an "intermediate" combination of these behaviors. We found that the multimodal sensory features of the lever-CS were important to the development and expression of sign-tracking. When the lever-CS was covered, and thus could only be heard moving, STs not only continued to approach the lever location but also started to approach the food cup during the CS period. While still predictive of reward, the auditory component of the lever-CS was a much weaker conditioned reinforcer than the visible lever-CS. This plasticity in behavioral responding observed in STs closely resembled behaviors normally seen in rats classified as "intermediates." Furthermore, the ability of both the lever-CS and the reward-delivery to evoke dopamine release in the nucleus accumbens was also altered by covering the lever-dopamine signaling in STs resembled neurotransmission observed in rats that normally only GT. These data suggest that while the visible lever-CS was attractive, wanted, and had incentive value for STs, when presented in isolation, the auditory component of the cue was simply predictive of reward, lacking incentive salience. Therefore, the specific sensory features of cues may differentially contribute to responding and ensure behavioral flexibility.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

The sensory features of a food cue influence its ability to act as an incentive stimulus and evoke dopamine release in the nucleus accumbens core

et al. 2016

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“…In addition, the CS modality can affect the acquisition of sign-tracking behavior. In example, rats do not readily sign-track to nose-poke ports or auditory tones 19,20 . Even when using a retractable lever as the CS, care should be taken not to overtrain rats.…”

Section: Discussionmentioning

confidence: 99%

Pavlovian Conditioned Approach Training in Rats

Fitzpatrick

Morrow

2016

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Short Abstract Here, we present a protocol to elicit Pavlovian conditioned approach behavior in rats. This procedure can be used to measure individual differences in the tendency to approach and attribute incentive salience to reward-related cues and investigate addiction vulnerability. Long Abstract Cues that are contingently paired with unconditioned, rewarding stimuli can acquire rewarding properties themselves through a process known as the attribution of incentive salience, or the transformation of neutral stimuli into attractive, “wanted’ stimuli capable of motivating behavior. Pavlovian conditioned approach (PCA) develops after the response-independent presentation of a conditioned stimulus (CS; e.g., a lever) that predicts the delivery of an unconditioned stimulus (US; e.g., a food pellet) and can be used to measure incentive salience. During training, three patterns of conditioned responses (CRs) can develop: sign-tracking behavior (CS-directed CR), goal-tracking behavior (US-directed CR), and an intermediate response (both CRs). Sign-trackers attribute incentive salience to reward-related cues and are more vulnerable to cue-induced reinstatement of drug-seeking as well as other addiction-related behaviors, making PCA a potentially valuable procedure for studying addiction vulnerability. Here, we describe materials and methods used to elicit PCA behavior from rats as well as analyze and interpret PCA behavior in individual experiments.

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“…According to the reward-prediction error hypothesis, since both sign- and goal-tracking are learned CRs, the lever should serve as an equally effective CS for all individuals, despite the difference in the type of CR that is elicited. Despite being equally effective CSs, a food-associated lever acts as a more robust conditioned reinforcer in individuals that have a propensity to sign-track to the lever CS versus those that goal-track in response to it (Robinson and Flagel, 2009; Meyer et al 2014); furthermore, stimuli that elicit sign-tracking behavior also serve as more robust conditioned reinforcers relative to stimuli that elicit goal-tracking behavior within individuals (Meyer et al 2014; Beckmann and Chow 2015). Collectively, the results suggest that while both sign- and goal-tracking responses are indicative of a learned CS-US relationship, sign-tracking responses are also reflective of the attribution of incentive value.…”

Section: Introductionmentioning

confidence: 99%

“…To better dissociate the acquisition of incentive value attribution from reward-prediction error learning, we utilized a 2-CS PCA procedure, where two different but equally-predictive and equally learned conditioned-stimuli (lever and tone) are used to preferentially elicit sign- and goal-tracking within an animal (Beckmann and Chow, 2015). Using a 2-CS PCA procedure, it has been demonstrated that a lever CS associated with sign-tracking engages an incentive value attribution process and a tone CS associated with goal-tracking engages a more general prediction error learning process within individuals (Beckmann and Chow, 2015).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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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.

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Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence

Cited by 66 publications

References 57 publications

The sensory features of a food cue influence its ability to act as an incentive stimulus and evoke dopamine release in the nucleus accumbens core

The sensory features of a food cue influence its ability to act as an incentive stimulus and evoke dopamine release in the nucleus accumbens core

Pavlovian Conditioned Approach Training in Rats

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

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