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      Sign Tracking, but Not Goal Tracking, is Resistant to Outcome Devaluation

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          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.

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          A selective role for dopamine in reward learning

          Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, whereby they themselves become attractive and desirable incentive stimuli. But individuals differ in whether a cue acts solely as a predictor that evokes a conditional response, or also serves as an incentive stimulus, and this determines the degree to which a cue might bias choice or even promote maladaptive behavior. Here we use rats that differ in the incentive motivational properties they attribute to food cues to probe the role of the neurotransmitter dopamine in stimulus-reward learning. We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors. Rather, dopamine acts selectively in a form of reward learning in which “incentive salience” is assigned to reward cues. In individuals with a propensity for this form of learning, reward cues come to powerfully motivate and control behavior. This work provides insight into the neurobiology of a form of reward learning that confers increased susceptibility to disorders of impulse control.
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            Motivation concepts in behavioral neuroscience.

            Concepts of motivation are vital to progress in behavioral neuroscience. Motivational concepts help us to understand what limbic brain systems are chiefly evolved to do, i.e., to mediate psychological processes that guide real behavior. This article evaluates some major motivation concepts that have historic importance or have influenced the interpretation of behavioral neuroscience research. These concepts include homeostasis, setpoints and settling points, intervening variables, hydraulic drives, drive reduction, appetitive and consummatory behavior, opponent processes, hedonic reactions, incentive motivation, drive centers, dedicated drive neurons (and drive neuropeptides and receptors), neural hierarchies, and new concepts from affective neuroscience such as allostasis, cognitive incentives, and reward 'liking' versus 'wanting'. Copyright 2004 Elsevier Inc.
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              Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction.

              Drugs of abuse acquire different degrees of control over thoughts and actions based not only on the effects of drugs themselves, but also on predispositions of the individual. Those individuals who become addicted are unable to shift their thoughts and actions away from drugs and drug-associated stimuli. Thus in addicts, exposure to places or things (cues) that has been previously associated with drug-taking often instigates renewed drug-taking. We and others have postulated that drug-associated cues acquire the ability to maintain and instigate drug-taking behavior in part because they acquire incentive motivational properties through Pavlovian (stimulus-stimulus) learning. In the case of compulsive behavioral disorders, including addiction, such cues may be attributed with pathological incentive value ("incentive salience"). For this reason, we have recently begun to explore individual differences in the tendency to attribute incentive salience to cues that predict rewards. When discrete cues are associated with the non-contingent delivery of food or drug rewards some animals come to quickly approach and engage the cue even if it is located at a distance from where the reward will be delivered. In these animals the reward-predictive cue itself becomes attractive, eliciting approach towards it, presumably because it is attributed with incentive salience. Animals that develop this type of conditional response are called "sign-trackers". Other animals, "goal-trackers", do not approach the reward-predictive cue, but upon cue presentation they immediately go to the location where food will be delivered (the "goal"). For goal-trackers the reward-predictive cue is not attractive, presumably because it is not attributed with incentive salience. We review here preliminary data suggesting that these individual differences in the tendency to attribute incentive salience to cues predictive of reward may confer vulnerability or resistance to compulsive behavioral disorders, including addiction. It will be important, therefore, to study how environmental, neurobiological and genetic interactions determine the extent to which individuals attribute incentive value to reward-predictive stimuli.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                16 December 2015
                2015
                : 9
                : 468
                Affiliations
                [1] 1Department of Psychiatry and Behavioral Science, Albert Einstein College of Medicine Bronx, NY, USA
                [2] 2Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine Bronx, NY, USA
                Author notes

                Edited by: Mark Walton, University of Oxford, UK

                Reviewed by: Etienne Coutureau, Centre National de la Recherche Scientifique/Université de Bordeaux, France; Benjamin Thomas Saunders, Johns Hopkins University, USA

                *Correspondence: Saleem M. Nicola saleem.nicola@ 123456einstein.yu.edu

                This article was submitted to Decision Neuroscience, a section of the journal Frontiers in Neuroscience

                †Present Address: Sara E. Morrison, Department of Neuroscience, University of Pittsburgh, Pittsburgh, PA, USA

                Article
                10.3389/fnins.2015.00468
                4679928
                26733783
                36bd5d69-d86e-4ab8-b36d-1699ad3bd0ef
                Copyright © 2015 Morrison, Bamkole and Nicola.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 21 September 2015
                : 24 November 2015
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 46, Pages: 12, Words: 9617
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: DA019473
                Award ID: DA038412
                Award ID: MH092757
                Award ID: DA034465
                Funded by: NARSAD 10.13039/100000874
                Funded by: Klarman Family Foundation 10.13039/100005310
                Funded by: Charles H. Revson Foundation 10.13039/100001312
                Categories
                Neuroscience
                Original Research

                Neurosciences
                sign tracking,goal tracking,devaluation,pavlovian conditioning,reward,rats
                Neurosciences
                sign tracking, goal tracking, devaluation, pavlovian conditioning, reward, rats

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