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      Quantifying Individual Variation in the Propensity to Attribute Incentive Salience to Reward Cues

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          Abstract

          If reward-associated cues acquire the properties of incentive stimuli they can come to powerfully control behavior, and potentially promote maladaptive behavior. Pavlovian incentive stimuli are defined as stimuli that have three fundamental properties: they are attractive, they are themselves desired, and they can spur instrumental actions. We have found, however, that there is considerable individual variation in the extent to which animals attribute Pavlovian incentive motivational properties (“incentive salience”) to reward cues. The purpose of this paper was to develop criteria for identifying and classifying individuals based on their propensity to attribute incentive salience to reward cues. To do this, we conducted a meta-analysis of a large sample of rats (N = 1,878) subjected to a classic Pavlovian conditioning procedure. We then used the propensity of animals to approach a cue predictive of reward (one index of the extent to which the cue was attributed with incentive salience), to characterize two behavioral phenotypes in this population: animals that approached the cue (“sign-trackers”) vs. others that approached the location of reward delivery (“goal-trackers”). This variation in Pavlovian approach behavior predicted other behavioral indices of the propensity to attribute incentive salience to reward cues. Thus, the procedures reported here should be useful for making comparisons across studies and for assessing individual variation in incentive salience attribution in small samples of the population, or even for classifying single animals.

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          Most cited references 118

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          The neural basis of drug craving: an incentive-sensitization theory of addiction.

          This paper presents a biopsychological theory of drug addiction, the 'Incentive-Sensitization Theory'. The theory addresses three fundamental questions. The first is: why do addicts crave drugs? That is, what is the psychological and neurobiological basis of drug craving? The second is: why does drug craving persist even after long periods of abstinence? The third is whether 'wanting' drugs (drug craving) is attributable to 'liking' drugs (to the subjective pleasurable effects of drugs)? The theory posits the following. (1) Addictive drugs share the ability to enhance mesotelencephalic dopamine neurotransmission. (2) One psychological function of this neural system is to attribute 'incentive salience' to the perception and mental representation of events associated with activation of the system. Incentive salience is a psychological process that transforms the perception of stimuli, imbuing them with salience, making them attractive, 'wanted', incentive stimuli. (3) In some individuals the repeated use of addictive drugs produces incremental neuroadaptations in this neural system, rendering it increasingly and perhaps permanently, hypersensitive ('sensitized') to drugs and drug-associated stimuli. The sensitization of dopamine systems is gated by associative learning, which causes excessive incentive salience to be attributed to the act of drug taking and to stimuli associated with drug taking. It is specifically the sensitization of incentive salience, therefore, that transforms ordinary 'wanting' into excessive drug craving. (4) It is further proposed that sensitization of the neural systems responsible for incentive salience ('for wanting') can occur independently of changes in neural systems that mediate the subjective pleasurable effects of drugs (drug 'liking') and of neural systems that mediate withdrawal. Thus, sensitization of incentive salience can produce addictive behavior (compulsive drug seeking and drug taking) even if the expectation of drug pleasure or the aversive properties of withdrawal are diminished and even in the face of strong disincentives, including the loss of reputation, job, home and family. We review evidence for this view of addiction and discuss its implications for understanding the psychology and neurobiology of addiction.
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            Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex.

            Emotions are multifaceted, but a key aspect of emotion involves the assessment of the value of environmental stimuli. This article reviews the many psychological representations, including representations of stimulus value, which are formed in the brain during Pavlovian and instrumental conditioning tasks. These representations may be related directly to the functions of cortical and subcortical neural structures. The basolateral amygdala (BLA) appears to be required for a Pavlovian conditioned stimulus (CS) to gain access to the current value of the specific unconditioned stimulus (US) that it predicts, while the central nucleus of the amygdala acts as a controller of brainstem arousal and response systems, and subserves some forms of stimulus-response Pavlovian conditioning. The nucleus accumbens, which appears not to be required for knowledge of the contingency between instrumental actions and their outcomes, nevertheless influences instrumental behaviour strongly by allowing Pavlovian CSs to affect the level of instrumental responding (Pavlovian-instrumental transfer), and is required for the normal ability of animals to choose rewards that are delayed. The prelimbic cortex is required for the detection of instrumental action-outcome contingencies, while insular cortex may allow rats to retrieve the values of specific foods via their sensory properties. The orbitofrontal cortex, like the BLA, may represent aspects of reinforcer value that govern instrumental choice behaviour. Finally, the anterior cingulate cortex, implicated in human disorders of emotion and attention, may have multiple roles in responding to the emotional significance of stimuli and to errors in performance, preventing responding to inappropriate stimuli.
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              Value-driven attentional capture.

              Attention selects which aspects of sensory input are brought to awareness. To promote survival and well-being, attention prioritizes stimuli both voluntarily, according to context-specific goals (e.g., searching for car keys), and involuntarily, through attentional capture driven by physical salience (e.g., looking toward a sudden noise). Valuable stimuli strongly modulate voluntary attention allocation, but there is little evidence that high-value but contextually irrelevant stimuli capture attention as a consequence of reward learning. Here we show that visual search for a salient target is slowed by the presence of an inconspicuous, task-irrelevant item that was previously associated with monetary reward during a brief training session. Thus, arbitrary and otherwise neutral stimuli imbued with value via associative learning capture attention powerfully and persistently during extinction, independently of goals and salience. Vulnerability to such value-driven attentional capture covaries across individuals with working memory capacity and trait impulsivity. This unique form of attentional capture may provide a useful model for investigating failures of cognitive control in clinical syndromes in which value assigned to stimuli conflicts with behavioral goals (e.g., addiction, obesity).
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                22 June 2012
                : 7
                : 6
                Affiliations
                [1 ]Department of Psychology, University of Michigan, Ann Arbor, Michigan, United States of America
                [2 ]Department of Psychiatry, University of Michigan, Ann Arbor, Michigan, United States of America
                University of Chicago, United States of America
                Author notes

                Conceived and designed the experiments: PJM VL BTS LMY SBF JDM TER. Performed the experiments: PJM VL BTS LMY SBF JDM. Analyzed the data: PJM VL BTS LMY. Wrote the paper: PJM TER. Commented on and edited the manuscript: PJM VL BTS LMY SBF JDM TER.

                Article
                PONE-D-12-08976
                10.1371/journal.pone.0038987
                3382216
                22761718
                Meyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Neuroscience
                Cognitive Neuroscience
                Cognition
                Decision Making
                Motor Reactions
                Animal Cognition
                Behavioral Neuroscience
                Learning and Memory
                Social and Behavioral Sciences
                Psychology
                Behavior
                Attention (Behavior)
                Emotions

                Uncategorized

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