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      A Neural Computational Model of Incentive Salience

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Incentive salience is a motivational property with ‘magnet-like’ qualities. When attributed to reward-predicting stimuli (cues), incentive salience triggers a pulse of ‘wanting’ and an individual is pulled toward the cues and reward. A key computational question is how incentive salience is generated during a cue re-encounter, which combines both learning and the state of limbic brain mechanisms. Learning processes, such as temporal-difference models, provide one way for stimuli to acquire cached predictive values of rewards. However, empirical data show that subsequent incentive values are also modulated on the fly by dynamic fluctuation in physiological states, altering cached values in ways requiring additional motivation mechanisms. Dynamic modulation of incentive salience for a Pavlovian conditioned stimulus (CS or cue) occurs during certain states, without necessarily requiring (re)learning about the cue. In some cases, dynamic modulation of cue value occurs during states that are quite novel, never having been experienced before, and even prior to experience of the associated unconditioned reward in the new state. Such cases can include novel drug-induced mesolimbic activation and addictive incentive-sensitization, as well as natural appetite states such as salt appetite. Dynamic enhancement specifically raises the incentive salience of an appropriate CS, without necessarily changing that of other CSs. Here we suggest a new computational model that modulates incentive salience by integrating changing physiological states with prior learning. We support the model with behavioral and neurobiological data from empirical tests that demonstrate dynamic elevations in cue-triggered motivation (involving natural salt appetite, and drug-induced intoxication and sensitization). Our data call for a dynamic model of incentive salience, such as presented here. Computational models can adequately capture fluctuations in cue-triggered ‘wanting’ only by incorporating modulation of previously learned values by natural appetite and addiction-related states.

          Author Summary

          Reward cues are potent triggers of desires, ranging from normal appetites to compulsive addictions. Food cues may trigger a sudden desire to eat before lunch, and drug cues may trigger even a ‘recovered addict’ to relapse again into drug taking. But learned cues are not constant in their motivating power. Food cues are more potent when you are hungry, and drug cues may become overwhelmingly potent to an addict who tries to take ‘just one’ drink or hit, precipitating an escalating binge of further relapse. These changes in cue-triggered desire produced by a change in biological state present a challenge to many current computational models of motivation. Such modulation can even be unlearned (though the modulation interacts with cues acquired through learning), in that the modulation instantly follows a physiological or neurobiological change (hunger, drug hit, etc.), altering the cue's ability to trigger desire for a relevant reward. Here we demonstrate concrete examples of instant modulation and propose how to build computational models of cue-triggered ‘wanting’ to better capture the dynamic interaction between learning and physiology that controls the incentive salience mechanism of motivation for rewards.

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          Most cited references48

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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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            Separate neural systems value immediate and delayed monetary rewards.

            When humans are offered the choice between rewards available at different points in time, the relative values of the options are discounted according to their expected delays until delivery. Using functional magnetic resonance imaging, we examined the neural correlates of time discounting while subjects made a series of choices between monetary reward options that varied by delay to delivery. We demonstrate that two separate systems are involved in such decisions. Parts of the limbic system associated with the midbrain dopamine system, including paralimbic cortex, are preferentially activated by decisions involving immediately available rewards. In contrast, regions of the lateral prefrontal cortex and posterior parietal cortex are engaged uniformly by intertemporal choices irrespective of delay. Furthermore, the relative engagement of the two systems is directly associated with subjects' choices, with greater relative fronto-parietal activity when subjects choose longer term options.
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              The debate over dopamine's role in reward: the case for incentive salience.

              Debate continues over the precise causal contribution made by mesolimbic dopamine systems to reward. There are three competing explanatory categories: 'liking', learning, and 'wanting'. Does dopamine mostly mediate the hedonic impact of reward ('liking')? Does it instead mediate learned predictions of future reward, prediction error teaching signals and stamp in associative links (learning)? Or does dopamine motivate the pursuit of rewards by attributing incentive salience to reward-related stimuli ('wanting')? Each hypothesis is evaluated here, and it is suggested that the incentive salience or 'wanting' hypothesis of dopamine function may be consistent with more evidence than either learning or 'liking'. In brief, recent evidence indicates that dopamine is neither necessary nor sufficient to mediate changes in hedonic 'liking' for sensory pleasures. Other recent evidence indicates that dopamine is not needed for new learning, and not sufficient to directly mediate learning by causing teaching or prediction signals. By contrast, growing evidence indicates that dopamine does contribute causally to incentive salience. Dopamine appears necessary for normal 'wanting', and dopamine activation can be sufficient to enhance cue-triggered incentive salience. Drugs of abuse that promote dopamine signals short circuit and sensitize dynamic mesolimbic mechanisms that evolved to attribute incentive salience to rewards. Such drugs interact with incentive salience integrations of Pavlovian associative information with physiological state signals. That interaction sets the stage to cause compulsive 'wanting' in addiction, but also provides opportunities for experiments to disentangle 'wanting', 'liking', and learning hypotheses. Results from studies that exploited those opportunities are described here. In short, dopamine's contribution appears to be chiefly to cause 'wanting' for hedonic rewards, more than 'liking' or learning for those rewards.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                July 2009
                July 2009
                17 July 2009
                : 5
                : 7
                : e1000437
                Affiliations
                [1 ]Department of Psychology, University of Michigan, Ann Arbor, Michigan, United States of America
                [2 ]McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
                University College London, United Kingdom
                Author notes

                Conceived and designed the experiments: JZ KCB AJT KSS JWA. Performed the experiments: AJT KSS. Analyzed the data: JZ AJT KSS JWA. Wrote the paper: JZ KCB JWA.

                Article
                08-PLCB-RA-0371R5
                10.1371/journal.pcbi.1000437
                2703828
                19609350
                21b613f0-5f20-42a8-a93b-2fb1e931b6b2
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 9 May 2008
                : 10 June 2009
                Page count
                Pages: 14
                Categories
                Research Article
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Cognitive Neuroscience
                Neuroscience/Neural Homeostasis
                Neuroscience/Theoretical Neuroscience
                Neuroscience/Psychology

                Quantitative & Systems biology
                Quantitative & Systems biology

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