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      Nucleus Accumbens Shell Dopamine Preferentially Tracks Information Related to Outcome Value of Reward

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          Abstract

          Effective decision-making requires organisms to predict reward values and bias behavior toward the best available option. The mesolimbic dopamine system, including the nucleus accumbens (NAc) shell and core, is involved in this process. Although studies support a role of the shell and core in specific aspects of decision-making (e.g., risk, effort, delay), no studies have directly compared dopamine release dynamics in these subregions to cues exclusively signaling the availability of different reward magnitudes. Here, fast-scan cyclic voltammetry was used to compare rapid dopamine release dynamics in the NAc subregions during a magnitude-based decision-making task. Rats learned that distinct cues signaled the availability of either a small or large reward (one or two sugar pellets), and then were given an opportunity to choose their preferred option. We found that peak dopamine release tracked the more preferred (higher-magnitude) option in both core and shell subregions. Critically, however, overall (i.e., global) dopamine release was significantly higher and longer lasting in the shell and tracked the preferred magnitude during the entire cue period. Further, in the shell (not core), dopamine signaling significantly declined immediately at the lever press for reward but increased during the period of reward consumption. Collectively, the results indicate that although dopamine release in both the core and shell are activated by cues signaling the opportunity to respond for rewards of different magnitudes, dopamine release in the shell plays a differential and unique role in tracking information related to the outcome value of reward.

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          Most cited references52

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          Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex.

          Anatomical and functional refinements of the meso-limbic dopamine system of the rat are discussed. Present experiments suggest that dopaminergic neurons localized in the posteromedial ventral tegmental area (VTA) and central linear nucleus raphe selectively project to the ventromedial striatum (medial olfactory tubercle and medial nucleus accumbens shell), whereas the anteromedial VTA has few if any projections to the ventral striatum, and the lateral VTA largely projects to the ventrolateral striatum (accumbens core, lateral shell and lateral tubercle). These findings complement the recent behavioral findings that cocaine and amphetamine are more rewarding when administered into the ventromedial striatum than into the ventrolateral striatum. Drugs such as nicotine and opiates are more rewarding when administered into the posterior VTA or the central linear nucleus than into the anterior VTA. A review of the literature suggests that (1) the midbrain has corresponding zones for the accumbens core and medial shell; (2) the striatal portion of the olfactory tubercle is a ventral extension of the nucleus accumbens shell; and (3) a model of two dopamine projection systems from the ventral midbrain to the ventral striatum is useful for understanding reward function. The medial projection system is important in the regulation of arousal characterized by affect and drive and plays a different role in goal-directed learning than the lateral projection system, as described in the variation-selection hypothesis of striatal functional organization.
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            Subsecond dopamine release promotes cocaine seeking.

            The dopamine-containing projection from the ventral tegmental area of the midbrain to the nucleus accumbens is critically involved in mediating the reinforcing properties of cocaine. Although neurons in this area respond to rewards on a subsecond timescale, neurochemical studies have only addressed the role of dopamine in drug addiction by examining changes in the tonic (minute-to-minute) levels of extracellular dopamine. To investigate the role of phasic (subsecond) dopamine signalling, we measured dopamine every 100 ms in the nucleus accumbens using electrochemical technology. Rapid changes in extracellular dopamine concentration were observed at key aspects of drug-taking behaviour in rats. Before lever presses for cocaine, there was an increase in dopamine that coincided with the initiation of drug-seeking behaviours. Notably, these behaviours could be reproduced by electrically evoking dopamine release on this timescale. After lever presses, there were further increases in dopamine concentration at the concurrent presentation of cocaine-related cues. These cues alone also elicited similar, rapid dopamine signalling, but only in animals where they had previously been paired to cocaine delivery. These findings reveal an unprecedented role for dopamine in the regulation of drug taking in real time.
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              Dopamine neurons and their role in reward mechanisms.

              Information related to rewards is processed by a limited number of brain structures. Recent studies have demonstrated that dopamine neurons respond to appetitive events, such as primary rewards and reward-predicting stimuli. Rather than responding unconditionally, these neurons signal deviations from the prediction of future appetitive events. These reward-related responses correspond formally to concepts of behavioral and computational learning theories and may thus constitute teaching signals for appetitive learning.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                26 May 2017
                7 June 2017
                May-Jun 2017
                : 4
                : 3
                : ENEURO.0058-17.2017
                Affiliations
                [1 ]Department of Psychology and Neuroscience, University of North Carolina , Chapel Hill, NC 27599
                [2 ]Department of Psychology and Neuroscience, University of Colorado Boulder , Boulder, CO 80309
                Author notes

                Authors report no conflict of interest.

                Author contributions: DAS performed research; DAS, MPS, and RMC wrote the paper.

                This work was supported by DA034021 (RMC), T32 DA007244 (DAS), and F31 DA042721-01 (DAS).

                Correspondence should be addressed to Regina M. Carelli, PhD, University of North Carolina, CB#3270 Davie Hall, Chapel Hill, NC 27599. E-mail: rcarelli@ 123456unc.edu .
                Author information
                http://orcid.org/0000-0001-8754-4665
                http://orcid.org/0000-0002-0491-880X
                Article
                eN-NWR-0058-17
                10.1523/ENEURO.0058-17.2017
                5461554
                c3bc96fd-12d8-43aa-a3aa-16856166fd3d
                Copyright © 2017 Sackett et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 22 February 2017
                : 6 April 2017
                : 5 May 2017
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 61, Pages: 10, Words: 7886
                Funding
                Funded by: National Institute of Drug Abuse
                Award ID: DA034021
                Funded by: National Instute of Drug Abuse
                Award ID: T32 DA007244
                Funded by: National Institute of Drug Abuse
                Award ID: F31 DA042721
                Categories
                1
                1.1
                New Research
                Cognition and Behavior
                Custom metadata
                May/June 2017

                accumbens,behavior,decision making,dopamine,electrochemistry,reward

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