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      Reward from bugs to bipeds: a comparative approach to understanding how reward circuits function

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          Abstract

          In a complex environment, animals learn from their responses to stimuli and events. Appropriate response to reward and punishment can promote survival, reproduction and increase evolutionary fitness. Interestingly, the neural processes underlying these responses are remarkably similar across phyla. In all species, dopamine is central to encoding reward and directing motivated behaviors, however, a comprehensive understanding of how circuits encode reward and direct motivated behaviors is still lacking. In part, this is a result of the sheer diversity of neurons, the heterogeneity of their responses and the complexity of neural circuits within which they are found. We argue that general features of reward circuitry are common across model organisms, and thus principles learned from invertebrate model organisms can inform research across species. In particular, we discuss circuit motifs that appear to be functionally equivalent from flies to primates. We argue that a comparative approach to studying and understanding reward circuit function provides a more comprehensive understanding of reward circuitry, and informs disorders that affect the brain’s reward circuitry.

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          Most cited references125

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          Distinct roles for direct and indirect pathway striatal neurons in reinforcement

          Dopamine signaling is implicated in reinforcement learning, but the neural substrates targeted by dopamine are poorly understood. Here, we bypassed dopamine signaling itself and tested how optogenetic activation of dopamine D1- or D2-receptor-expressing striatal projection neurons influenced reinforcement learning in mice. Stimulating D1-expressing neurons induced persistent reinforcement, whereas stimulating D2-expressing neurons induced transient punishment, demonstrating that activation of these circuits is sufficient to modify the probability of performing future actions.
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            Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli.

            Midbrain dopamine (DA) neurons are not homogeneous but differ in their molecular properties and responses to external stimuli. We examined whether the modulation of excitatory synapses on DA neurons by rewarding or aversive stimuli depends on the brain area to which these DA neurons project. We identified DA neuron subpopulations in slices after injection of "Retrobeads" into single target areas of adult mice and found differences in basal synaptic properties. Administration of cocaine selectively modified excitatory synapses on DA cells projecting to nucleus accumbens (NAc) medial shell while an aversive stimulus selectively modified synapses on DA cells projecting to medial prefrontal cortex. In contrast, synapses on DA neurons projecting to NAc lateral shell were modified by both rewarding and aversive stimuli, which presumably reflects saliency. These results suggest that the mesocorticolimbic DA system may be comprised of three anatomically distinct circuits, each modified by distinct aspects of motivationally relevant stimuli. Copyright © 2011 Elsevier Inc. All rights reserved.
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              Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior.

              In the basal ganglia, convergent input and dopaminergic modulation of the direct striatonigral and the indirect striatopallidal pathways are critical in rewarding and aversive learning and drug addiction. To explore how the basal ganglia information is processed and integrated through these two pathways, we developed a reversible neurotransmission blocking technique, in which transmission of each pathway was selectively blocked by specific expression of transmission-blocking tetanus toxin in a doxycycline-dependent manner. The results indicated that the coordinated modulation of these two pathways was necessary for dopamine-mediated acute psychostimulant actions. This modulation, however, shifted to the predominant roles of the direct pathway in reward learning and cocaine sensitization and the indirect pathway in aversive behavior. These two pathways thus have distinct roles: the direct pathway critical for distinguishing associative rewarding stimuli from nonassociative ones and the indirect pathway for rapid memory formation to avoid aversive stimuli.
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                Author and article information

                Journal
                J Neurogenet
                J. Neurogenet
                INEG
                ineg20
                Journal of Neurogenetics
                Taylor & Francis
                0167-7063
                1563-5260
                2 April 2016
                22 June 2016
                : 30
                : 2 , Neurogenetics of Connectomes: From Fly to Fish
                : 133-148
                Affiliations
                [ a ]Department of Neuroscience, Brown University , Providence, RI, USA
                Author notes
                CONTACT Karla R. Kaun karla_kaun@ 123456brown.edu Department of Neuroscience, Brown University , 185 Meeting Street, Providence, RI 02912, USA
                Article
                1180385
                10.1080/01677063.2016.1180385
                4926782
                27328845
                4639f6bf-4168-4442-8401-bf816a0fca5a
                © 2016 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.

                History
                : 3 February 2016
                : 13 April 2016
                : 15 April 2016
                Page count
                Pages: 16
                Funding
                Funded by: Brown Institute of Brain Science, Center for Nervous System Function, Center of Biomedical Research Excellence (NIGMS)
                Award ID: 5P20GM103645-03
                Funded by: Rhode Island Foundation Medical Research Award
                Award ID: 20144133
                Categories
                Review
                Review Article

                Genetics
                behavior,dopamine,functional conservation,neuromodulators,neuropeptides,neurotransmitters
                Genetics
                behavior, dopamine, functional conservation, neuromodulators, neuropeptides, neurotransmitters

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