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      Cannabinoid Modulation of Dopamine Release During Motivation, Periodic Reinforcement, Exploratory Behavior, Habit Formation, and Attention

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          Abstract

          Motivational and attentional processes energize action sequences to facilitate evolutionary competition and promote behavioral fitness. Decades of neuropharmacology, electrophysiology and electrochemistry research indicate that the mesocorticolimbic DA pathway modulates both motivation and attention. More recently, it was realized that mesocorticolimbic DA function is tightly regulated by the brain’s endocannabinoid system and greatly influenced by exogenous cannabinoids—which have been harnessed by humanity for medicinal, ritualistic, and recreational uses for 12,000 years. Exogenous cannabinoids, like the primary psychoactive component of cannabis, delta-9-tetrahydrocannabinol, produce their effects by acting at binding sites for naturally occurring endocannabinoids. The brain’s endocannabinoid system consists of two G-protein coupled receptors, endogenous lipid ligands for these receptor targets, and several synthetic and metabolic enzymes involved in their production and degradation. Emerging evidence indicates that the endocannabinoid 2-arachidonoylglycerol is necessary to observe concurrent increases in DA release and motivated behavior. And the historical pharmacology literature indicates a role for cannabinoid signaling in both motivational and attentional processes. While both types of behaviors have been scrutinized under manipulation by either DA or cannabinoid agents, there is considerably less insight into prospective interactions between these two important signaling systems. This review attempts to summate the relevance of cannabinoid modulation of DA release during operant tasks designed to investigate either motivational or attentional control of behavior. We first describe how cannabinoids influence DA release and goal-directed action under a variety of reinforcement contingencies. Then we consider the role that endocannabinoids might play in switching an animal’s motivation from a goal-directed action to the search for an alternative outcome, in addition to the formation of long-term habits. Finally, dissociable features of attentional behavior using both the 5-choice serial reaction time task and the attentional set-shifting task are discussed along with their distinct influences by DA and cannabinoids. We end with discussing potential targets for further research regarding DA-cannabinoid interactions within key substrates involved in motivation and attention.

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          Most cited references353

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          The attention system of the human brain.

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            An integrative theory of prefrontal cortex function.

            The prefrontal cortex has long been suspected to play an important role in cognitive control, in the ability to orchestrate thought and action in accordance with internal goals. Its neural basis, however, has remained a mystery. Here, we propose that cognitive control stems from the active maintenance of patterns of activity in the prefrontal cortex that represent goals and the means to achieve them. They provide bias signals to other brain structures whose net effect is to guide the flow of activity along neural pathways that establish the proper mappings between inputs, internal states, and outputs needed to perform a given task. We review neurophysiological, neurobiological, neuroimaging, and computational studies that support this theory and discuss its implications as well as further issues to be addressed
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              Structure of a cannabinoid receptor and functional expression of the cloned cDNA.

              Marijuana and many of its constituent cannabinoids influence the central nervous system (CNS) in a complex and dose-dependent manner. Although CNS depression and analgesia are well documented effects of the cannabinoids, the mechanisms responsible for these and other cannabinoid-induced effects are not so far known. The hydrophobic nature of these substances has suggested that cannabinoids resemble anaesthetic agents in their action, that is, they nonspecifically disrupt cellular membranes. Recent evidence, however, has supported a mechanism involving a G protein-coupled receptor found in brain and neural cell lines, and which inhibits adenylate cyclase activity in a dose-dependent, stereoselective and pertussis toxin-sensitive manner. Also, the receptor is more responsive to psychoactive cannabinoids than to non-psychoactive cannabinoids. Here we report the cloning and expression of a complementary DNA that encodes a G protein-coupled receptor with all of these properties. Its messenger RNA is found in cell lines and regions of the brain that have cannabinoid receptors. These findings suggest that this protein is involved in cannabinoid-induced CNS effects (including alterations in mood and cognition) experienced by users of marijuana.
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                Author and article information

                Contributors
                Journal
                Front Synaptic Neurosci
                Front Synaptic Neurosci
                Front. Synaptic Neurosci.
                Frontiers in Synaptic Neuroscience
                Frontiers Media S.A.
                1663-3563
                10 June 2021
                2021
                : 13
                : 660218
                Affiliations
                [1] 1Department of Psychology, University of Colorado Denver , Denver, CO, United States
                [2] 2Department of Biomedical Sciences, Marquette University , Milwaukee, WI, United States
                Author notes

                Edited by: Luigia Cristino, Istituto di Chimica Biomolecolare (CNR), Italy

                Reviewed by: Heather Bradshaw, Indiana University Bloomington, United States; Brady Atwood, Indiana University, United States

                *Correspondence: Erik B. Oleson, erik.oleson@ 123456ucdenver.edu

                These authors have contributed equally to this work

                Article
                10.3389/fnsyn.2021.660218
                8222827
                34177546
                7d39645a-d9b0-4ae9-92fe-1789429cc567
                Copyright © 2021 Oleson, Hamilton and Gomez.

                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) and the copyright owner(s) 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
                : 29 January 2021
                : 05 May 2021
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 354, Pages: 31, Words: 0
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Funded by: National Institutes of Health 10.13039/100000002
                Funded by: Boettcher Foundation 10.13039/100005508
                Categories
                Neuroscience
                Review

                Neurosciences
                cannabinoids,dopamine,motivation,reinforcement,attention,habit,timing,adjunctive
                Neurosciences
                cannabinoids, dopamine, motivation, reinforcement, attention, habit, timing, adjunctive

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