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      Dorsal Striatal Circuits for Habits, Compulsions and Addictions


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          Here, we review the neural circuit bases of habits, compulsions, and addictions, behaviors which are all characterized by relatively automatic action performance. We discuss relevant studies, primarily from the rodent literature, and describe how major headway has been made in identifying the brain regions and neural cell types whose activity is modulated during the acquisition and performance of these automated behaviors. The dorsal striatum and cortical inputs to this structure have emerged as key players in the wider basal ganglia circuitry encoding behavioral automaticity, and changes in the activity of different neuronal cell-types in these brain regions have been shown to co-occur with the formation of automatic behaviors. We highlight how disordered functioning of these neural circuits can result in neuropsychiatric disorders, such as obsessive-compulsive disorder (OCD) and drug addiction. Finally, we discuss how the next phase of research in the field may benefit from integration of approaches for access to cells based on their genetic makeup, activity, connectivity and precise anatomical location.

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          Most cited references165

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          Fully integrated silicon probes for high-density recording of neural activity

          Sensory, motor and cognitive operations involve the coordinated action of large neuronal populations across multiple brain regions in both superficial and deep structures. Existing extracellular probes record neural activity with excellent spatial and temporal (sub-millisecond) resolution, but from only a few dozen neurons per shank. Optical Ca2+ imaging offers more coverage but lacks the temporal resolution needed to distinguish individual spikes reliably and does not measure local field potentials. Until now, no technology compatible with use in unrestrained animals has combined high spatiotemporal resolution with large volume coverage. Here we design, fabricate and test a new silicon probe known as Neuropixels to meet this need. Each probe has 384 recording channels that can programmably address 960 complementary metal–oxide–semiconductor (CMOS) processing-compatible low-impedance TiN sites that tile a single 10-mm long, 70 × 20-μm cross-section shank. The 6 × 9-mm probe base is fabricated with the shank on a single chip. Voltage signals are filtered, amplified, multiplexed and digitized on the base, allowing the direct transmission of noise-free digital data from the probe. The combination of dense recording sites and high channel count yielded well-isolated spiking activity from hundreds of neurons per probe implanted in mice and rats. Using two probes, more than 700 well-isolated single neurons were recorded simultaneously from five brain structures in an awake mouse. The fully integrated functionality and small size of Neuropixels probes allowed large populations of neurons from several brain structures to be recorded in freely moving animals. This combination of high-performance electrode technology and scalable chip fabrication methods opens a path towards recording of brain-wide neural activity during behaviour.
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            Synaptic plasticity: multiple forms, functions, and mechanisms.

            Experiences, whether they be learning in a classroom, a stressful event, or ingestion of a psychoactive substance, impact the brain by modifying the activity and organization of specific neural circuitry. A major mechanism by which the neural activity generated by an experience modifies brain function is via modifications of synaptic transmission; that is, synaptic plasticity. Here, we review current understanding of the mechanisms of the major forms of synaptic plasticity at excitatory synapses in the mammalian brain. We also provide examples of the possible developmental and behavioral functions of synaptic plasticity and how maladaptive synaptic plasticity may contribute to neuropsychiatric disorders.
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              Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action.

              Recent behavioral studies in both humans and rodents have found evidence that performance in decision-making tasks depends on two different learning processes; one encoding the relationship between actions and their consequences and a second involving the formation of stimulus-response associations. These learning processes are thought to govern goal-directed and habitual actions, respectively, and have been found to depend on homologous corticostriatal networks in these species. Thus, recent research using comparable behavioral tasks in both humans and rats has implicated homologous regions of cortex (medial prefrontal cortex/medial orbital cortex in humans and prelimbic cortex in rats) and of dorsal striatum (anterior caudate in humans and dorsomedial striatum in rats) in goal-directed action and in the control of habitual actions (posterior lateral putamen in humans and dorsolateral striatum in rats). These learning processes have been argued to be antagonistic or competing because their control over performance appears to be all or none. Nevertheless, evidence has started to accumulate suggesting that they may at times compete and at others cooperate in the selection and subsequent evaluation of actions necessary for normal choice performance. It appears likely that cooperation or competition between these sources of action control depends not only on local interactions in dorsal striatum but also on the cortico-basal ganglia network within which the striatum is embedded and that mediates the integration of learning with basic motivational and emotional processes. The neural basis of the integration of learning and motivation in choice and decision-making is still controversial and we review some recent hypotheses relating to this issue.

                Author and article information

                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                18 July 2019
                : 13
                : 28
                [1] 1Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem , Jerusalem, Israel
                [2] 2Zuckerman Postdoctoral Scholar , Jerusalem, Israel
                [3] 3Institute of Life Sciences, Edmond J. Safra Campus, Hebrew University of Jerusalem , Jerusalem, Israel
                [4] 4Program in Child and Brain Development, MaRS Centre, Canadian Institute for Advanced Research , Toronto, ON, Canada
                Author notes

                Edited by: Jimena Andersen, Stanford University, United States

                Reviewed by: Sarah Heilbronner, University of Minnesota Twin Cities, United States; Eric Burguière, Centre National de la Recherche Scientifique (CNRS), France

                These authors have contributed equally to this work

                Copyright © 2019 Lipton, Gonzales and Citri.

                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.

                : 17 January 2019
                : 27 June 2019
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 162, Pages: 14, Words: 12695
                Funded by: H2020 European Research Council 10.13039/100010663
                Award ID: 770951
                Funded by: Israel Science Foundation 10.13039/501100003977
                Award ID: 393/12, 1062/18, 1796/12
                Funded by: FP7 People: Marie-Curie Actions 10.13039/100011264
                Award ID: PCIG13-GA-2013-618201
                Funded by: Canadian Institute for Advanced Research 10.13039/100007631
                Funded by: National Institute for Psychobiology in Israel, Hebrew University of Jerusalem 10.13039/501100001739
                Mini Review

                habits,goal-directed behavior,striatum,prefrontal cortex,dorsomedial striatum,dorsolateral striatum


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