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      Putative Cholinergic Interneurons in the Ventral and Dorsal Regions of the Striatum Have Distinct Roles in a Two Choice Alternative Association Task

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          Abstract

          The striatum consists of GABAergic projection neurons and various types of interneurons. Despite their relative scarcity, these interneurons play a key role in information processing in the striatum. One such class of interneurons is the cholinergic tonically active neurons (TANs). In the dorsal striatum, TANs are traditionally considered to be responsive to events of motivational significance. However, in recent years, studies have suggested that TANs are not exclusively related to reward and reward-predicting stimuli, but may contribute to other processes, including responses to aversive stimuli, detecting the spatial location of stimuli and generating movement. Currently there is little data concerning TAN activity in the ventral striatum (VS) of behaving animals. Here, we simultaneously recorded neurons in the ventral and the dorsolateral (DLS) regions of the striatum while animals performed a two choice alternative association task. Our data show that a large percentage of the putative TANs in both regions responded around movement initiation and execution. The majority of these neurons exhibited directional selectivity which was stronger in DLS relative to VS. In addition, the preferred directions in VS were mostly contralateral to the recording site whereas the observed preferred directions in DLS were equally distributed contralaterally and ipsilaterally to the recording site. The most interesting difference between DLS and VS was that DLS TANs maintained activity alterations throughout the movement whereas TANs in VS exhibited short-lasting phasic activity alterations that were maintained throughout the movement by different neurons. Our findings suggest that coding of movement by TANs in both regions overlaps to some degree, yet the differences in response patterns support the notion that the TANs in DLS participate in the motor loop whereas TANs in VS convey event-related information such as movement initiation, movement direction, and end of movement.

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          Most cited references37

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          Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill.

          The learning of new skills is characterized by an initial phase of rapid improvement in performance and a phase of more gradual improvements as skills are automatized and performance asymptotes. Using in vivo striatal recordings, we observed region-specific changes in neural activity during the different phases of skill learning, with the associative or dorsomedial striatum being preferentially engaged early in training and the sensorimotor or dorsolateral striatum being engaged later in training. Ex vivo recordings from medium spiny striatal neurons in brain slices of trained mice revealed that the changes observed in vivo corresponded to regional- and training-specific changes in excitatory synaptic transmission in the striatum. Furthermore, the potentiation of glutamatergic transmission observed in dorsolateral striatum after extensive training was preferentially expressed in striatopallidal neurons, rather than striatonigral neurons. These findings demonstrate that region- and pathway-specific plasticity sculpts the circuits involved in the performance of the skill as it becomes automatized.
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            Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop.

            This paper reviews some of the recent findings on different aspects of the anatomical organization of the basal ganglia. Attempts have been made to delineate the anatomical substrate of information processing along the cortico-basal ganglia-thalamo-cortical loop. Emphasis has been placed on data obtained with highly sensitive anterograde tract-tracing methods applied to the study of the main axis of the loop, which is composed of the striatum, the pallidum, and the substantia nigra. These findings have highlighted the complexities of the organization of the intrinsic basal ganglia circuitry, which comprises multiple modular units that are distributed according to highly ordered and repetitive patterns. Such an arrangement is well suited to convey cortical information in a highly specific manner throughout the basal ganglia. The basal ganglia circuitry is also designed so as to modulate in a precise manner the neuronal activity of several brain functional systems, which are involved in the direct control of different aspects of psychomotor behavior. Of utmost importance is the action of the basal ganglia on thalamocortical premotor neurons. It is through these neurons, which can be considered as a sort of final common pathway, that the basal ganglia ultimately influence the complex neuronal computation that goes on at cortical level.
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              From motivation to action: functional interface between the limbic system and the motor system.

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                Author and article information

                Journal
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Research Foundation
                1662-5137
                31 May 2011
                2011
                : 5
                : 36
                Affiliations
                [1] 1simpleGonda Interdisciplinary Brain Research Center, Bar Ilan University Ramat-Gan, Israel
                [2] 2simpleThe Goodman Faculty of Life Sciences, Bar Ilan University Ramat-Gan, Israel
                Author notes

                Edited by: James M. Tepper, Rutgers, The State University of New Jersey, USA

                Reviewed by: Joshua D. Berke, University of Michigan, USA; Mandar Shrikrishna Jog, University of Western Ontario, Canada

                *Correspondence: Dana Cohen, The Gonda Interdisciplinary Brain Research Center, Bar Ilan University, Ramat Gan 52900, Israel. e-mail: danacoh@ 123456gmail.com
                Article
                10.3389/fnsys.2011.00036
                3106210
                21660109
                8e1a704e-dd59-4afa-86da-91b6b0ae4b22
                Copyright © 2011 Yarom and Cohen.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 31 January 2011
                : 18 May 2011
                Page count
                Figures: 4, Tables: 0, Equations: 1, References: 53, Pages: 9, Words: 7741
                Categories
                Neuroscience
                Original Research

                Neurosciences
                ventral striatum,motor control,movement coding,dorsal striatum,chronic recording,cholinergic interneurons

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