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      Unique contributions of parvalbumin and cholinergic interneurons in organizing striatal networks during movement

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          Abstract

          Striatal pavalbumin (PV) and cholinergic (CHI) interneurons are poised to play major roles in behavior by coordinating the networks of medium spiny cells that relay motor output. However, the small numbers and scattered distribution of these cells has made it difficult to directly assess their contribution to activity in networks of MSNs during behavior. Here, we build upon recent improvements in single cell calcium imaging combined with optogenetics to test the capacity of PVs and CHIs to affect MSN activity and behavior in mice engaged in voluntarily locomotion. We find that PVs and CHIs have unique effects on MSN activity and dissociable roles in supporting movement. PV cells facilitate movement by refining the activation of MSN networks responsible for movement execution. CHIs, in contrast, synchronize activity within MSN networks to signal the end of a movement bout. These results provide new insights into the striatal network activity that supports movement.

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          Most cited references 49

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          Imaging large-scale neural activity with cellular resolution in awake, mobile mice.

          We report a technique for two-photon fluorescence imaging with cellular resolution in awake, behaving mice with minimal motion artifact. The apparatus combines an upright, table-mounted two-photon microscope with a spherical treadmill consisting of a large, air-supported Styrofoam ball. Mice, with implanted cranial windows, are head restrained under the objective while their limbs rest on the ball's upper surface. Following adaptation to head restraint, mice maneuver on the spherical treadmill as their heads remain motionless. Image sequences demonstrate that running-associated brain motion is limited to approximately 2-5 microm. In addition, motion is predominantly in the focal plane, with little out-of-plane motion, making the application of a custom-designed Hidden-Markov-Model-based motion correction algorithm useful for postprocessing. Behaviorally correlated calcium transients from large neuronal and astrocytic populations were routinely measured, with an estimated motion-induced false positive error rate of <5%.
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            Putting a spin on the dorsal-ventral divide of the striatum.

            Since its conception three decades ago, the idea that the striatum consists of a dorsal sensorimotor part and a ventral portion processing limbic information has sparked a quest for functional correlates and anatomical characteristics of the striatal divisions. But this classic dorsal-ventral distinction might not offer the best view of striatal function. Anatomy and neurophysiology show that the two striatal areas have the same basic structure and that sharp boundaries are absent. Behaviorally, a distinction between dorsolateral and ventromedial seems most valid, in accordance with a mediolateral functional zonation imposed on the striatum by its excitatory cortical, thalamic and amygdaloid inputs. Therefore, this review presents a synthesis between the dorsal-ventral distinction and the more mediolateral-oriented functional striatal gradient.
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              • Article: not found

              D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons.

              Dopamine shapes a wide variety of psychomotor functions. This is mainly accomplished by modulating cortical and thalamic glutamatergic signals impinging upon principal medium spiny neurons (MSNs) of the striatum. Several lines of evidence suggest that dopamine D1 receptor signaling enhances dendritic excitability and glutamatergic signaling in striatonigral MSNs, whereas D2 receptor signaling exerts the opposite effect in striatopallidal MSNs. The functional antagonism between these two major striatal dopamine receptors extends to the regulation of synaptic plasticity. Recent studies, using transgenic mice in which cells express D1 and D2 receptors, have uncovered unappreciated differences between MSNs that shape glutamatergic signaling and the influence of DA on synaptic plasticity. These studies have also shown that long-term alterations in dopamine signaling produce profound and cell-type-specific reshaping of corticostriatal connectivity and function.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                25 January 2019
                25 February 2019
                April 2019
                13 September 2019
                : 22
                : 4
                : 586-597
                Affiliations
                [1 ]Boston University, Department of Biomedical Engineering, Boston, MA 02215
                [2 ]Icahn School of Medicine at Mt. Sinai, Department of Neuroscience, New York, NY 10129
                [3 ]Yale School of Medicine, Department of Psychiatry, New Haven, CT, 06510
                [4 ]Boston University, Department of Mathematics and Statistics, Boston, MA 02215
                [5 ]Boston University, Department of Electrical and Computer Engineering, Boston, MA 02215
                Author notes
                [*]

                These authors contributed equally to this work

                Correspondence should be addressed to: Xue Han ( xuehan@ 123456bu.edu ), 44 Cummington Street, Boston, MA 02215. Phone: 617-358-6189

                Author Contributions

                W.M.H. and H.J.G. performed all experiments. M.R. and D.Z. analyzed the data. M.B. contributed software for video processing and data analysis. X.H. supervised the study. W.M.H, H.J.G, M.R., A.G.D, and X.H. wrote the manuscript, and contributed to the interpretation of the results. A.G.D. and MK provided consultation on statistical analysis and on permutation tests. V.S. provided consultation on calcium imaging data analysis and on generalized linear models.

                Article
                NIHMS1519155
                10.1038/s41593-019-0341-3
                6744276
                30804530

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                Categories
                Article

                Neurosciences

                striatum, motor, basal ganglia, calcium imaging, gcamp6f, in vivo imaging

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