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      Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Summary

          Layering of neural circuits facilitates the separation of neurons with high spatial sensitivity from those that play integrative temporal roles. Although anatomical layers are readily identifiable in the brain, layering is not structurally obvious in the spinal cord. But computational studies of motor behaviors have led to the concept of layered processing in the spinal cord. It has been postulated that spinal V3 interneurons (INs) play multiple roles in locomotion, leading us to investigate whether they form layered microcircuits. Using patch-clamp recordings in combination with holographic glutamate uncaging, we demonstrate focal, layered modules, in which ventromedial V3 INs form synapses with one another and with ventrolateral V3 INs, which in turn form synapses with ipsilateral motoneurons. Motoneurons, in turn, provide recurrent excitatory, glutamatergic input to V3 INs. Thus, ventral V3 interneurons form layered microcircuits that could function to ensure well-timed, spatially specific movements.

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          Highlights

          • Two populations of ventral spinal V3 interneurons (INs) can be distinguished

          • Medial (V3 VMed) and lateral (V3 VLat) populations differ in connectivity patterns

          • Motoneuron axons recurrently excite ipsilateral V3 INs

          • Ventral spinal V3 INs form layered microcircuits for motor output

          Abstract

          Using electrophysiology combined with holographic photostimulation, Chopek et al. demonstrate focal layered microcircuits within the spinal cord. These microcircuits are composed of two ventral V3 interneuron sub-populations and ipsilateral motoneurons. Synaptic connectivity was established from medial to lateral, with motoneurons recurrently exciting both V3 interneuron sub-populations.

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          Most cited references 59

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          Neuronal circuits of the neocortex.

          We explore the extent to which neocortical circuits generalize, i.e., to what extent can neocortical neurons and the circuits they form be considered as canonical? We find that, as has long been suspected by cortical neuroanatomists, the same basic laminar and tangential organization of the excitatory neurons of the neocortex is evident wherever it has been sought. Similarly, the inhibitory neurons show characteristic morphology and patterns of connections throughout the neocortex. We offer a simple model of cortical processing that is consistent with the major features of cortical circuits: The superficial layer neurons within local patches of cortex, and within areas, cooperate to explore all possible interpretations of different cortical input and cooperatively select an interpretation consistent with their various cortical and subcortical inputs.
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            Decoding the organization of spinal circuits that control locomotion.

             Ole Kiehn (2016)
            Unravelling the functional operation of neuronal networks and linking cellular activity to specific behavioural outcomes are among the biggest challenges in neuroscience. In this broad field of research, substantial progress has been made in studies of the spinal networks that control locomotion. Through united efforts using electrophysiological and molecular genetic network approaches and behavioural studies in phylogenetically diverse experimental models, the organization of locomotor networks has begun to be decoded. The emergent themes from this research are that the locomotor networks have a modular organization with distinct transmitter and molecular codes and that their organization is reconfigured with changes to the speed of locomotion or changes in gait.
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              Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo.

              Dopamine neurons in the ventral tegmental area (VTA) play an important role in the motivational systems underlying drug addiction, and recent work has suggested that they also release the excitatory neurotransmitter glutamate. To assess a physiological role for glutamate corelease, we disrupted the expression of vesicular glutamate transporter 2 selectively in dopamine neurons. The conditional knockout abolishes glutamate release from midbrain dopamine neurons in culture and severely reduces their excitatory synaptic output in mesoaccumbens slices. Baseline motor behavior is not affected, but stimulation of locomotor activity by cocaine is impaired, apparently through a selective reduction of dopamine stores in the projection of VTA neurons to ventral striatum. Glutamate co-entry promotes monoamine storage by increasing the pH gradient that drives vesicular monoamine transport. Remarkably, low concentrations of glutamate acidify synaptic vesicles more slowly but to a greater extent than equimolar Cl(-), indicating a distinct, presynaptic mechanism to regulate quantal size. Copyright 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Cell Rep
                Cell Rep
                Cell Reports
                Cell Press
                2211-1247
                02 October 2018
                02 October 2018
                02 October 2018
                : 25
                : 1
                : 146-156.e3
                Affiliations
                [1 ]Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, NS B3H 4R2, Canada
                [2 ]Sobell Department of Neuromuscular Diseases, Institute of Neurology, University College London, London WC1N 3BG, UK
                [3 ]Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, UK
                Author notes
                []Corresponding author r.brownstone@ 123456ucl.ac.uk
                [∗∗ ]Corresponding author ying.zhang@ 123456dal.ca
                [4]

                Lead Contact

                Article
                S2211-1247(18)31414-1
                10.1016/j.celrep.2018.08.095
                6180347
                30282024
                © 2018 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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