Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits
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 mot...
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Published in | Cell reports (Cambridge) Vol. 25; no. 1; pp. 146 - 156.e3 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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United States
Elsevier Inc
02.10.2018
Cell Press Elsevier |
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ISSN | 2211-1247 2211-1247 |
DOI | 10.1016/j.celrep.2018.08.095 |
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Abstract | 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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•Two populations of ventral spinal V3 interneurons (INs) can be distinguished•Medial (V3VMed) and lateral (V3VLat) populations differ in connectivity patterns•Motoneuron axons recurrently excite ipsilateral V3 INs•Ventral spinal V3 INs form layered microcircuits for motor output
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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AbstractList | 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. 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. [Display omitted] •Two populations of ventral spinal V3 interneurons (INs) can be distinguished•Medial (V3VMed) and lateral (V3VLat) populations differ in connectivity patterns•Motoneuron axons recurrently excite ipsilateral V3 INs•Ventral spinal V3 INs form layered microcircuits for motor output 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. 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. : 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. Keywords: motoneurons, microcircuits, spinal interneurons, interneuron subpopulations, holographic photostimulation, caged glutamate, spatial light modulator, recurrent excitation 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. • 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 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. 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.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. |
Author | Zhang, Ying Chopek, Jeremy W. Beato, Marco Nascimento, Filipe Brownstone, Robert M. |
AuthorAffiliation | 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 1 Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, NS B3H 4R2, Canada |
AuthorAffiliation_xml | – name: 1 Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, NS B3H 4R2, Canada – name: 3 Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, UK – name: 2 Sobell Department of Neuromuscular Diseases, Institute of Neurology, University College London, London WC1N 3BG, UK |
Author_xml | – sequence: 1 givenname: Jeremy W. surname: Chopek fullname: Chopek, Jeremy W. organization: Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, NS B3H 4R2, Canada – sequence: 2 givenname: Filipe surname: Nascimento fullname: Nascimento, Filipe organization: Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, UK – sequence: 3 givenname: Marco surname: Beato fullname: Beato, Marco organization: Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, UK – sequence: 4 givenname: Robert M. surname: Brownstone fullname: Brownstone, Robert M. email: r.brownstone@ucl.ac.uk organization: Sobell Department of Neuromuscular Diseases, Institute of Neurology, University College London, London WC1N 3BG, UK – sequence: 5 givenname: Ying surname: Zhang fullname: Zhang, Ying email: ying.zhang@dal.ca organization: Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, NS B3H 4R2, Canada |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30282024$$D View this record in MEDLINE/PubMed |
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Keywords | spinal interneurons microcircuits interneuron subpopulations recurrent excitation caged glutamate motoneurons holographic photostimulation spatial light modulator |
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SubjectTerms | Animals caged glutamate holographic photostimulation interneuron subpopulations Interneurons - physiology Mice microcircuits motoneurons Motor Neurons - physiology recurrent excitation spatial light modulator Spinal Cord - physiology spinal interneurons |
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Title | Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits |
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