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 inCell reports (Cambridge) Vol. 25; no. 1; pp. 146 - 156.e3
Main Authors Chopek, Jeremy W., Nascimento, Filipe, Beato, Marco, Brownstone, Robert M., Zhang, Ying
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 02.10.2018
Cell Press
Elsevier
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Online AccessGet full text
ISSN2211-1247
2211-1247
DOI10.1016/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. [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.
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
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Issue 1
Keywords spinal interneurons
microcircuits
interneuron subpopulations
recurrent excitation
caged glutamate
motoneurons
holographic photostimulation
spatial light modulator
Language English
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Snippet Layering of neural circuits facilitates the separation of neurons with high spatial sensitivity from those that play integrative temporal roles. Although...
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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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