Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit

Relay of muscle-derived sensory information to the CNS is essential for the execution of motor behavior, but how proprioceptive sensory neurons (pSNs) establish functionally appropriate connections is poorly understood. A prevailing model of sensory-motor circuit assembly is that peripheral, target-...

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Main Authors: Maggie M Shin, Catarina Catela, Jeremy Dasen
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/56374
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spelling doaj-c559db669d624f7fa6f68495434f1e1d2021-05-05T21:25:19ZengeLife Sciences Publications LtdeLife2050-084X2020-08-01910.7554/eLife.56374Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuitMaggie M Shin0https://orcid.org/0000-0001-7891-0774Catarina Catela1Jeremy Dasen2https://orcid.org/0000-0002-9434-874XNeuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, United StatesDepartment of Neurobiology, University of Chicago, Chicago, United StatesNeuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, United StatesRelay of muscle-derived sensory information to the CNS is essential for the execution of motor behavior, but how proprioceptive sensory neurons (pSNs) establish functionally appropriate connections is poorly understood. A prevailing model of sensory-motor circuit assembly is that peripheral, target-derived, cues instruct pSN identities and patterns of intraspinal connectivity. To date no known intrinsic determinants of muscle-specific pSN fates have been described in vertebrates. We show that expression of Hox transcription factors defines pSN subtypes, and these profiles are established independently of limb muscle. The Hoxc8 gene is expressed by pSNs and motor neurons (MNs) targeting distal forelimb muscles, and sensory-specific depletion of Hoxc8 in mice disrupts sensory-motor synaptic matching, without affecting pSN survival or muscle targeting. These results indicate that the diversity and central specificity of pSNs and MNs are regulated by a common set of determinants, thus linking early rostrocaudal patterning to the assembly of limb control circuits.https://elifesciences.org/articles/56374spinal cordmotor neuronproprioceptionsensory neuronhox geneneural circuit
collection DOAJ
language English
format Article
sources DOAJ
author Maggie M Shin
Catarina Catela
Jeremy Dasen
spellingShingle Maggie M Shin
Catarina Catela
Jeremy Dasen
Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
eLife
spinal cord
motor neuron
proprioception
sensory neuron
hox gene
neural circuit
author_facet Maggie M Shin
Catarina Catela
Jeremy Dasen
author_sort Maggie M Shin
title Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
title_short Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
title_full Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
title_fullStr Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
title_full_unstemmed Intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
title_sort intrinsic control of neuronal diversity and synaptic specificity in a proprioceptive circuit
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-08-01
description Relay of muscle-derived sensory information to the CNS is essential for the execution of motor behavior, but how proprioceptive sensory neurons (pSNs) establish functionally appropriate connections is poorly understood. A prevailing model of sensory-motor circuit assembly is that peripheral, target-derived, cues instruct pSN identities and patterns of intraspinal connectivity. To date no known intrinsic determinants of muscle-specific pSN fates have been described in vertebrates. We show that expression of Hox transcription factors defines pSN subtypes, and these profiles are established independently of limb muscle. The Hoxc8 gene is expressed by pSNs and motor neurons (MNs) targeting distal forelimb muscles, and sensory-specific depletion of Hoxc8 in mice disrupts sensory-motor synaptic matching, without affecting pSN survival or muscle targeting. These results indicate that the diversity and central specificity of pSNs and MNs are regulated by a common set of determinants, thus linking early rostrocaudal patterning to the assembly of limb control circuits.
topic spinal cord
motor neuron
proprioception
sensory neuron
hox gene
neural circuit
url https://elifesciences.org/articles/56374
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AT catarinacatela intrinsiccontrolofneuronaldiversityandsynapticspecificityinaproprioceptivecircuit
AT jeremydasen intrinsiccontrolofneuronaldiversityandsynapticspecificityinaproprioceptivecircuit
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