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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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 |
work_keys_str_mv |
AT maggiemshin intrinsiccontrolofneuronaldiversityandsynapticspecificityinaproprioceptivecircuit AT catarinacatela intrinsiccontrolofneuronaldiversityandsynapticspecificityinaproprioceptivecircuit AT jeremydasen intrinsiccontrolofneuronaldiversityandsynapticspecificityinaproprioceptivecircuit |
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