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Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn

Nociceptive information is relayed through the spinal cord dorsal horn, a critical area in sensory processing. The neuronal circuits in this region that underpin sensory perception must be clarified to better understand how dysfunction can lead to pathological pain. This study used an optogenetic ap...

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Autores principales: Smith, Kelly M, Browne, Tyler J, Davis, Olivia C, Coyle, A, Boyle, Kieran A, Watanabe, Masahiko, Dickinson, Sally A, Iredale, Jacqueline A, Gradwell, Mark A, Jobling, Phillip, Callister, Robert J, Dayas, Christopher V, Hughes, David I, Graham, Brett A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908433/
https://www.ncbi.nlm.nih.gov/pubmed/31713514
http://dx.doi.org/10.7554/eLife.49190
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author Smith, Kelly M
Browne, Tyler J
Davis, Olivia C
Coyle, A
Boyle, Kieran A
Watanabe, Masahiko
Dickinson, Sally A
Iredale, Jacqueline A
Gradwell, Mark A
Jobling, Phillip
Callister, Robert J
Dayas, Christopher V
Hughes, David I
Graham, Brett A
author_facet Smith, Kelly M
Browne, Tyler J
Davis, Olivia C
Coyle, A
Boyle, Kieran A
Watanabe, Masahiko
Dickinson, Sally A
Iredale, Jacqueline A
Gradwell, Mark A
Jobling, Phillip
Callister, Robert J
Dayas, Christopher V
Hughes, David I
Graham, Brett A
author_sort Smith, Kelly M
collection PubMed
description Nociceptive information is relayed through the spinal cord dorsal horn, a critical area in sensory processing. The neuronal circuits in this region that underpin sensory perception must be clarified to better understand how dysfunction can lead to pathological pain. This study used an optogenetic approach to selectively activate spinal interneurons that express the calcium-binding protein calretinin (CR). We show that these interneurons form an interconnected network that can initiate and sustain enhanced excitatory signaling, and directly relay signals to lamina I projection neurons. Photoactivation of CR interneurons in vivo resulted in a significant nocifensive behavior that was morphine sensitive, caused a conditioned place aversion, and was enhanced by spared nerve injury. Furthermore, halorhodopsin-mediated inhibition of these interneurons elevated sensory thresholds. Our results suggest that dorsal horn circuits that involve excitatory CR neurons are important for the generation and amplification of pain and identify these interneurons as a future analgesic target.
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spelling pubmed-69084332019-12-16 Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn Smith, Kelly M Browne, Tyler J Davis, Olivia C Coyle, A Boyle, Kieran A Watanabe, Masahiko Dickinson, Sally A Iredale, Jacqueline A Gradwell, Mark A Jobling, Phillip Callister, Robert J Dayas, Christopher V Hughes, David I Graham, Brett A eLife Neuroscience Nociceptive information is relayed through the spinal cord dorsal horn, a critical area in sensory processing. The neuronal circuits in this region that underpin sensory perception must be clarified to better understand how dysfunction can lead to pathological pain. This study used an optogenetic approach to selectively activate spinal interneurons that express the calcium-binding protein calretinin (CR). We show that these interneurons form an interconnected network that can initiate and sustain enhanced excitatory signaling, and directly relay signals to lamina I projection neurons. Photoactivation of CR interneurons in vivo resulted in a significant nocifensive behavior that was morphine sensitive, caused a conditioned place aversion, and was enhanced by spared nerve injury. Furthermore, halorhodopsin-mediated inhibition of these interneurons elevated sensory thresholds. Our results suggest that dorsal horn circuits that involve excitatory CR neurons are important for the generation and amplification of pain and identify these interneurons as a future analgesic target. eLife Sciences Publications, Ltd 2019-11-12 /pmc/articles/PMC6908433/ /pubmed/31713514 http://dx.doi.org/10.7554/eLife.49190 Text en © 2019, Smith et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Smith, Kelly M
Browne, Tyler J
Davis, Olivia C
Coyle, A
Boyle, Kieran A
Watanabe, Masahiko
Dickinson, Sally A
Iredale, Jacqueline A
Gradwell, Mark A
Jobling, Phillip
Callister, Robert J
Dayas, Christopher V
Hughes, David I
Graham, Brett A
Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title_full Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title_fullStr Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title_full_unstemmed Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title_short Calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
title_sort calretinin positive neurons form an excitatory amplifier network in the spinal cord dorsal horn
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908433/
https://www.ncbi.nlm.nih.gov/pubmed/31713514
http://dx.doi.org/10.7554/eLife.49190
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