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Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn

Interneurons of the spinal dorsal horn are central to somatosensory and nociceptive processing. A mechanistic understanding of their function depends on profound knowledge of their intrinsic properties and their integration into dorsal horn circuits. Here, we have used BAC transgenic mice expressing...

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Autores principales: Punnakkal, Pradeep, Schoultz, Carolin, Haenraets, Karen, Wildner, Hendrik, Zeilhofer, Hanns Ulrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3934713/
https://www.ncbi.nlm.nih.gov/pubmed/24324003
http://dx.doi.org/10.1113/jphysiol.2013.264937
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author Punnakkal, Pradeep
Schoultz, Carolin
Haenraets, Karen
Wildner, Hendrik
Zeilhofer, Hanns Ulrich
author_facet Punnakkal, Pradeep
Schoultz, Carolin
Haenraets, Karen
Wildner, Hendrik
Zeilhofer, Hanns Ulrich
author_sort Punnakkal, Pradeep
collection PubMed
description Interneurons of the spinal dorsal horn are central to somatosensory and nociceptive processing. A mechanistic understanding of their function depends on profound knowledge of their intrinsic properties and their integration into dorsal horn circuits. Here, we have used BAC transgenic mice expressing enhanced green fluorescent protein (eGFP) under the control of the vesicular glutamate transporter (vGluT2) gene (vGluT2::eGFP mice) to perform a detailed electrophysiological and morphological characterisation of excitatory dorsal horn neurons, and to compare their properties to those of GABAergic (Gad67::eGFP tagged) and glycinergic (GlyT2::eGFP tagged) neurons. vGluT2::eGFP was detected in about one-third of all excitatory dorsal horn neurons and, as demonstrated by the co-expression of vGluT2::eGFP with different markers of subtypes of glutamatergic neurons, probably labelled a representative fraction of these neurons. Three types of dendritic tree morphologies (vertical, central, and radial), but no islet cell-type morphology, were identified in vGluT2::eGFP neurons. vGluT2::eGFP neurons had more depolarised action potential thresholds and longer action potential durations than inhibitory neurons, while no significant differences were found for the resting membrane potential, input resistance, cell capacitance and after-hyperpolarisation. Delayed firing and single action potential firing were the single most prevalent firing patterns in vGluT2::eGFP neurons of the superficial and deep dorsal horn, respectively. By contrast, tonic firing prevailed in inhibitory interneurons of the dorsal horn. Capsaicin-induced synaptic inputs were detected in about half of the excitatory and inhibitory neurons, and occurred more frequently in superficial than in deep dorsal horn neurons. Primary afferent-evoked (polysynaptic) inhibitory inputs were found in the majority of glutamatergic and glycinergic neurons, but only in less than half of the GABAergic population. Excitatory dorsal horn neurons thus differ from their inhibitory counterparts in several biophysical properties and possibly also in their integration into the local neuronal circuitry.
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spelling pubmed-39347132014-05-22 Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn Punnakkal, Pradeep Schoultz, Carolin Haenraets, Karen Wildner, Hendrik Zeilhofer, Hanns Ulrich J Physiol Neuroscience: Behavioural/Systems/Cognitive Interneurons of the spinal dorsal horn are central to somatosensory and nociceptive processing. A mechanistic understanding of their function depends on profound knowledge of their intrinsic properties and their integration into dorsal horn circuits. Here, we have used BAC transgenic mice expressing enhanced green fluorescent protein (eGFP) under the control of the vesicular glutamate transporter (vGluT2) gene (vGluT2::eGFP mice) to perform a detailed electrophysiological and morphological characterisation of excitatory dorsal horn neurons, and to compare their properties to those of GABAergic (Gad67::eGFP tagged) and glycinergic (GlyT2::eGFP tagged) neurons. vGluT2::eGFP was detected in about one-third of all excitatory dorsal horn neurons and, as demonstrated by the co-expression of vGluT2::eGFP with different markers of subtypes of glutamatergic neurons, probably labelled a representative fraction of these neurons. Three types of dendritic tree morphologies (vertical, central, and radial), but no islet cell-type morphology, were identified in vGluT2::eGFP neurons. vGluT2::eGFP neurons had more depolarised action potential thresholds and longer action potential durations than inhibitory neurons, while no significant differences were found for the resting membrane potential, input resistance, cell capacitance and after-hyperpolarisation. Delayed firing and single action potential firing were the single most prevalent firing patterns in vGluT2::eGFP neurons of the superficial and deep dorsal horn, respectively. By contrast, tonic firing prevailed in inhibitory interneurons of the dorsal horn. Capsaicin-induced synaptic inputs were detected in about half of the excitatory and inhibitory neurons, and occurred more frequently in superficial than in deep dorsal horn neurons. Primary afferent-evoked (polysynaptic) inhibitory inputs were found in the majority of glutamatergic and glycinergic neurons, but only in less than half of the GABAergic population. Excitatory dorsal horn neurons thus differ from their inhibitory counterparts in several biophysical properties and possibly also in their integration into the local neuronal circuitry. John Wiley & Sons Ltd 2014-02-15 2014-01-08 /pmc/articles/PMC3934713/ /pubmed/24324003 http://dx.doi.org/10.1113/jphysiol.2013.264937 Text en ©2013 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society. http://creativecommons.org/licenses/by/3.0/ This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience: Behavioural/Systems/Cognitive
Punnakkal, Pradeep
Schoultz, Carolin
Haenraets, Karen
Wildner, Hendrik
Zeilhofer, Hanns Ulrich
Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title_full Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title_fullStr Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title_full_unstemmed Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title_short Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
title_sort morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn
topic Neuroscience: Behavioural/Systems/Cognitive
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3934713/
https://www.ncbi.nlm.nih.gov/pubmed/24324003
http://dx.doi.org/10.1113/jphysiol.2013.264937
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