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


Punnakkal, Pradeep; von Schoultz, Carolin; Haenraets, Karen; Wildner, Hendrik; Zeilhofer, Hanns Ulrich (2014). Morphological, biophysical and synaptic properties of glutamatergic neurons of the mouse spinal dorsal horn. Journal of Physiology, 592(4):759-776.

Abstract

Interneurons of the spinal dorsal horn take a centre stage in 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 eGFP under the control of the vGluT2 gene (vGluT2-eGFP mice) to perform a detailed electrophysiological and morphological characterization 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 that, as demonstrated by the coexpression of vGluT2-eGFP with different markers of subtypes of glutamatergic neurons, likely 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.

Abstract

Interneurons of the spinal dorsal horn take a centre stage in 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 eGFP under the control of the vGluT2 gene (vGluT2-eGFP mice) to perform a detailed electrophysiological and morphological characterization 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 that, as demonstrated by the coexpression of vGluT2-eGFP with different markers of subtypes of glutamatergic neurons, likely 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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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Institute of Pharmacology and Toxicology
07 Faculty of Science > Institute of Pharmacology and Toxicology
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Language:English
Date:2014
Deposited On:16 Dec 2013 13:22
Last Modified:08 Dec 2017 01:05
Publisher:Wiley-Blackwell
ISSN:0022-3751
Additional Information:The definitive version is available at www.blackwell-synergy.com and www.jphysiol.org
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1113/jphysiol.2013.264937
PubMed ID:24324003

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