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Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord

BACKGROUND: Substantia gelatinosa (SG, lamina II) is a spinal cord region where most unmyelinated primary afferents terminate and the central nociceptive processing begins. The glutamatergic excitatory interneurons (EINs) form the majority of the SG neuron population, but little is known about the m...

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Autores principales: Santos, Sónia F. A., Luz, Liliana L., Szucs, Peter, Lima, Deolinda, Derkach, Victor A., Safronov, Boris V.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2778873/
https://www.ncbi.nlm.nih.gov/pubmed/19956641
http://dx.doi.org/10.1371/journal.pone.0008047
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author Santos, Sónia F. A.
Luz, Liliana L.
Szucs, Peter
Lima, Deolinda
Derkach, Victor A.
Safronov, Boris V.
author_facet Santos, Sónia F. A.
Luz, Liliana L.
Szucs, Peter
Lima, Deolinda
Derkach, Victor A.
Safronov, Boris V.
author_sort Santos, Sónia F. A.
collection PubMed
description BACKGROUND: Substantia gelatinosa (SG, lamina II) is a spinal cord region where most unmyelinated primary afferents terminate and the central nociceptive processing begins. The glutamatergic excitatory interneurons (EINs) form the majority of the SG neuron population, but little is known about the mechanisms of signal processing in their synapses. METHODOLOGY: To describe the functional organization and properties of excitatory synapses formed by SG EINs, we did non-invasive recordings from 183 pairs of monosynaptically connected neurons. An intact presynaptic SG EIN was specifically stimulated through the cell-attached pipette while the evoked EPSCs/EPSPs were recorded through perforated-patch from a postsynaptic neuron (laminae I-III). PRINCIPAL FINDINGS: We found that the axon of an SG EIN forms multiple functional synapses on the dendrites of a postsynaptic neuron. In many cases, EPSPs evoked by stimulating an SG EIN were sufficient to elicit spikes in a postsynaptic neuron. EPSCs were carried through both Ca(2+)-permeable (CP) and Ca(2+)-impermeable (CI) AMPA receptors (AMPARs) and showed diverse forms of functional plasticity. The synaptic efficacy could be enhanced through both activation of silent synapses and strengthening of already active synapses. We have also found that a high input resistance (R(IN), >0.5 GΩ) of the postsynaptic neuron is necessary for resolving distal dendritic EPSCs/EPSPs and correct estimation of their efficacy. CONCLUSIONS/SIGNIFICANCE: We conclude that the multiple synapses formed by an SG EIN on a postsynaptic neuron increase synaptic excitation and provide basis for diverse forms of plasticity. This functional organization can be important for sensory, i.e. nociceptive, processing in the spinal cord.
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spelling pubmed-27788732009-12-03 Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord Santos, Sónia F. A. Luz, Liliana L. Szucs, Peter Lima, Deolinda Derkach, Victor A. Safronov, Boris V. PLoS One Research Article BACKGROUND: Substantia gelatinosa (SG, lamina II) is a spinal cord region where most unmyelinated primary afferents terminate and the central nociceptive processing begins. The glutamatergic excitatory interneurons (EINs) form the majority of the SG neuron population, but little is known about the mechanisms of signal processing in their synapses. METHODOLOGY: To describe the functional organization and properties of excitatory synapses formed by SG EINs, we did non-invasive recordings from 183 pairs of monosynaptically connected neurons. An intact presynaptic SG EIN was specifically stimulated through the cell-attached pipette while the evoked EPSCs/EPSPs were recorded through perforated-patch from a postsynaptic neuron (laminae I-III). PRINCIPAL FINDINGS: We found that the axon of an SG EIN forms multiple functional synapses on the dendrites of a postsynaptic neuron. In many cases, EPSPs evoked by stimulating an SG EIN were sufficient to elicit spikes in a postsynaptic neuron. EPSCs were carried through both Ca(2+)-permeable (CP) and Ca(2+)-impermeable (CI) AMPA receptors (AMPARs) and showed diverse forms of functional plasticity. The synaptic efficacy could be enhanced through both activation of silent synapses and strengthening of already active synapses. We have also found that a high input resistance (R(IN), >0.5 GΩ) of the postsynaptic neuron is necessary for resolving distal dendritic EPSCs/EPSPs and correct estimation of their efficacy. CONCLUSIONS/SIGNIFICANCE: We conclude that the multiple synapses formed by an SG EIN on a postsynaptic neuron increase synaptic excitation and provide basis for diverse forms of plasticity. This functional organization can be important for sensory, i.e. nociceptive, processing in the spinal cord. Public Library of Science 2009-11-30 /pmc/articles/PMC2778873/ /pubmed/19956641 http://dx.doi.org/10.1371/journal.pone.0008047 Text en Santos et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Santos, Sónia F. A.
Luz, Liliana L.
Szucs, Peter
Lima, Deolinda
Derkach, Victor A.
Safronov, Boris V.
Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title_full Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title_fullStr Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title_full_unstemmed Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title_short Transmission Efficacy and Plasticity in Glutamatergic Synapses Formed by Excitatory Interneurons of the Substantia Gelatinosa in the Rat Spinal Cord
title_sort transmission efficacy and plasticity in glutamatergic synapses formed by excitatory interneurons of the substantia gelatinosa in the rat spinal cord
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2778873/
https://www.ncbi.nlm.nih.gov/pubmed/19956641
http://dx.doi.org/10.1371/journal.pone.0008047
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