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 me...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2009-11-01
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| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC2778873?pdf=render |
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| author | Sónia F A Santos Liliana L Luz Peter Szucs Deolinda Lima Victor A Derkach Boris V Safronov |
| author_facet | Sónia F A Santos Liliana L Luz Peter Szucs Deolinda Lima Victor A Derkach Boris V Safronov |
| author_sort | Sónia F A Santos |
| collection | DOAJ |
| 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 GOmega) 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. |
| first_indexed | 2024-12-11T13:53:19Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-11T13:53:19Z |
| publishDate | 2009-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-7ea90fb151584d9499cd7217e4d128192022-12-22T01:04:11ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-11-01411e804710.1371/journal.pone.0008047Transmission efficacy and plasticity in glutamatergic synapses formed by excitatory interneurons of the substantia gelatinosa in the rat spinal cord.Sónia F A SantosLiliana L LuzPeter SzucsDeolinda LimaVictor A DerkachBoris V SafronovBACKGROUND: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 GOmega) 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.http://europepmc.org/articles/PMC2778873?pdf=render |
| spellingShingle | Sónia F A Santos Liliana L Luz Peter Szucs Deolinda Lima Victor A Derkach Boris V Safronov Transmission efficacy and plasticity in glutamatergic synapses formed by excitatory interneurons of the substantia gelatinosa in the rat spinal cord. PLoS ONE |
| 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 |
| url | http://europepmc.org/articles/PMC2778873?pdf=render |
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