Evidence of calcium-permeable AMPA receptors in dendritic spines of CA1 pyramidal neurons
Identifieur interne : 000136 ( Pmc/Checkpoint ); précédent : 000135; suivant : 000137Evidence of calcium-permeable AMPA receptors in dendritic spines of CA1 pyramidal neurons
Auteurs : Hayley A. Mattison [États-Unis] ; Ashish A. Bagal [États-Unis] ; Michael Mohammadi [États-Unis] ; Nisha S. Pulimood [États-Unis] ; Christian G. Reich [États-Unis] ; Bradley E. Alger [États-Unis] ; Joseph P. Y. Kao [États-Unis] ; Scott M. Thompson [États-Unis]Source :
- Journal of Neurophysiology [ 0022-3077 ] ; 2014.
Abstract
GluA2-lacking, calcium-permeable α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPARs) have unique properties, but their presence at excitatory synapses in pyramidal cells is controversial. We have tested certain predictions of the model that such receptors are present in CA1 cells and show here that the polyamine spermine, but not philanthotoxin, causes use-dependent inhibition of synaptically evoked excitatory responses in stratum radiatum, but not s. oriens, in cultured and acute hippocampal slices. Stimulation of single dendritic spines by photolytic release of caged glutamate induced an
Url:
DOI: 10.1152/jn.00578.2013
PubMed: 24760782
PubMed Central: 4064414
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>GluA2-lacking, calcium-permeable α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPARs) have unique properties, but their presence at excitatory synapses in pyramidal cells is controversial. We have tested certain predictions of the model that such receptors are present in CA1 cells and show here that the polyamine spermine, but not philanthotoxin, causes use-dependent inhibition of synaptically evoked excitatory responses in stratum radiatum, but not s. oriens, in cultured and acute hippocampal slices. Stimulation of single dendritic spines by photolytic release of caged glutamate induced an <italic>N</italic>
-methyl-<sc>d</sc>
-aspartate receptor-independent, use- and spermine-sensitive calcium influx only at apical spines in cultured slices. Bath application of glutamate also triggered a spermine-sensitive influx of cobalt into CA1 cell dendrites in s. radiatum. Responses of single apical, but not basal, spines to photostimulation displayed prominent paired-pulse facilitation (PPF) consistent with use-dependent relief of cytoplasmic polyamine block. Responses at apical dendrites were diminished, and PPF was increased, by spermine. Intracellular application of pep2m, which inhibits recycling of GluA2-containing AMPARs, reduced apical spine responses and increased PPF. We conclude that some calcium-permeable, polyamine-sensitive AMPARs, perhaps lacking GluA2 subunits, are present at synapses on apical dendrites of CA1 pyramidal cells, which may allow distinct forms of synaptic plasticity and computation at different sets of excitatory inputs.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Neurophysiol</journal-id>
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<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
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<title-group><article-title>Evidence of calcium-permeable AMPA receptors in dendritic spines of CA1 pyramidal neurons</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Mattison</surname>
<given-names>Hayley A.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bagal</surname>
<given-names>Ashish A.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mohammadi</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pulimood</surname>
<given-names>Nisha S.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Reich</surname>
<given-names>Christian G.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Alger</surname>
<given-names>Bradley E.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kao</surname>
<given-names>Joseph P. Y.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Thompson</surname>
<given-names>Scott M.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1"><sup>1</sup>
Department of Physiology, University of Maryland School of Medicine, Baltimore, Maryland;</aff>
<aff id="aff2"><sup>2</sup>
Membrane Biology Training Program, University of Maryland School of Medicine, Baltimore, Maryland;</aff>
<aff id="aff3"><sup>3</sup>
Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland; and</aff>
<aff id="aff4"><sup>4</sup>
Center for Biomedical Engineering and Technology, University of Maryland School of Medicine, Baltimore, Maryland</aff>
</contrib-group>
<author-notes><corresp id="cor1">Address for reprint requests and other correspondence: S. M. Thompson, <addr-line>Dept. of Physiology, Univ. of Maryland School of Medicine, 655 W. Baltimore St., Baltimore, MD 21201</addr-line>
(e-mail: <email>sthom003@umaryland.edu</email>
).</corresp>
</author-notes>
<pub-date pub-type="epub"><day>23</day>
<month>4</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="ppub"><day>15</day>
<month>7</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>15</day>
<month>7</month>
<year>2015</year>
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<pmc-comment> PMC Release delay is 12 months and 0 days and was based on the . </pmc-comment>
<volume>112</volume>
<issue>2</issue>
<fpage>263</fpage>
<lpage>275</lpage>
<history><date date-type="received"><day>14</day>
<month>8</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>18</day>
<month>4</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2014 the American Physiological Society</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>American Physiological Society</copyright-holder>
</permissions>
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<abstract><p>GluA2-lacking, calcium-permeable α-amino-3-hydroxy-5-methylisoxazole-4-propionate receptors (AMPARs) have unique properties, but their presence at excitatory synapses in pyramidal cells is controversial. We have tested certain predictions of the model that such receptors are present in CA1 cells and show here that the polyamine spermine, but not philanthotoxin, causes use-dependent inhibition of synaptically evoked excitatory responses in stratum radiatum, but not s. oriens, in cultured and acute hippocampal slices. Stimulation of single dendritic spines by photolytic release of caged glutamate induced an <italic>N</italic>
-methyl-<sc>d</sc>
-aspartate receptor-independent, use- and spermine-sensitive calcium influx only at apical spines in cultured slices. Bath application of glutamate also triggered a spermine-sensitive influx of cobalt into CA1 cell dendrites in s. radiatum. Responses of single apical, but not basal, spines to photostimulation displayed prominent paired-pulse facilitation (PPF) consistent with use-dependent relief of cytoplasmic polyamine block. Responses at apical dendrites were diminished, and PPF was increased, by spermine. Intracellular application of pep2m, which inhibits recycling of GluA2-containing AMPARs, reduced apical spine responses and increased PPF. We conclude that some calcium-permeable, polyamine-sensitive AMPARs, perhaps lacking GluA2 subunits, are present at synapses on apical dendrites of CA1 pyramidal cells, which may allow distinct forms of synaptic plasticity and computation at different sets of excitatory inputs.</p>
</abstract>
<kwd-group><kwd>calcium</kwd>
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<name sortKey="Alger, Bradley E" sort="Alger, Bradley E" uniqKey="Alger B" first="Bradley E." last="Alger">Bradley E. Alger</name>
<name sortKey="Bagal, Ashish A" sort="Bagal, Ashish A" uniqKey="Bagal A" first="Ashish A." last="Bagal">Ashish A. Bagal</name>
<name sortKey="Kao, Joseph P Y" sort="Kao, Joseph P Y" uniqKey="Kao J" first="Joseph P. Y." last="Kao">Joseph P. Y. Kao</name>
<name sortKey="Kao, Joseph P Y" sort="Kao, Joseph P Y" uniqKey="Kao J" first="Joseph P. Y." last="Kao">Joseph P. Y. Kao</name>
<name sortKey="Kao, Joseph P Y" sort="Kao, Joseph P Y" uniqKey="Kao J" first="Joseph P. Y." last="Kao">Joseph P. Y. Kao</name>
<name sortKey="Mattison, Hayley A" sort="Mattison, Hayley A" uniqKey="Mattison H" first="Hayley A." last="Mattison">Hayley A. Mattison</name>
<name sortKey="Mohammadi, Michael" sort="Mohammadi, Michael" uniqKey="Mohammadi M" first="Michael" last="Mohammadi">Michael Mohammadi</name>
<name sortKey="Pulimood, Nisha S" sort="Pulimood, Nisha S" uniqKey="Pulimood N" first="Nisha S." last="Pulimood">Nisha S. Pulimood</name>
<name sortKey="Pulimood, Nisha S" sort="Pulimood, Nisha S" uniqKey="Pulimood N" first="Nisha S." last="Pulimood">Nisha S. Pulimood</name>
<name sortKey="Reich, Christian G" sort="Reich, Christian G" uniqKey="Reich C" first="Christian G." last="Reich">Christian G. Reich</name>
<name sortKey="Thompson, Scott M" sort="Thompson, Scott M" uniqKey="Thompson S" first="Scott M." last="Thompson">Scott M. Thompson</name>
<name sortKey="Thompson, Scott M" sort="Thompson, Scott M" uniqKey="Thompson S" first="Scott M." last="Thompson">Scott M. Thompson</name>
</country>
</tree>
</affiliations>
</record>
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