Voltage-controlled plasticity at GluR2-deficient synapses onto hippocampal interneurons

Fernanda Laezza, Raymond Dingledine

Research output: Contribution to journalArticle

39 Citations (Scopus)

Abstract

High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum intemeurons expressing GluR2-lacking, Ca 2+-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-D-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at -30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to -70 mV, by strong depolarization to 0 mV, by D-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca 2+ chelator bis-(o-arninophenoxy)-N,N,N′,N′-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.

Original languageEnglish (US)
Pages (from-to)3575-3581
Number of pages7
JournalJournal of Neurophysiology
Volume92
Issue number6
DOIs
StatePublished - Dec 2004
Externally publishedYes

Fingerprint

Interneurons
N-Methyl-D-Aspartate Receptors
Synapses
AMPA Receptors
Membrane Potentials
2-Amino-5-phosphonovalerate
Long-Term Potentiation
Pyramidal Cells
Chelating Agents
Synaptic Transmission
Injections
Acids

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Voltage-controlled plasticity at GluR2-deficient synapses onto hippocampal interneurons. / Laezza, Fernanda; Dingledine, Raymond.

In: Journal of Neurophysiology, Vol. 92, No. 6, 12.2004, p. 3575-3581.

Research output: Contribution to journalArticle

@article{afd9840c0a4c40bfbf3b34699d036d41,
title = "Voltage-controlled plasticity at GluR2-deficient synapses onto hippocampal interneurons",
abstract = "High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum intemeurons expressing GluR2-lacking, Ca 2+-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-D-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at -30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to -70 mV, by strong depolarization to 0 mV, by D-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca 2+ chelator bis-(o-arninophenoxy)-N,N,N′,N′-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.",
author = "Fernanda Laezza and Raymond Dingledine",
year = "2004",
month = "12",
doi = "10.1152/jn.00425.2004",
language = "English (US)",
volume = "92",
pages = "3575--3581",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "6",

}

TY - JOUR

T1 - Voltage-controlled plasticity at GluR2-deficient synapses onto hippocampal interneurons

AU - Laezza, Fernanda

AU - Dingledine, Raymond

PY - 2004/12

Y1 - 2004/12

N2 - High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum intemeurons expressing GluR2-lacking, Ca 2+-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-D-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at -30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to -70 mV, by strong depolarization to 0 mV, by D-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca 2+ chelator bis-(o-arninophenoxy)-N,N,N′,N′-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.

AB - High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum intemeurons expressing GluR2-lacking, Ca 2+-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-D-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at -30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to -70 mV, by strong depolarization to 0 mV, by D-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca 2+ chelator bis-(o-arninophenoxy)-N,N,N′,N′-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.

UR - http://www.scopus.com/inward/record.url?scp=8644260773&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=8644260773&partnerID=8YFLogxK

U2 - 10.1152/jn.00425.2004

DO - 10.1152/jn.00425.2004

M3 - Article

VL - 92

SP - 3575

EP - 3581

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 6

ER -