Persistent increase of hippocampal presynaptic axon excitability after repetitive electrical stimulation

Dependence on N-methyl-D-aspartate receptor activity, nitric-oxide synthase, and temperature

B. L. Mcnaughton, J. Shen, G. Rao, T. C. Foster, Carol A Barnes

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40 Citations (Scopus)

Abstract

The electrical excitability of Schaffer collateral axons and/or terminals was studied in hippocampal slices by monitoring single, CA3 pyramidal neurons activated antidromically from CA1 stratum radiatum. At 22°C, weak, repetitive stimulation with as few as 10 impulses at 2 Hz led to a robust lowering of the antidromic activation threshold that lasted >30 min. The effect was completely absent at 32°C and was blocked by both the N-methyl- D-aspartate receptor antagonist, 2-amino-5-phosphonovalerate and the inhibitor of nitric-oxide synthase, L-nitroarginine methyl ester. Such threshold lowering would alter the variance of synaptic responses from axons stimulated in the variable excitation region of their input-output functions. These results thus raise important doubts about the interpretation of experiments in which the so-called minimal-stimulation method has been used at reduced temperature to infer changes in quantal transmission during hippocampal long-term potentiation. In the present experiments, no changes were observed in the estimate of excitatory postsynaptic potential quantal content in long-term potentiation experiments at either temperature, which could not be accounted for by an artifactual, temperature-dependent change in the responsiveness of presynaptic axons.

Original languageEnglish (US)
Pages (from-to)4830-4834
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume91
Issue number11
DOIs
StatePublished - May 24 1994

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N-Methyl-D-Aspartate Receptors
Nitric Oxide Synthase
Electric Stimulation
Axons
Long-Term Potentiation
Temperature
2-Amino-5-phosphonovalerate
Hippocampal CA1 Region
Pyramidal Cells
Excitatory Postsynaptic Potentials
Nitroarginine
Presynaptic Terminals
Hippocampus
Esters

Keywords

  • long-term potentiation
  • neurophysiology
  • quantal analysis

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

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abstract = "The electrical excitability of Schaffer collateral axons and/or terminals was studied in hippocampal slices by monitoring single, CA3 pyramidal neurons activated antidromically from CA1 stratum radiatum. At 22°C, weak, repetitive stimulation with as few as 10 impulses at 2 Hz led to a robust lowering of the antidromic activation threshold that lasted >30 min. The effect was completely absent at 32°C and was blocked by both the N-methyl- D-aspartate receptor antagonist, 2-amino-5-phosphonovalerate and the inhibitor of nitric-oxide synthase, L-nitroarginine methyl ester. Such threshold lowering would alter the variance of synaptic responses from axons stimulated in the variable excitation region of their input-output functions. These results thus raise important doubts about the interpretation of experiments in which the so-called minimal-stimulation method has been used at reduced temperature to infer changes in quantal transmission during hippocampal long-term potentiation. In the present experiments, no changes were observed in the estimate of excitatory postsynaptic potential quantal content in long-term potentiation experiments at either temperature, which could not be accounted for by an artifactual, temperature-dependent change in the responsiveness of presynaptic axons.",
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T2 - Dependence on N-methyl-D-aspartate receptor activity, nitric-oxide synthase, and temperature

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AU - Shen, J.

AU - Rao, G.

AU - Foster, T. C.

AU - Barnes, Carol A

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N2 - The electrical excitability of Schaffer collateral axons and/or terminals was studied in hippocampal slices by monitoring single, CA3 pyramidal neurons activated antidromically from CA1 stratum radiatum. At 22°C, weak, repetitive stimulation with as few as 10 impulses at 2 Hz led to a robust lowering of the antidromic activation threshold that lasted >30 min. The effect was completely absent at 32°C and was blocked by both the N-methyl- D-aspartate receptor antagonist, 2-amino-5-phosphonovalerate and the inhibitor of nitric-oxide synthase, L-nitroarginine methyl ester. Such threshold lowering would alter the variance of synaptic responses from axons stimulated in the variable excitation region of their input-output functions. These results thus raise important doubts about the interpretation of experiments in which the so-called minimal-stimulation method has been used at reduced temperature to infer changes in quantal transmission during hippocampal long-term potentiation. In the present experiments, no changes were observed in the estimate of excitatory postsynaptic potential quantal content in long-term potentiation experiments at either temperature, which could not be accounted for by an artifactual, temperature-dependent change in the responsiveness of presynaptic axons.

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