Synchronization of rat hippocampal neurons in the absence of excitatory amino acid-mediated transmission

Massimo Avoli, Takeki Nagao, Rüdiger Köhling, Anne Lücke, Donatella Mattia

Research output: Contribution to journalArticle

Abstract

Extracellular and intracellular recordings and measurements of extracellular K+ concentration ([K+](o)) were performed in the adult rat hippocampus in an in vitro slice preparation. Excitatory amino acid receptor antagonists, as well as the K+-channel blockers 4-aminopyridine (4AP, 50 μM) and/or tetraethylammonium (TEA, 5 mM), were added to the bath. Synchronous, negative-going field potentials were recorded in the CA3 stratum radiatum during application of 4AP and excitatory amino acid receptor antagonists. Each of these events was associated with an intracellular long-lasting depolarization and a concomitant rise in [K+](o) that attained peak values of 4.3 ± 0.1 mM (mean ± S.E.M., n = 6 slices) and lasted 29 ± 3 s. These field potentials were still recorded in CA3 stratum radiatum after addition of TEA. Under these conditions, prolonged field potentials (40.2 ± 4.5 s, n = 18) characterized by a prominent positive component; discharge of population spikes also occurred. [K+](o) increases associated with these prolonged field-potential discharges had a considerable variability in magnitude (peak value = 3.8-14.1 mM, 6.1 ± 0.7 mM, n = 5) and duration (14-210 s; 48 ± 13 s, n = 5). In 8% of the cases spreading depression-like episodes were observed. [K+](o) increases during spreading depression-like episodes attained peak values of 11-27 mM (22.8 ± 0.2 mM, n = 2) and had a duration of 160-396 s (244 ± 29 s, n = 2). all types of synchronous activity were abolished by the GABA(A)-receptor antagonist bicuculline methiodide (10 μM) (n = 11). A similar effect was obtained by applying Ca2+-free/high-Mg2+ medium (n = 5). Simultaneous field-potential recordings in CA3, CA1, dentate area and subiculum demonstrated that negative-going potentials and prolonged field-potential discharges, occurred in all areas in a synchronous fashion. Spreading depression-like episodes were more frequently recorded in the CA1 than in the CA3 area and were not seen in the subiculum or dentate area. These experiments indicate that a glutamatergic-independent, synchronous GABA-mediated potential which is elicited by 4APin the adult rat hippocampus continues to occur in the presence of TEA. In addition, concomitant application of these K+ channel blockers induces a novel type of prolonged field-potential discharge as well as spreading depression-like episodes. Since all synchronous potentials (including-spreading depression-like episodes) were abolished by bicuculline methiodide, we conclude that their occurrence is presumably dependent upon the post-synaptic activation of GABA(A) receptors located on neuronal and glial elements. As excitatory synaptic transmission was nominally blocked under our experimental conditions, we also propose that rises in [K+](o) and consequent redistribution processes are per se sufficient to make all types of synchronous activity propagate.

Original languageEnglish
Pages (from-to)188-196
Number of pages9
JournalBrain Research
Volume735
Issue number2
DOIs
Publication statusPublished - Oct 7 1996

Fingerprint

Excitatory Amino Acids
Hippocampus
Hippocampal CA3 Region
Neurons
Excitatory Amino Acid Antagonists
Glutamate Receptors
GABA-A Receptor Antagonists
4-Aminopyridine
Tetraethylammonium
GABA-A Receptors
Baths
Synaptic Transmission
Neuroglia
gamma-Aminobutyric Acid
Population
bicuculline methiodide

Keywords

  • Excitatory amino acid
  • Hippocampus
  • K concentration increase
  • K-channel blocker
  • Synchronization

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Synchronization of rat hippocampal neurons in the absence of excitatory amino acid-mediated transmission. / Avoli, Massimo; Nagao, Takeki; Köhling, Rüdiger; Lücke, Anne; Mattia, Donatella.

In: Brain Research, Vol. 735, No. 2, 07.10.1996, p. 188-196.

Research output: Contribution to journalArticle

Avoli, Massimo ; Nagao, Takeki ; Köhling, Rüdiger ; Lücke, Anne ; Mattia, Donatella. / Synchronization of rat hippocampal neurons in the absence of excitatory amino acid-mediated transmission. In: Brain Research. 1996 ; Vol. 735, No. 2. pp. 188-196.
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N2 - Extracellular and intracellular recordings and measurements of extracellular K+ concentration ([K+](o)) were performed in the adult rat hippocampus in an in vitro slice preparation. Excitatory amino acid receptor antagonists, as well as the K+-channel blockers 4-aminopyridine (4AP, 50 μM) and/or tetraethylammonium (TEA, 5 mM), were added to the bath. Synchronous, negative-going field potentials were recorded in the CA3 stratum radiatum during application of 4AP and excitatory amino acid receptor antagonists. Each of these events was associated with an intracellular long-lasting depolarization and a concomitant rise in [K+](o) that attained peak values of 4.3 ± 0.1 mM (mean ± S.E.M., n = 6 slices) and lasted 29 ± 3 s. These field potentials were still recorded in CA3 stratum radiatum after addition of TEA. Under these conditions, prolonged field potentials (40.2 ± 4.5 s, n = 18) characterized by a prominent positive component; discharge of population spikes also occurred. [K+](o) increases associated with these prolonged field-potential discharges had a considerable variability in magnitude (peak value = 3.8-14.1 mM, 6.1 ± 0.7 mM, n = 5) and duration (14-210 s; 48 ± 13 s, n = 5). In 8% of the cases spreading depression-like episodes were observed. [K+](o) increases during spreading depression-like episodes attained peak values of 11-27 mM (22.8 ± 0.2 mM, n = 2) and had a duration of 160-396 s (244 ± 29 s, n = 2). all types of synchronous activity were abolished by the GABA(A)-receptor antagonist bicuculline methiodide (10 μM) (n = 11). A similar effect was obtained by applying Ca2+-free/high-Mg2+ medium (n = 5). Simultaneous field-potential recordings in CA3, CA1, dentate area and subiculum demonstrated that negative-going potentials and prolonged field-potential discharges, occurred in all areas in a synchronous fashion. Spreading depression-like episodes were more frequently recorded in the CA1 than in the CA3 area and were not seen in the subiculum or dentate area. These experiments indicate that a glutamatergic-independent, synchronous GABA-mediated potential which is elicited by 4APin the adult rat hippocampus continues to occur in the presence of TEA. In addition, concomitant application of these K+ channel blockers induces a novel type of prolonged field-potential discharge as well as spreading depression-like episodes. Since all synchronous potentials (including-spreading depression-like episodes) were abolished by bicuculline methiodide, we conclude that their occurrence is presumably dependent upon the post-synaptic activation of GABA(A) receptors located on neuronal and glial elements. As excitatory synaptic transmission was nominally blocked under our experimental conditions, we also propose that rises in [K+](o) and consequent redistribution processes are per se sufficient to make all types of synchronous activity propagate.

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