GABA-mediated synchronization in the human neocortex: Elevations in extracellular potassium and presynaptic mechanisms

J. Louvel, C. Papatheodoropoulos, A. Siniscalchi, I. Kurcewicz, R. Pumain, B. Devaux, B. Turak, V. Esposito, J. G. Villemeure, M. Avoli

Research output: Contribution to journalArticle

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Abstract

Field potential and extracellular [K+] ([K+]o) recordings were made in the human neocortex in an in vitro slice preparation to study the synchronous activity that occurs in the presence of 4-aminopyridine (50 μM) and ionotropic excitatory amino acid receptor antagonists. Under these experimental conditions, negative or negative-positive field potentials accompanied by rises in [K+]o (up to 4.1 mM from a baseline of 3.25 mM) occurred spontaneously at intervals of 3-27 s. Both field potentials and [K+]o elevations were largest at approximately 1000 μm from the pia. Similar events were induced by neocortical electrical stimuli. Application of medium containing low [Ca2+]/high [Mg2+] (n = 3 slices), antagonism of the GABAA receptor (n = 7) or μ-opioid receptor activation (n = 4) abolished these events. Hence, they represented network, GABA-mediated potentials mainly reflecting the activation of type A receptors following GABA release from interneurons. The GABAB receptor agonist baclofen (10-100 μM, n = 11) reduced and abolished the GABA-mediated potentials (ID50 = 18 μM). Baclofen effects were antagonized by the GABAB receptor antagonist CGP 35348 (0.1-1 mM, n = 6; ID50 = 0.19 mM). CGP 38345 application to control medium increased the amplitude of the GABA-mediated potentials and the concomitant [K+]o rises without modifying their rate of occurrence. The GABA-mediated potentials were not influenced by the broad-spectrum metabotropic glutamate agonist (±)-1-aminocyclopentane-trans-1,3-dicarboxylic acid (100 μM, n = 10), but decreased in rate with the group I receptor agonist (S)-3,5-dihydroxyphenylglycine (10-100 μM, n = 9). Our data indicate that human neocortical networks challenged with 4-aminopyridine generate glutamatergic-independent, GABA-mediated potentials that are modulated by μ-opioid and GABAB receptors presumably located on interneuron terminals. These events are associated with [K+]o elevations that may contribute to interneuron synchronization in the absence of ionotropic excitatory synaptic transmission.

Original languageEnglish
Pages (from-to)803-813
Number of pages11
JournalNeuroscience
Volume105
Issue number4
DOIs
Publication statusPublished - Aug 22 2001

Fingerprint

Neocortex
gamma-Aminobutyric Acid
Potassium
Interneurons
4-Aminopyridine
Opioid Receptors
GABA-A Receptors
GABA-B Receptors
Excitatory Amino Acid Agonists
Excitatory Amino Acid Antagonists
Baclofen
Glutamate Receptors
Synaptic Transmission

Keywords

  • [K]
  • GABA
  • Human cortex
  • Opioid receptors
  • Synchronization

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Louvel, J., Papatheodoropoulos, C., Siniscalchi, A., Kurcewicz, I., Pumain, R., Devaux, B., ... Avoli, M. (2001). GABA-mediated synchronization in the human neocortex: Elevations in extracellular potassium and presynaptic mechanisms. Neuroscience, 105(4), 803-813. https://doi.org/10.1016/S0306-4522(01)00247-0

GABA-mediated synchronization in the human neocortex : Elevations in extracellular potassium and presynaptic mechanisms. / Louvel, J.; Papatheodoropoulos, C.; Siniscalchi, A.; Kurcewicz, I.; Pumain, R.; Devaux, B.; Turak, B.; Esposito, V.; Villemeure, J. G.; Avoli, M.

In: Neuroscience, Vol. 105, No. 4, 22.08.2001, p. 803-813.

Research output: Contribution to journalArticle

Louvel, J, Papatheodoropoulos, C, Siniscalchi, A, Kurcewicz, I, Pumain, R, Devaux, B, Turak, B, Esposito, V, Villemeure, JG & Avoli, M 2001, 'GABA-mediated synchronization in the human neocortex: Elevations in extracellular potassium and presynaptic mechanisms', Neuroscience, vol. 105, no. 4, pp. 803-813. https://doi.org/10.1016/S0306-4522(01)00247-0
Louvel J, Papatheodoropoulos C, Siniscalchi A, Kurcewicz I, Pumain R, Devaux B et al. GABA-mediated synchronization in the human neocortex: Elevations in extracellular potassium and presynaptic mechanisms. Neuroscience. 2001 Aug 22;105(4):803-813. https://doi.org/10.1016/S0306-4522(01)00247-0
Louvel, J. ; Papatheodoropoulos, C. ; Siniscalchi, A. ; Kurcewicz, I. ; Pumain, R. ; Devaux, B. ; Turak, B. ; Esposito, V. ; Villemeure, J. G. ; Avoli, M. / GABA-mediated synchronization in the human neocortex : Elevations in extracellular potassium and presynaptic mechanisms. In: Neuroscience. 2001 ; Vol. 105, No. 4. pp. 803-813.
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