Literature DB >> 24344272

Tonic GABAA conductance bidirectionally controls interneuron firing pattern and synchronization in the CA3 hippocampal network.

Ivan Pavlov1, Leonid P Savtchenko, Inseon Song, Jaeyeon Koo, Alexey Pimashkin, Dmitri A Rusakov, Alexey Semyanov.   

Abstract

The spiking output of interneurons is key for rhythm generation in the brain. However, what controls interneuronal firing remains incompletely understood. Here we combine dynamic clamp experiments with neural network simulations to understand how tonic GABAA conductance regulates the firing pattern of CA3 interneurons. In baseline conditions, tonic GABAA depolarizes these cells, thus exerting an excitatory action while also reducing the excitatory postsynaptic potential (EPSP) amplitude through shunting. As a result, the emergence of weak tonic GABAA conductance transforms the interneuron firing pattern driven by individual EPSPs into a more regular spiking mode determined by the cell intrinsic properties. The increased regularity of spiking parallels stronger synchronization of the local network. With further increases in tonic GABAA conductance the shunting inhibition starts to dominate over excitatory actions and thus moderates interneuronal firing. The remaining spikes tend to follow the timing of suprathreshold EPSPs and thus become less regular again. The latter parallels a weakening in network synchronization. Thus, our observations suggest that tonic GABAA conductance can bidirectionally control brain rhythms through changes in the excitability of interneurons and in the temporal structure of their firing patterns.

Entities:  

Keywords:  extrasynaptic signaling; oscillations; tonic conductance

Mesh:

Substances:

Year:  2013        PMID: 24344272      PMCID: PMC3890854          DOI: 10.1073/pnas.1308388110

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  26 in total

Review 1.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks.

Authors:  Marlene Bartos; Imre Vida; Peter Jonas
Journal:  Nat Rev Neurosci       Date:  2007-01       Impact factor: 34.870

Review 2.  Role of GABAergic inhibition in hippocampal network oscillations.

Authors:  Edward O Mann; Ole Paulsen
Journal:  Trends Neurosci       Date:  2007-05-25       Impact factor: 13.837

3.  Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model.

Authors:  X J Wang; G Buzsáki
Journal:  J Neurosci       Date:  1996-10-15       Impact factor: 6.167

4.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro.

Authors:  A Fisahn; F G Pike; E H Buhl; O Paulsen
Journal:  Nature       Date:  1998-07-09       Impact factor: 49.962

5.  Properties of gamma frequency oscillatory activity induced in hippocampal slices from the adult GAD67-GFP (Deltaneo) mouse.

Authors:  Cheng B Lu; Yuchio Yanagawa; Zaineb Henderson
Journal:  Brain Res       Date:  2010-02-06       Impact factor: 3.252

6.  The interaction between vigabatrin and diazepam on the electroencephalogram during active behaviour in rats: an isobolic analysis.

Authors:  Brigitte M Bouwman; Erica Heesen; Clementina M van Rijn
Journal:  Eur J Pharmacol       Date:  2004-07-14       Impact factor: 4.432

7.  Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons.

Authors:  Edward O Mann; Istvan Mody
Journal:  Nat Neurosci       Date:  2009-12-20       Impact factor: 24.884

8.  Excitatory synaptic responses mediated by GABAA receptors in the hippocampus.

Authors:  H B Michelson; R K Wong
Journal:  Science       Date:  1991-09-20       Impact factor: 47.728

9.  Tonic excitation or inhibition is set by GABA(A) conductance in hippocampal interneurons.

Authors:  Inseon Song; Leonid Savtchenko; Alexey Semyanov
Journal:  Nat Commun       Date:  2011-07-05       Impact factor: 14.919

10.  Different transporter systems regulate extracellular GABA from vesicular and non-vesicular sources.

Authors:  Inseon Song; Kirill Volynski; Tanja Brenner; Yuri Ushkaryov; Matthew Walker; Alexey Semyanov
Journal:  Front Cell Neurosci       Date:  2013-03-13       Impact factor: 5.505

View more
  24 in total

1.  In vitro gamma oscillations following partial and complete ablation of δ subunit-containing GABAA receptors from parvalbumin interneurons.

Authors:  Isabella Ferando; Istvan Mody
Journal:  Neuropharmacology       Date:  2014-09-28       Impact factor: 5.250

2.  Tonic regulation of stationary asynchronous firing of a neural network.

Authors:  D A Adamchik; V B Kazantsev
Journal:  J Comput Neurosci       Date:  2017-05-16       Impact factor: 1.621

3.  Tonic GABAA Conductance Favors Spike-Timing-Dependent over Theta-Burst-Induced Long-Term Potentiation in the Hippocampus.

Authors:  Yulia Dembitskaya; Yu-Wei Wu; Alexey Semyanov
Journal:  J Neurosci       Date:  2020-04-23       Impact factor: 6.167

4.  Sex Differences in the Alcohol-Mediated Modulation of BLA Network States.

Authors:  Alyssa DiLeo; Pantelis Antonoudiou; Spencer Ha; Jamie L Maguire
Journal:  eNeuro       Date:  2022-07-08

5.  Age-related changes in tonic activation of presynaptic versus extrasynaptic γ-amniobutyric acid type B receptors in rat medial prefrontal cortex.

Authors:  Haley E Carpenter; Kyle B Kelly; Jennifer L Bizon; Charles J Frazier
Journal:  Neurobiol Aging       Date:  2016-05-21       Impact factor: 4.673

6.  GABA-mediated tonic inhibition differentially modulates gain in functional subtypes of cortical interneurons.

Authors:  Alexander Bryson; Robert John Hatch; Bas-Jan Zandt; Christian Rossert; Samuel F Berkovic; Christopher A Reid; David B Grayden; Sean L Hill; Steven Petrou
Journal:  Proc Natl Acad Sci U S A       Date:  2020-01-23       Impact factor: 11.205

7.  Allopregnanolone Mediates Affective Switching Through Modulation of Oscillatory States in the Basolateral Amygdala.

Authors:  Pantelis Antonoudiou; Phillip L W Colmers; Najah L Walton; Grant L Weiss; Anne C Smith; David P Nguyen; Mike Lewis; Michael C Quirk; Lea Barros; Laverne C Melon; Jamie L Maguire
Journal:  Biol Psychiatry       Date:  2021-07-27       Impact factor: 13.382

8.  Diurnal properties of tonic and synaptic GABAA receptor-mediated currents in suprachiasmatic nucleus neurons.

Authors:  Michael Moldavan; Olga Cravetchi; Charles N Allen
Journal:  J Neurophysiol       Date:  2021-07-14       Impact factor: 2.974

9.  Ectopic Expression of α6 and δ GABAA Receptor Subunits in Hilar Somatostatin Neurons Increases Tonic Inhibition and Alters Network Activity in the Dentate Gyrus.

Authors:  Xiaoping Tong; Zechun Peng; Nianhui Zhang; Yliana Cetina; Christine S Huang; Martin Wallner; Thomas S Otis; Carolyn R Houser
Journal:  J Neurosci       Date:  2015-12-09       Impact factor: 6.167

10.  A synthetic synaptic organizer protein restores glutamatergic neuronal circuits.

Authors:  Kunimichi Suzuki; Jonathan Elegheert; Inseon Song; Hiroyuki Sasakura; Oleg Senkov; Keiko Matsuda; Wataru Kakegawa; Amber J Clayton; Veronica T Chang; Maura Ferrer-Ferrer; Eriko Miura; Rahul Kaushik; Masashi Ikeno; Yuki Morioka; Yuka Takeuchi; Tatsuya Shimada; Shintaro Otsuka; Stoyan Stoyanov; Masahiko Watanabe; Kosei Takeuchi; Alexander Dityatev; A Radu Aricescu; Michisuke Yuzaki
Journal:  Science       Date:  2020-08-28       Impact factor: 63.714

View more

北京卡尤迪生物科技股份有限公司 © 2022-2023.