Hub GABA Neurons Mediate Gamma-frequency Oscillations at Ictal-like Event Onset in the Immature Hippocampus

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2012 Apr 17

PMID 22500630

Citations 32

Authors

Pascale P Quilichini

Michel Le Van Quyen

Anton Ivanov

Dennis A Turner

Aurelie Carabalona

Henri Gozlan

Monique Esclapez

Christophe Bernard

Affiliations

Soon will be listed here.

Abstract

Gamma-frequency oscillations (GFOs, >40 Hz) are a general network signature at seizure onset at all stages of development, with possible deleterious consequences in the immature brain. At early developmental stages, the simultaneous occurrence of GFOs in different brain regions suggests the existence of a long-ranging synchronizing mechanism at seizure onset. Here, we show that hippocamposeptal (HS) neurons, which are GABA long-range projection neurons, are mandatory to drive the firing of hippocampal interneurons in a high-frequency regime at the onset of epileptiform discharges in the intact, immature septohippocampal formation. The synchronized firing of interneurons in turn produces GFOs, which are abolished after the elimination of a small number of HS neurons. Because they provide the necessary fast conduit for pacing large neuronal populations and display intra- and extrahippocampal long-range projections, HS neurons appear to belong to the class of hub cells that play a crucial role in the synchronization of developing networks.

Citing Articles

Regulation of Hippocamposeptal Synaptic Transmission by GABARs Is Altered in 5XFAD Mice in a Sex- and Age-Dependent Manner.

Damborsky J, Yakel J J Mol Neurosci. 2024; 74(3):82.

PMID: 39212758 PMC: 11364565. DOI: 10.1007/s12031-024-02260-0.

Genetic Knockout of TRPM2 Increases Neuronal Excitability of Hippocampal Neurons by Inhibiting Kv7 Channel in Epilepsy.

Ying Y, Gong L, Tao X, Ding J, Chen N, Yao Y Mol Neurobiol. 2022; 59(11):6918-6933.

PMID: 36053438 DOI: 10.1007/s12035-022-02993-2.

Regulation of hippocamposeptal input within the medial septum/diagonal band of Broca.

Damborsky J, Yakel J Neuropharmacology. 2021; 191:108589.

PMID: 33933476 PMC: 8217288. DOI: 10.1016/j.neuropharm.2021.108589.

Dynamic core-periphery structure of information sharing networks in entorhinal cortex and hippocampus.

Pedreschi N, Bernard C, Clawson W, Quilichini P, Barrat A, Battaglia D Netw Neurosci. 2021; 4(3):946-975.

PMID: 33615098 PMC: 7888487. DOI: 10.1162/netn_a_00142.

Phenobarbital, midazolam, bumetanide, and neonatal seizures: The devil is in the details.

Ben-Ari Y, Delpire E Epilepsia. 2021; 62(4):935-940.

PMID: 33534145 PMC: 8035263. DOI: 10.1111/epi.16830.

References

Kohling R, Vreugdenhil M, Bracci E, Jefferys J . Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J Neurosci. 2000; 20(18):6820-9. PMC: 6772821. View

Avoli M, Perreault P . A GABAergic depolarizing potential in the hippocampus disclosed by the convulsant 4-aminopyridine. Brain Res. 1987; 400(1):191-5. DOI: 10.1016/0006-8993(87)90671-8. View

Gulyas A, Hajos N, Katona I, Freund T . Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur J Neurosci. 2003; 17(9):1861-72. DOI: 10.1046/j.1460-9568.2003.02630.x. View

Gozlan H, Ben-Ari Y . Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit. Cereb Cortex. 2003; 13(6):684-92. DOI: 10.1093/cercor/13.6.684. View

Worrell G, Parish L, Cranstoun S, Jonas R, Baltuch G, Litt B . High-frequency oscillations and seizure generation in neocortical epilepsy. Brain. 2004; 127(Pt 7):1496-506. DOI: 10.1093/brain/awh149. View

Dyhrfjeld-Johnsen J, Santhakumar V, Morgan R, Huerta R, Tsimring L, Soltesz I . Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol. 2006; 97(2):1566-87. DOI: 10.1152/jn.00950.2006. View

Michelson H, Wong R . Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science. 1991; 253(5026):1420-3. DOI: 10.1126/science.1654594. View

Jinno S, Klausberger T, Marton L, Dalezios Y, Roberts J, Fuentealba P . Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci. 2007; 27(33):8790-804. PMC: 2270609. DOI: 10.1523/JNEUROSCI.1847-07.2007. View

Whittington M, Traub R . Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 2003; 26(12):676-82. DOI: 10.1016/j.tins.2003.09.016. View

10.

Bonifazi P, GOLDIN M, Picardo M, Jorquera I, Cattani A, Bianconi G . GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science. 2009; 326(5958):1419-24. DOI: 10.1126/science.1175509. View

11.

Tort A, Rotstein H, Dugladze T, Gloveli T, Kopell N . On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc Natl Acad Sci U S A. 2007; 104(33):13490-5. PMC: 1948921. DOI: 10.1073/pnas.0705708104. View

12.

Traub R, Spruston N, Soltesz I, Konnerth A, Whittington M, Jefferys G . Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Prog Neurobiol. 1998; 55(6):563-75. DOI: 10.1016/s0301-0082(98)00020-3. View

13.

Buzsaki G, Geisler C, Henze D, Wang X . Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci. 2004; 27(4):186-93. DOI: 10.1016/j.tins.2004.02.007. View

14.

Oliva Jr A, Jiang M, Lam T, Smith K, Swann J . Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci. 2000; 20(9):3354-68. PMC: 6773106. View

15.

Dzhala V, Kuchibhotla K, Glykys J, Kahle K, Swiercz W, Feng G . Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci. 2010; 30(35):11745-61. PMC: 3070296. DOI: 10.1523/JNEUROSCI.1769-10.2010. View

16.

Steriade M, DEMETRESCU M . Post-primary cortical responses to flashes and their specific potentiation by steady light. Electroencephalogr Clin Neurophysiol. 1966; 20(6):576-90. DOI: 10.1016/0013-4694(66)90022-8. View

17.

Ruusuvuori E, Li H, Huttu K, Palva J, Smirnov S, Rivera C . Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci. 2004; 24(11):2699-707. PMC: 6729533. DOI: 10.1523/JNEUROSCI.5176-03.2004. View

18.

Bartos M, Vida I, Jonas P . Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 2006; 8(1):45-56. DOI: 10.1038/nrn2044. View

19.

Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa J . GABAA, NMDA and AMPA receptors: a developmentally regulated 'ménage à trois'. Trends Neurosci. 1997; 20(11):523-9. DOI: 10.1016/s0166-2236(97)01147-8. View

20.

Traub R, Draguhn A, Whittington M, Baldeweg T, Bibbig A, Buhl E . Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci. 2002; 13(1):1-30. DOI: 10.1515/revneuro.2002.13.1.1. View