Rapid Desynchronization of an Electrically Coupled Interneuron Network with Sparse Excitatory Synaptic Input

Koen Vervaeke, Andrea LÖrincz, Padraig Gleeson, Matteo Farinella, Z. Nusser, R. Angus Silver

Research output: Contribution to journalArticle

128 Citations (Scopus)

Abstract

Electrical synapses between interneurons contribute to synchronized firing and network oscillations in the brain. However, little is known about how such networks respond to excitatory synaptic input. To investigate this, we studied electrically coupled Golgi cells (GoC) in the cerebellar input layer. We show with immunohistochemistry, electron microscopy, and electrophysiology that Connexin-36 is necessary for functional gap junctions (GJs) between GoC dendrites. In the absence of coincident synaptic input, GoCs synchronize their firing. In contrast, sparse, coincident mossy fiber input triggered a mixture of excitation and inhibition of GoC firing and spike desynchronization. Inhibition is caused by propagation of the spike afterhyperpolarization through GJs. This triggers network desynchronization because heterogeneous coupling to surrounding cells causes spike-phase dispersion. Detailed network models predict that desynchronization is robust, local, and dependent on synaptic input properties. Our results show that GJ coupling can be inhibitory and either promote network synchronization or trigger rapid network desynchronization depending on the synaptic input.

Original languageEnglish
Pages (from-to)435-451
Number of pages17
JournalNeuron
Volume67
Issue number3
DOIs
Publication statusPublished - Aug 2010

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Interneurons
Gap Junctions
Electrical Synapses
Electrophysiology
Dendrites
Electron Microscopy
Immunohistochemistry
Brain

Keywords

  • Molneuro
  • Signaling
  • Sysneuro

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Rapid Desynchronization of an Electrically Coupled Interneuron Network with Sparse Excitatory Synaptic Input. / Vervaeke, Koen; LÖrincz, Andrea; Gleeson, Padraig; Farinella, Matteo; Nusser, Z.; Silver, R. Angus.

In: Neuron, Vol. 67, No. 3, 08.2010, p. 435-451.

Research output: Contribution to journalArticle

Vervaeke, Koen ; LÖrincz, Andrea ; Gleeson, Padraig ; Farinella, Matteo ; Nusser, Z. ; Silver, R. Angus. / Rapid Desynchronization of an Electrically Coupled Interneuron Network with Sparse Excitatory Synaptic Input. In: Neuron. 2010 ; Vol. 67, No. 3. pp. 435-451.
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