Cellular correlate of assembly formation in oscillating hippocampal networks in vitro

Florian Bähner, Elisa K. Weiss, Gunnar Birke, Nikolaus Maier, Dietmar Schmitz, Uwe Rudolph, Michael Frotscher, Roger D. Traub, Martin Both, Andreas Draguhn

Research output: Contribution to journalArticlepeer-review

Abstract

Neurons form transiently stable assemblies that may underlie cognitive functions, including memory formation. In most brain regions, coherent activity is organized by network oscillations that involve sparse firing within a well-defined minority of cells. Despite extensive work on the underlying cellular mechanisms, a fundamental question remains unsolved: how are participating neurons distinguished from the majority of nonparticipators? We used physiological and modeling techniques to analyze neuronal activity in mouse hippocampal slices during spontaneously occurring high-frequency network oscillations. Network-entrained action potentials were exclusively observed in a defined subset of pyramidal cells, yielding a strict distinction between participating and nonparticipating neurons. These spikes had unique properties, because they were generated in the axon without prior depolarization of the soma. GABA A receptors had a dual role in pyramidal cell recruitment. First, the sparse occurrence of entrained spikes was accomplished by intense perisomatic inhibition. Second, antidromic spike generation was facilitated by tonic effects of GABA in remote axonal compartments. Ectopic spike generation together with strong somatodendritic inhibition may provide a cellular mechanism for the definition of oscillating assemblies.

Original languageEnglish (US)
Pages (from-to)E607-E616
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number35
DOIs
StatePublished - Aug 30 2011
Externally publishedYes

Keywords

  • Antidromic action potentials
  • CA1 pyramidal cells
  • Interneurons
  • Ripples

ASJC Scopus subject areas

  • General

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