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Research Article

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, and Andreas Draguhn
PNAS first published July 18, 2011; https://doi.org/10.1073/pnas.1103546108
Florian Bähner
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Elisa K. Weiss
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Gunnar Birke
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Nikolaus Maier
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Dietmar Schmitz
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Uwe Rudolph
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Michael Frotscher
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Roger D. Traub
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Martin Both
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Andreas Draguhn
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  • For correspondence: andreas.draguhn@physiologie.uni-heidelberg.de
  1. Edited by* N. Kopell, Boston University, Boston, MA, and approved June 20, 2011 (received for review March 4, 2011)

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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. GABAA 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.

  • antidromic action potentials
  • CA1 pyramidal cells
  • interneurons
  • ripples

Footnotes

  • ↵1M.B. and A.D. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. E-mail: andreas.draguhn{at}physiologie.uni-heidelberg.de.
  • Author contributions: F.B., D.S., R.D.T., and A.D. designed research; F.B., E.K.W., G.B., N.M., M.F., R.D.T., and M.B. performed research; U.R. contributed new reagents/analytic tools; F.B., E.K.W., G.B., N.M., D.S., M.F., R.D.T., and M.B. analyzed data; and F.B., R.D.T., M.B., and A.D. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1103546108/-/DCSupplemental.

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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
Proceedings of the National Academy of Sciences Jul 2011, 201103546; DOI: 10.1073/pnas.1103546108

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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
Proceedings of the National Academy of Sciences Jul 2011, 201103546; DOI: 10.1073/pnas.1103546108
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Proceedings of the National Academy of Sciences: 118 (3)
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