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Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo

Nature Neuroscience volume 7, pages 41–47 (2004)Cite this article

A Corrigendum to this article was published on 01 July 2006

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Abstract

Behavior-contingent network oscillations bring about transient, functionally coherent neuronal assemblies in the cerebral cortex, including the hippocampus. Inhibitory input on and close to the soma is believed to phase intrinsic oscillations and output of pyramidal cells, but the function of GABA release to pyramidal cell dendrites remains unknown. We recorded the oscillation-locked spike timing of identified bistratified interneurons in rats. These cells mainly innervated small dendritic shafts of pyramidal cells co-aligned with the glutamatergic Schaffer collateral/commissural input. During theta oscillations, bistratified cells fired at a phase when, on average, pyramidal cell dendrites are most hyperpolarized. Interneurons targeting the perisomatic domain discharge at an earlier phase. During sharp wave–associated ripples, bistratified cells fired with high frequency and in-phase with basket cells, on average 1–2 ms after the discharges in pyramidal cell somata and dendrites. Our results indicate that bistratified cells rhythmically modulate glutamatergic input to the dendrites of pyramidal cells to actively promote the precise input/output transformation during network oscillations.

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Figure 1: Firing pattern and labeling of a bistratified cell (T92a) in the hippocampus in vivo.
Figure 2: Fluorescence micrographs showing bistratified cells expressing immunoreactivity for parvalbumin, somatostatin, neuropeptide Y and the α1 subunit of the GABAA receptor.
Figure 3: Synaptic targets of bistratified cells.
Figure 4: The firing of an identified bistratified cell (T104b) is intimately related to ongoing network oscillations.
Figure 5: Comparison of the firing patterns of bistratified cells and basket cells during theta oscillations, whole ripple episodes and single ripple cycles (basket cell data for a and b are taken from ref. 9 with permission).

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  • 20 June 2006

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Notes

  1. *NOTE: In the version of this article initially published, the dose of urethane anesthesia in the Methods section was incorrect. The correct dose should be 1.25 g per kg of body weight. The error has been corrected in the PDF version of the article. The authors regret the error.

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Acknowledgements

We thank P. Cobden, B. Micklem and L. Norman for technical assistance, S. Gray and G. Horseman from Cambridge Electronic Design for computing assistance, Y. Dalezios for help with statistics, P. Szucs for help with reconstructions of cells and G. Buzsaki, J. Csicsvari, M. Hausser and G. Tamas for critically reading an earlier version of the manuscript. This work was supported in part by grant P16637-B02 from the Austrian Science Fund.

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  1. Department of Pharmacology, MRC Anatomical Neuropharmacology Unit, Oxford University, Mansfield Road, Oxford, OX1 3TH, UK

    Thomas Klausberger, László F Márton, Agnes Baude, J David B Roberts, Peter J Magill & Peter Somogyi

  2. CNRS UMR 6150, Faculté de Médecine, IFR Jean Roche, Bd. Pierre Dramard, Marseille, 13916 Cedex 20, France

    Agnes Baude

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Correspondence to Thomas Klausberger.

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Klausberger, T., Márton, L., Baude, A. et al. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7, 41–47 (2004). https://doi.org/10.1038/nn1159

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