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Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo

Nature volume 421, pages 844–848 (2003)Cite this article

A Corrigendum to this article was published on 15 June 2006

Abstract

Neural-network oscillations at distinct frequencies have been implicated in the encoding, consolidation and retrieval of information in the hippocampus. Some GABA (γ-aminobutyric acid)-containing interneurons fire phase-locked to theta oscillations (4–8 Hz) or to sharp-wave-associated ripple oscillations (120–200 Hz), which represent different behavioural states1,2,3,4,5,6. Interneurons also entrain pyramidal cells in vitro7. The large diversity of interneurons8,9,10 poses the question of whether they have specific roles in shaping distinct network activities in vivo. Here we report that three distinct interneuron types—basket, axo-axonic and oriens–lacunosum-moleculare cells—visualized and defined by synaptic connectivity as well as by neurochemical markers, contribute differentially to theta and ripple oscillations in anaesthetized rats. The firing patterns of individual cells of the same class are remarkably stereotyped and provide unique signatures for each class. We conclude that the diversity of interneurons, innervating distinct domains of pyramidal cells11, emerged to coordinate the activity of pyramidal cells in a temporally distinct and brain-state-dependent manner.

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Figure 1: Firing patterns of a parvalbumin-positive basket cell (T44b) in vivo.
Figure 2: Firing patterns of a parvalbumin-positive axo-axonic cell (T76b) in vivo.
Figure 3: Firing patterns of an O-LM cell (T64a) in vivo.
Figure 4: Distinct interneuron classes generate different firing patterns during theta and ripple oscillations in vivo.

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Acknowledgements

We thank G. Horseman and S. Gray from Cambridge Electronic Design, and P. Jays and L. Norman for technical assistance. We thank Z. Nusser, G. Tamas and J. Csicsvari for critically reading an earlier version of the manuscript, and Y. Dalezios for help with the statistics. T.K. was supported by an Erwin Schroedinger Fellowship from the Austrian Science Fund during part of this study; G.B. was supported by the National Institutes of Health.

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Authors and Affiliations

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

    Thomas Klausberger, Peter J. Magill, László F. Márton, J. David B. Roberts, Philip M. Cobden & Peter Somogyi

  2. Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey, 07102, USA

    György Buzsáki

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  1. Thomas Klausberger
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Correspondence to Thomas Klausberger.

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Klausberger, T., Magill, P., Márton, L. et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844–848 (2003). https://doi.org/10.1038/nature01374

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