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Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling

Nature Neuroscience volume 15, pages 763768 (2012) | Download Citation

Abstract

Gamma oscillations in the dentate gyrus and hippocampal CA3 show variable coherence in vivo, but the mechanisms and relevance for information flow are unknown. We found that carbachol-induced oscillations in rat CA3 have biphasic phase-response curves, consistent with the ability to couple with oscillations in afferent projections. Differences in response to stimulation of either the intrinsic feedback circuit or the dentate gyrus were well described by varying an impulse vector in a two-dimensional dynamical system, representing the relative input to excitatory and inhibitory neurons. Responses to sinusoidally modulated optogenetic stimulation confirmed that the CA3 network oscillation can entrain to periodic inputs, with a steep dependence of entrainment phase on input frequency. CA3 oscillations are therefore suited to coupling with oscillations in the dentate gyrus over a broad range of frequencies.

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Acknowledgements

We are grateful to N. Burgess for comments on the manuscript and to K. Deisseroth for the ChR2 plasmid. This work was supported by the Wellcome Trust, the European Research Council, the Brain Research Trust and the Guarantors of Brain.

Author information

Author notes

    • Thomas Akam
    •  & Emily Ferenczi

    Present addresses: Champalimaud Centre, Lisbon, Portugal (T.A.) and Neurosciences Program, Stanford University, Stanford, California, USA (E.F.).

Affiliations

  1. University College London Institute of Neurology, University College London, London, UK.

    • Thomas Akam
    • , Iris Oren
    • , Laura Mantoan
    • , Emily Ferenczi
    •  & Dimitri M Kullmann

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Contributions

T.A. and D.M.K. designed the experiments and wrote the manuscript. T.A. and E.F. conducted the electrical stimulation rephasing experiments. I.O. conducted the intracellular recording experiments. T.A. and L.M. conducted the optogenetic experiments. T.A. performed the computational modeling and data analysis.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Thomas Akam or Dimitri M Kullmann.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–4

Videos

  1. 1.

    Supplementary Video 1a

    Rephasing Animations: Weak alveus stimulation

  2. 2.

    Supplementary Video 1b

    Rephasing Animations: Strong alveus stimulation

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    Supplementary Video 1c

    Rephasing Animations: Weak dentate stimulation

  4. 4.

    Supplementary Video 1d

    Rephasing Animations: Weak dentate stimulation

  5. 5.

    Supplementary Video 2a

    Intracellular current trajectory animations: alveus stimulation

  6. 6.

    Supplementary Video 2b

    Intracellular current trajectory animations: dentate stimulation

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DOI

https://doi.org/10.1038/nn.3081

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