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Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling

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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Figure 1: Measurement of network PRCs in the hippocampal CA3 subfield.
Figure 2: A neural mass model reproduces rephasing behavior.
Figure 3: Population data and model behavior.
Figure 4
Figure 5: Optogenetic rephasing.
Figure 6: Entrainment demonstrated with modulated light ramps.

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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

Authors and Affiliations

Authors

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.

Corresponding authors

Correspondence to Thomas Akam or Dimitri M Kullmann.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 2679 kb)

Supplementary Video 1a

Rephasing Animations: Weak alveus stimulation (MOV 2747 kb)

Supplementary Video 1b

Rephasing Animations: Strong alveus stimulation (MOV 2554 kb)

Supplementary Video 1c

Rephasing Animations: Weak dentate stimulation (MOV 2748 kb)

Supplementary Video 1d

Rephasing Animations: Weak dentate stimulation (MOV 2393 kb)

Supplementary Video 2a

Intracellular current trajectory animations: alveus stimulation (MOV 459 kb)

Supplementary Video 2b

Intracellular current trajectory animations: dentate stimulation (MOV 1503 kb)

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Akam, T., Oren, I., Mantoan, L. et al. Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling. Nat Neurosci 15, 763–768 (2012). https://doi.org/10.1038/nn.3081

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