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Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons

Nature Neuroscience 16, 1812–1820 (2013) | Download Citation

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Abstract

Timing is a crucial aspect of synaptic integration. For pyramidal neurons that integrate thousands of synaptic inputs spread across hundreds of microns, it is thus a challenge to maintain the timing of incoming inputs at the axo-somatic integration site. Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of hyperpolarization-activated cation-nonselective (HCN) channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma. Using simultaneous multi-site whole-cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree. While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a new mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

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Acknowledgements

We thank R. Chitwood, N. Dembrow, R. Gray and R. Narayanan for helpful discussions during the course of this study. We also thank members of the Johnston laboratory and L.L. Colgin for comments on earlier versions of this manuscript. This work was supported by grant MH 048432 from US National Institutes of Health to D.J.

Author information

Affiliations

  1. Institute for Neuroscience Graduate Program, The University of Texas at Austin, Austin, Texas, USA.

    • Sachin P Vaidya

  2. Center for Learning and Memory, The University of Texas at Austin, Austin, Texas, USA.

    • Sachin P Vaidya
    •  & Daniel Johnston

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Contributions

S.P.V. & D.J. designed the experiments, interpreted the results and wrote the manuscript. S.P.V. performed the experiments, computer simulations and analysis of data.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Daniel Johnston.

Integrated supplementary information

Supplementary figures

  1. 1.

    Theta frequency oscillatory synchrony is observed only at the soma

  2. 2.

    ZPPsoma comparison between CA1 neuron, the ball-and-stick model and morphologically realistic model

  3. 3.

    Gradient of inductance achieves oscillatory synchrony with less voltage attenuation

  4. 4.

    The spatial distribution of HCN channels achieves maximum transfer at synchronization frequency

  5. 5.

    Dependence of oscillatory synchrony on the voltage dependence of activation and kinetics of HCN channels

  6. 6.

    Voltage dependence of SyncFreq

  7. 7.

    Addition of ZD7288 alters the band-pass filtering of SyncFreqs

  8. 8.

    Accuracy of dynamic clamp over current clamp for high-frequency synaptic inputs

  9. 9.

    Measurement of impedance phase profile (ZPP) by chirp versus sinusoids

  10. 10.

    Time-frequency analysis using continuous wavelet transform

Supplementary information

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    Supplementary Text and Figures

    Supplementary Figures 1–10

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DOI

https://doi.org/10.1038/nn.3562