Letter | Published:

Calcium transient prevalence across the dendritic arbour predicts place field properties

Nature volume 517, pages 200204 (08 January 2015) | Download Citation

Abstract

Establishing the hippocampal cellular ensemble that represents an animal’s environment involves the emergence and disappearance of place fields in specific CA1 pyramidal neurons1,2,3,4, and the acquisition of different spatial firing properties across the active population5. While such firing flexibility and diversity have been linked to spatial memory, attention and task performance6,7, the cellular and network origin of these place cell features is unknown. Basic integrate-and-fire models of place firing propose that such features result solely from varying inputs to place cells8,9, but recent studies3,10 suggest instead that place cells themselves may play an active role through regenerative dendritic events. However, owing to the difficulty of performing functional recordings from place cell dendrites, no direct evidence of regenerative dendritic events exists, leaving any possible connection to place coding unknown. Using multi-plane two-photon calcium imaging of CA1 place cell somata, axons and dendrites in mice navigating a virtual environment, here we show that regenerative dendritic events do exist in place cells of behaving mice, and, surprisingly, their prevalence throughout the arbour is highly spatiotemporally variable. Furthermore, we show that the prevalence of such events predicts the spatial precision and persistence or disappearance of place fields. This suggests that the dynamics of spiking throughout the dendritic arbour may play a key role in forming the hippocampal representation of space.

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Acknowledgements

We are grateful to B. Mensh for discussions on data conceptualization, interpretation and presentation. We thank C. Harvey, B. Mensh, N. Spruston, C. Woolley, W. Kath and L. Looger for comments on the manuscript, E. Han and P. Boueri for technical assistance, and V. Jayaraman, R. Kerr, D. Kim, L. Looger, K. Svoboda from the GENIE Project (Janelia Farm, Howard Hughes Medical Institute) for GCaMP6. This work was supported by The Klingenstein Foundation, The Whitehall Foundation, The Chicago Biomedical Consortium with support from the Searle Funds at The Chicago Community Trust, Northwestern University, The National Institutes of Health (1R01MH101297), and M.S. is an Ellison Medical Foundation Fellow of the Life Sciences Research Foundation.

Author information

Affiliations

  1. Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA

    • Mark E. J. Sheffield
    •  & Daniel A. Dombeck

Authors

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Contributions

M.S. performed the experiments, D.D. built the experimental apparatus, M.S. performed data analysis with strategy suggestions from D.D. Both authors conceived and designed the experiments, interpreted the data and wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Daniel A. Dombeck.

Extended data

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    Supplementary Information

    This file contains Supplementary Notes and additional references.

Videos

  1. 1.

    Somatic, axonal and dendritic place field transients

    Time-series video from two different place cells in different mice (see Figures for scale; Figs 2c and 1b for first and second place cell, respectively). In each cell, time-series videos from somatic and dendritic imaging planes were co-acquired (at 10.4 frames/sec in each plane; planes separated by 70 and 85 μm for first and second place cell, respectively). The time series from each of the imaging planes are aligned in time and vertically concatenated for presentation (displayed at 20 frames/sec). Each somatic (and axonal/dendritic) transient occurs during a separate place field traversal. Note the variability in branch spiking across the visible dendritic branches and the similarity in somatic and axonal (second place cell) transients between the different place field traversals.

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DOI

https://doi.org/10.1038/nature13871

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