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Parvalbumin interneurons mediate neuronal circuitry–neurogenesis coupling in the adult hippocampus

Nature Neuroscience 16, 1728–1730 (2013) | Download Citation

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Abstract

Using immunohistology, electron microscopy, electrophysiology and optogenetics, we found that proliferating adult mouse hippocampal neural precursors received immature GABAergic synaptic inputs from parvalbumin-expressing interneurons. Recently shown to suppress adult quiescent neural stem cell activation, parvalbumin interneuron activation promoted newborn neuronal progeny survival and development. Our results suggest a niche mechanism involving parvalbumin interneurons that couples local circuit activity to the diametric regulation of two critical early phases of adult hippocampal neurogenesis.

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Acknowledgements

We thank members of the Song and Ming laboratories for discussion, L. Tsai and K. Deisseroth for initial help with optogenetics, and Q. Hussaini, Y. Cai and L. Liu for technical support. The electron microscopy images were acquired at the electron microscopy facility of the University of Lausanne. This work was supported by grants from the US National Institutes of Health (NS047344, ES021957) and The Brain & Behavior Research Foundation to H.S., from the US National Institutes of Health (NS048271, HD069184), the Dr. Miriam and Sheldon G. Adelson Medical Research Foundation, The Brain & Behavior Research Foundation and Maryland Stem Cell Research Fund to G.M., from the Swiss National Science Foundation (PP00A-119026/1) to N.T., from The Brain & Behavior Research Foundationand Maryland Stem Cell Research Fund to K.M.C., by postdoctoral fellowships from Maryland Stem Cell Research Fund to J. Song, Z.W. and C.Z., from the Fondation Leenaards to J.M., and by a pre-doctoral fellowship from The Children's Tumor Foundation to G.J.S.

Author information

    • Jiaqi Sun
    • , Jonathan Moss
    •  & Zhexing Wen

    These authors contributed equally to this work.

    • Nicolas Toni
    • , Guo-li Ming
    •  & Hongjun Song

    These authors jointly directed this work.

Affiliations

  1. Institute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Juan Song
    • , Jiaqi Sun
    • , Zhexing Wen
    • , Gerald J Sun
    • , Derek Hsu
    • , Chun Zhong
    • , Heydar Davoudi
    • , Kimberly M Christian
    • , Guo-li Ming
    •  & Hongjun Song

  2. Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Juan Song
    • , Zhexing Wen
    • , Chun Zhong
    • , Kimberly M Christian
    • , Guo-li Ming
    •  & Hongjun Song

  3. Department of Pharmacology and Neuroscience Center, University of North Carolina School of Medicine, Chapel Hill, North Carolina, USA.

    • Juan Song

  4. School of Life Sciences, Tsinghua University, Beijing, China.

    • Jiaqi Sun

  5. Department of Fundamental Neurosciences, University of Lausanne, Lausanne, Switzerland.

    • Jonathan Moss
    •  & Nicolas Toni

  6. The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Gerald J Sun
    • , Guo-li Ming
    •  & Hongjun Song

  7. Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Heydar Davoudi

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Contributions

J. Song led and contributed to all aspects of the study. J.M. and N.T. performed electron microscopy analyses. J. Sun, Z.W., G.J.S., D.H., C.Z., H.D. and K.M.C. contributed to tool development and data collection and analyses. G.M. and H.S. supervised the project and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Nicolas Toni or Guo-li Ming or Hongjun Song.

Integrated supplementary information

Supplementary figures

  1. 1.

    Immunohistological characterization of newborn progeny during early proliferative phases of adult hippocampal neurogenesis.

  2. 2.

    Electrophysiological characterization of newborn progeny during early proliferative phases of adult hippocampal neurogenesis.

  3. 3.

    Synaptic inputs onto proliferating neural progeny from PV+ interneurons.

  4. 4.

    Immuno-EM analyses of synapses and close appositions between PV+ axon terminals and newborn progeny in the adult dentate gyrus.

  5. 5.

    Characterization of PV+ neuron synaptic inputs onto newborn progeny with optogenetic tools.

  6. 6.

    Activation of PV+ neurons at 8 Hz reduces cell death of newborn progeny.

  7. 7.

    Effect of optogenetic activation of PV+ or SST+ interneurons during early proliferative phases of adult hippocampal neurogenesis in vivo.

  8. 8.

    Effect of suppressing PV+, or SST+, interneuron activation during early phases of adult hippocampal neurogenesis in vivo.

  9. 9.

    Optogenetic manipulations do not appear to affect properties of mature dentate granule neurons in the adult dentate gyrus.

  10. 10.

    PV+ neuron activity regulates dendritic growth of newborn neurons during adult hippocampal neurogenesis.

  11. 11.

    Models of activity-dependent diametric regulation of adult hippocampal neurogenesis processes and two critical periods of activity-dependent survival of newborn neuronal progeny.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–11 and Supplementary Table 1

Videos

  1. 1.

    Close association between GFP+ newborn progeny and GAD67+Synapsin I+ synaptic puncta in the adult dentate gyrus.

    Adult mice injected with onco-retroviruses to express GFP in proliferating progenitors in the adult SGZ. Shown is a surface-rendered reconstruction of a series of confocal images of the dentate gyrus (90 x 90 x 30 mm) for immunostaining of GFP (green), GAD67 (blue) and synapsin I (red) at 4 dpi.

  2. 2.

    Close association between GFP+ newborn progeny and PV+Synapsin I+ synaptic puncta in the adult dentate gyrus.

    Adult mice were injected with onco-retroviruses to express GFP in proliferating progenitors in the adult SGZ. Shown is a surface-rendered reconstruction of a series of confocal images of the dentate gyrus (90 x 90 x 30 mm) for immunostaining of GFP (green), PV (blue) and synapsin I (red) at 4 dpi.

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DOI

https://doi.org/10.1038/nn.3572