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Ultrasensitive fluorescent proteins for imaging neuronal activity

Author

Listed:
  • Tsai-Wen Chen

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Trevor J. Wardill

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA
    Present address: Marine Biological Laboratory, Program in Sensory Physiology and Behavior, 7 MBL Street, Woods Hole, Massachusetts 02543, USA.)

  • Yi Sun

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Stefan R. Pulver

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Sabine L. Renninger

    (Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Avenida Brasília, Doca de Pedrouços, 1400-038, Lisbon, Portugal)

  • Amy Baohan

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA
    University of California Los Angeles, Los Angeles, California 90095, USA)

  • Eric R. Schreiter

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Rex A. Kerr

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Michael B. Orger

    (Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Avenida Brasília, Doca de Pedrouços, 1400-038, Lisbon, Portugal)

  • Vivek Jayaraman

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Loren L. Looger

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Karel Svoboda

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

  • Douglas S. Kim

    (Janelia Farm Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA)

Abstract

Fluorescent calcium sensors are widely used to image neural activity. Using structure-based mutagenesis and neuron-based screening, we developed a family of ultrasensitive protein calcium sensors (GCaMP6) that outperformed other sensors in cultured neurons and in zebrafish, flies and mice in vivo. In layer 2/3 pyramidal neurons of the mouse visual cortex, GCaMP6 reliably detected single action potentials in neuronal somata and orientation-tuned synaptic calcium transients in individual dendritic spines. The orientation tuning of structurally persistent spines was largely stable over timescales of weeks. Orientation tuning averaged across spine populations predicted the tuning of their parent cell. Although the somata of GABAergic neurons showed little orientation tuning, their dendrites included highly tuned dendritic segments (5–40-µm long). GCaMP6 sensors thus provide new windows into the organization and dynamics of neural circuits over multiple spatial and temporal scales.

Suggested Citation

  • Tsai-Wen Chen & Trevor J. Wardill & Yi Sun & Stefan R. Pulver & Sabine L. Renninger & Amy Baohan & Eric R. Schreiter & Rex A. Kerr & Michael B. Orger & Vivek Jayaraman & Loren L. Looger & Karel Svobod, 2013. "Ultrasensitive fluorescent proteins for imaging neuronal activity," Nature, Nature, vol. 499(7458), pages 295-300, July.
  • Handle: RePEc:nat:nature:v:499:y:2013:i:7458:d:10.1038_nature12354
    DOI: 10.1038/nature12354
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    Cited by:

    1. Guillaume Viejo & Thomas Cortier & Adrien Peyrache, 2018. "Brain-state invariant thalamo-cortical coordination revealed by non-linear encoders," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-25, March.
    2. Zengpeng Han & Nengsong Luo & Wenyu Ma & Xiaodong Liu & Yuxiang Cai & Jiaxin Kou & Jie Wang & Lei Li & Siqi Peng & Zihong Xu & Wen Zhang & Yuxiang Qiu & Yang Wu & Chaohui Ye & Kunzhang Lin & Fuqiang X, 2023. "AAV11 enables efficient retrograde targeting of projection neurons and enhances astrocyte-directed transduction," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Yuanlong Zhang & Xiaofei Song & Jiachen Xie & Jing Hu & Jiawei Chen & Xiang Li & Haiyu Zhang & Qiqun Zhou & Lekang Yuan & Chui Kong & Yibing Shen & Jiamin Wu & Lu Fang & Qionghai Dai, 2023. "Large depth-of-field ultra-compact microscope by progressive optimization and deep learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Jeffrey P Nguyen & Ashley N Linder & George S Plummer & Joshua W Shaevitz & Andrew M Leifer, 2017. "Automatically tracking neurons in a moving and deforming brain," PLOS Computational Biology, Public Library of Science, vol. 13(5), pages 1-19, May.
    5. Johannes Friedrich & Weijian Yang & Daniel Soudry & Yu Mu & Misha B Ahrens & Rafael Yuste & Darcy S Peterka & Liam Paninski, 2017. "Multi-scale approaches for high-speed imaging and analysis of large neural populations," PLOS Computational Biology, Public Library of Science, vol. 13(8), pages 1-24, August.
    6. Jilt Sebastian & Mriganka Sur & Hema A Murthy & Mathew Magimai-Doss, 2021. "Signal-to-signal neural networks for improved spike estimation from calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-19, March.
    7. Jina Yun & Simon Hansen & Otto Morris & David T. Madden & Clare Peters Libeu & Arjun J. Kumar & Cameron Wehrfritz & Aaron H. Nile & Yingnan Zhang & Lijuan Zhou & Yuxin Liang & Zora Modrusan & Michelle, 2023. "Senescent cells perturb intestinal stem cell differentiation through Ptk7 induced noncanonical Wnt and YAP signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Omer Mano & Damon A Clark, 2017. "Graphics Processing Unit-Accelerated Code for Computing Second-Order Wiener Kernels and Spike-Triggered Covariance," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-11, January.
    9. Richard F Betzel & Katherine C Wood & Christopher Angeloni & Maria Neimark Geffen & Danielle S Bassett, 2019. "Stability of spontaneous, correlated activity in mouse auditory cortex," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-25, December.
    10. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    11. Philipp Berens & Jeremy Freeman & Thomas Deneux & Nikolay Chenkov & Thomas McColgan & Artur Speiser & Jakob H Macke & Srinivas C Turaga & Patrick Mineault & Peter Rupprecht & Stephan Gerhard & Rainer , 2018. "Community-based benchmarking improves spike rate inference from two-photon calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 14(5), pages 1-13, May.
    12. Sophie Aimon & Takeo Katsuki & Tongqiu Jia & Logan Grosenick & Michael Broxton & Karl Deisseroth & Terrence J Sejnowski & Ralph J Greenspan, 2019. "Fast near-whole–brain imaging in adult Drosophila during responses to stimuli and behavior," PLOS Biology, Public Library of Science, vol. 17(2), pages 1-31, February.
    13. Franziska Bierbuesse & Anaïs C. Bourges & Vincent Gielen & Viola Mönkemöller & Wim Vandenberg & Yi Shen & Johan Hofkens & Pieter Vanden Berghe & Robert E. Campbell & Benjamien Moeyaert & Peter Dedecke, 2022. "Absolute measurement of cellular activities using photochromic single-fluorophore biosensors and intermittent quantification," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    14. Hyung Chul Lee & Nidia M. M. Oliveira & Cato Hastings & Peter Baillie-Benson & Adam A. Moverley & Hui-Chun Lu & Yi Zheng & Elise L. Wilby & Timothy T. Weil & Karen M. Page & Jianping Fu & Naomi Moris , 2024. "Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. Johannes Friedrich & Pengcheng Zhou & Liam Paninski, 2017. "Fast online deconvolution of calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-26, March.
    16. Roman Dvorkin & Noam E Ziv, 2016. "Relative Contributions of Specific Activity Histories and Spontaneous Processes to Size Remodeling of Glutamatergic Synapses," PLOS Biology, Public Library of Science, vol. 14(10), pages 1-33, October.
    17. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    18. Jimin Wu & Yuzhi Chen & Ashok Veeraraghavan & Eyal Seidemann & Jacob T. Robinson, 2024. "Mesoscopic calcium imaging in a head-unrestrained male non-human primate using a lensless microscope," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    19. Che-Hang Yu & Jeffrey N. Stirman & Yiyi Yu & Riichiro Hira & Spencer L. Smith, 2021. "Diesel2p mesoscope with dual independent scan engines for flexible capture of dynamics in distributed neural circuitry," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    20. Liang Shi & Xiaoxi Fu & Shen Gui & Tong Wan & Junjie Zhuo & Jinling Lu & Pengcheng Li, 2024. "Global spatiotemporal synchronizing structures of spontaneous neural activities in different cell types," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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