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Precision calcium imaging of dense neural populations via a cell body-targeted calcium indicator

Or A. Shemesh, Changyang Linghu, Kiryl D. Piatkevich, Daniel Goodwin, Howard J. Gritton, Michael F. Romano, Cody Siciliano, Ruixuan Gao, Chi-Chieh (Jay) Yu, Hua-An Tseng, Seth Bensussen, Sujatha Narayan, Chao-Tsung Yang, Limor Freifeld, Ishan Gupta, Habiba Noamany, Nikita Pak, Young-Gyu Yoon, Jeremy F.P. Ullmann, Burcu Guner-Ataman, Zoe R. Sheinkopf, Won Min Park, Shoh Asano, Amy E. Keating, James S. Trimmer, Jacob Reimer, Andreas Tolias, Kay M. Tye, Xue Han, Misha B. Ahrens, Edward S. Boyden
doi: https://doi.org/10.1101/773069
Or A. Shemesh
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
4Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
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Changyang Linghu
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
6Department of Electrical Engineering and Computer Science, MIT, Cambridge, Massachusetts, USA.
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Kiryl D. Piatkevich
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
4Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
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Daniel Goodwin
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
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Howard J. Gritton
7Boston University, Department of Biomedical Engineering, Boston, MA 02215.
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Michael F. Romano
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Cody Siciliano
8The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Ruixuan Gao
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Chi-Chieh (Jay) Yu
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
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Hua-An Tseng
7Boston University, Department of Biomedical Engineering, Boston, MA 02215.
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Seth Bensussen
7Boston University, Department of Biomedical Engineering, Boston, MA 02215.
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Sujatha Narayan
10Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA.
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Chao-Tsung Yang
10Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA.
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Limor Freifeld
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
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Ishan Gupta
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
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Habiba Noamany
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Nikita Pak
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
9Department of Mechanical Engineering, MIT, Cambridge, Massachusetts, USA.
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Young-Gyu Yoon
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
6Department of Electrical Engineering and Computer Science, MIT, Cambridge, Massachusetts, USA.
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Jeremy F.P. Ullmann
12Epilepsy Genetics Program, Department of Neurology, Boston Children’s Hospital & Harvard Medical School, Massachusetts, USA.
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Burcu Guner-Ataman
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Zoe R. Sheinkopf
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Won Min Park
11Department of Biology, MIT, Cambridge, Massachusetts, USA.
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Shoh Asano
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Amy E. Keating
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
11Department of Biology, MIT, Cambridge, Massachusetts, USA.
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James S. Trimmer
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
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Jacob Reimer
14Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA.
15Center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, TX, USA.
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Andreas Tolias
14Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA.
15Center for Neuroscience and Artificial Intelligence, Baylor College of Medicine, Houston, TX, USA.
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Kay M. Tye
8The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
16The Salk Institute for Biological Science, La Jolla, CA 92037.
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Xue Han
7Boston University, Department of Biomedical Engineering, Boston, MA 02215.
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Misha B. Ahrens
10Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, USA.
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Edward S. Boyden
1The MIT Media Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA.
2Department of Biological Engineering, MIT, Cambridge, Massachusetts, USA.
3MIT Center for Neurobiological Engineering, MIT, Cambridge, Massachusetts, USA.
4Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts, USA.
5MIT McGovern Institute for Brain Research, MIT, Cambridge, Massachusetts, USA.
13Koch Institute, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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  • For correspondence: esb@media.mit.edu
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Abstract

Methods for one-photon fluorescent imaging of calcium dynamics in vivo are popular due to their ability to simultaneously capture the dynamics of hundreds of neurons across large fields of view, at a low equipment complexity and cost. In contrast to two-photon methods, however, one-photon methods suffer from higher levels of crosstalk between cell bodies and the surrounding neuropil, resulting in decreased signal-to-noise and artifactual correlations of neural activity. Here, we address this problem by engineering cell body-targeted variants of the fluorescent calcium indicator GCaMP6f. We screened fusions of GCaMP6f to both natural as well as engineered peptides, and identified fusions that localized GCaMP6f to within approximately 50 microns of the cell body of neurons in live mice and larval zebrafish. One-photon imaging of soma-targeted GCaMP6f in dense neural circuits reported fewer artifactual spikes from neuropil, increased signal-to-noise ratio, and decreased artifactual correlation across neurons. Thus, soma-targeting of fluorescent calcium indicators increases neuronal signal fidelity and may facilitate even greater usage of simple, powerful, one-photon methods of population imaging of neural calcium dynamics.

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Posted September 17, 2019.
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Precision calcium imaging of dense neural populations via a cell body-targeted calcium indicator
Or A. Shemesh, Changyang Linghu, Kiryl D. Piatkevich, Daniel Goodwin, Howard J. Gritton, Michael F. Romano, Cody Siciliano, Ruixuan Gao, Chi-Chieh (Jay) Yu, Hua-An Tseng, Seth Bensussen, Sujatha Narayan, Chao-Tsung Yang, Limor Freifeld, Ishan Gupta, Habiba Noamany, Nikita Pak, Young-Gyu Yoon, Jeremy F.P. Ullmann, Burcu Guner-Ataman, Zoe R. Sheinkopf, Won Min Park, Shoh Asano, Amy E. Keating, James S. Trimmer, Jacob Reimer, Andreas Tolias, Kay M. Tye, Xue Han, Misha B. Ahrens, Edward S. Boyden
bioRxiv 773069; doi: https://doi.org/10.1101/773069
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Precision calcium imaging of dense neural populations via a cell body-targeted calcium indicator
Or A. Shemesh, Changyang Linghu, Kiryl D. Piatkevich, Daniel Goodwin, Howard J. Gritton, Michael F. Romano, Cody Siciliano, Ruixuan Gao, Chi-Chieh (Jay) Yu, Hua-An Tseng, Seth Bensussen, Sujatha Narayan, Chao-Tsung Yang, Limor Freifeld, Ishan Gupta, Habiba Noamany, Nikita Pak, Young-Gyu Yoon, Jeremy F.P. Ullmann, Burcu Guner-Ataman, Zoe R. Sheinkopf, Won Min Park, Shoh Asano, Amy E. Keating, James S. Trimmer, Jacob Reimer, Andreas Tolias, Kay M. Tye, Xue Han, Misha B. Ahrens, Edward S. Boyden
bioRxiv 773069; doi: https://doi.org/10.1101/773069

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