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Chandelier cell anatomy and function reveal a variably distributed but common signal

Casey M. Schneider-Mizell, Agnes L. Bodor, Forrest Collman, Derrick Brittain, Adam A. Bleckert, Sven Dorkenwald, Nicholas L. Turner, Thomas Macrina, Kisuk Lee, Ran Lu, Jingpeng Wu, View ORCID ProfileJun Zhuang, Anirban Nandi, View ORCID ProfileBrian Hu, JoAnn Buchanan, Marc M. Takeno, Russel Torres, Gayathri Mahalingam, Daniel J. Bumbarger, Yang Li, Tom Chartrand, Nico Kemnitz, William M. Silversmith, Dodam Ih, Jonathan Zung, Aleksandar Zlateski, Ignacio Tartavull, Sergiy Popovych, William Wong, Manuel Castro, Chris S. Jordan, Emmanouil Froudarakis, Lynne Becker, Shelby Suckow, Jacob Reimer, Andreas S. Tolias, Costas Anastassiou, H. Sebastian Seung, R. Clay Reid, Nuno Maçarico da Costa
doi: https://doi.org/10.1101/2020.03.31.018952
Casey M. Schneider-Mizell
1Allen Institute for Brain Sciences
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  • For correspondence: nunod@alleninstitute.org
Agnes L. Bodor
1Allen Institute for Brain Sciences
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Forrest Collman
1Allen Institute for Brain Sciences
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Derrick Brittain
1Allen Institute for Brain Sciences
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Adam A. Bleckert
1Allen Institute for Brain Sciences
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Sven Dorkenwald
2Princeton Neuroscience Institute, Princeton University
3Computer Science Department, Princeton University
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Nicholas L. Turner
2Princeton Neuroscience Institute, Princeton University
3Computer Science Department, Princeton University
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Thomas Macrina
2Princeton Neuroscience Institute, Princeton University
3Computer Science Department, Princeton University
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Kisuk Lee
2Princeton Neuroscience Institute, Princeton University
4Brain & Cognitive Sciences Department, Massachusetts Institute of Technology
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Ran Lu
2Princeton Neuroscience Institute, Princeton University
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Jingpeng Wu
2Princeton Neuroscience Institute, Princeton University
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Jun Zhuang
1Allen Institute for Brain Sciences
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Anirban Nandi
1Allen Institute for Brain Sciences
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Brian Hu
1Allen Institute for Brain Sciences
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JoAnn Buchanan
1Allen Institute for Brain Sciences
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Marc M. Takeno
1Allen Institute for Brain Sciences
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Russel Torres
1Allen Institute for Brain Sciences
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Gayathri Mahalingam
1Allen Institute for Brain Sciences
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Daniel J. Bumbarger
1Allen Institute for Brain Sciences
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Yang Li
1Allen Institute for Brain Sciences
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Tom Chartrand
1Allen Institute for Brain Sciences
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Nico Kemnitz
2Princeton Neuroscience Institute, Princeton University
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William M. Silversmith
2Princeton Neuroscience Institute, Princeton University
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Dodam Ih
2Princeton Neuroscience Institute, Princeton University
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Jonathan Zung
2Princeton Neuroscience Institute, Princeton University
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Aleksandar Zlateski
2Princeton Neuroscience Institute, Princeton University
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Ignacio Tartavull
2Princeton Neuroscience Institute, Princeton University
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Sergiy Popovych
2Princeton Neuroscience Institute, Princeton University
3Computer Science Department, Princeton University
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William Wong
2Princeton Neuroscience Institute, Princeton University
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Manuel Castro
2Princeton Neuroscience Institute, Princeton University
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Chris S. Jordan
2Princeton Neuroscience Institute, Princeton University
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Emmanouil Froudarakis
5Department of Neuroscience, Baylor College of Medicine
6Center for Neuroscience and Artificial Intelligence, Baylor College of Medicine
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Lynne Becker
1Allen Institute for Brain Sciences
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Shelby Suckow
1Allen Institute for Brain Sciences
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Jacob Reimer
5Department of Neuroscience, Baylor College of Medicine
6Center for Neuroscience and Artificial Intelligence, Baylor College of Medicine
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Andreas S. Tolias
5Department of Neuroscience, Baylor College of Medicine
6Center for Neuroscience and Artificial Intelligence, Baylor College of Medicine
7Department of Electrical and Computer Engineering, Rice University
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Costas Anastassiou
1Allen Institute for Brain Sciences
8Department of Neurology, University of British Columbia
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H. Sebastian Seung
2Princeton Neuroscience Institute, Princeton University
3Computer Science Department, Princeton University
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R. Clay Reid
1Allen Institute for Brain Sciences
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Nuno Maçarico da Costa
1Allen Institute for Brain Sciences
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  • For correspondence: nunod@alleninstitute.org
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Abstract

The activity and connectivity of inhibitory cells has a profound impact on the operation of neuronal networks. While the average connectivity of many inhibitory cell types has been characterized, we still lack an understanding of how individual interneurons distribute their synapses onto their targets and how heterogeneous the inhibition is onto different individual excitatory neurons. Here, we use large-scale volumetric electron microscopy (EM) and functional imaging to address this question for chandelier cells in layer 2/3 of mouse visual cortex. Using dense morphological reconstructions from EM, we mapped the complete chandelier input onto 153 pyramidal neurons. We find that the number of input synapses is highly variable across the population, but the variability is correlated with structural features of the target neuron: soma depth, soma size, and the number of perisomatic synapses received. Functionally, we found that chandelier cell activity in vivo was highly correlated and tracks pupil diameter, a proxy for arousal state. We propose that chandelier cells provide a global signal whose strength is individually adjusted for each target neuron. This approach, combining comprehensive structural analysis with functional recordings of identified cell types, will be a powerful tool to uncover the wiring rules across the diversity of cortical cell types.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 01, 2020.
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Chandelier cell anatomy and function reveal a variably distributed but common signal
Casey M. Schneider-Mizell, Agnes L. Bodor, Forrest Collman, Derrick Brittain, Adam A. Bleckert, Sven Dorkenwald, Nicholas L. Turner, Thomas Macrina, Kisuk Lee, Ran Lu, Jingpeng Wu, Jun Zhuang, Anirban Nandi, Brian Hu, JoAnn Buchanan, Marc M. Takeno, Russel Torres, Gayathri Mahalingam, Daniel J. Bumbarger, Yang Li, Tom Chartrand, Nico Kemnitz, William M. Silversmith, Dodam Ih, Jonathan Zung, Aleksandar Zlateski, Ignacio Tartavull, Sergiy Popovych, William Wong, Manuel Castro, Chris S. Jordan, Emmanouil Froudarakis, Lynne Becker, Shelby Suckow, Jacob Reimer, Andreas S. Tolias, Costas Anastassiou, H. Sebastian Seung, R. Clay Reid, Nuno Maçarico da Costa
bioRxiv 2020.03.31.018952; doi: https://doi.org/10.1101/2020.03.31.018952
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Chandelier cell anatomy and function reveal a variably distributed but common signal
Casey M. Schneider-Mizell, Agnes L. Bodor, Forrest Collman, Derrick Brittain, Adam A. Bleckert, Sven Dorkenwald, Nicholas L. Turner, Thomas Macrina, Kisuk Lee, Ran Lu, Jingpeng Wu, Jun Zhuang, Anirban Nandi, Brian Hu, JoAnn Buchanan, Marc M. Takeno, Russel Torres, Gayathri Mahalingam, Daniel J. Bumbarger, Yang Li, Tom Chartrand, Nico Kemnitz, William M. Silversmith, Dodam Ih, Jonathan Zung, Aleksandar Zlateski, Ignacio Tartavull, Sergiy Popovych, William Wong, Manuel Castro, Chris S. Jordan, Emmanouil Froudarakis, Lynne Becker, Shelby Suckow, Jacob Reimer, Andreas S. Tolias, Costas Anastassiou, H. Sebastian Seung, R. Clay Reid, Nuno Maçarico da Costa
bioRxiv 2020.03.31.018952; doi: https://doi.org/10.1101/2020.03.31.018952

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