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Reconciling functional differences in populations of neurons recorded with two-photon imaging and electrophysiology

Joshua H. Siegle, Peter Ledochowitsch, Xiaoxuan Jia, Daniel Millman, View ORCID ProfileGabriel K. Ocker, Shiella Caldejon, Linzy Casal, Andrew Cho, Daniel J. Denman, Séverine Durand, Peter A. Groblewski, Greggory Heller, India Kato, Sara Kivikas, Jerome Lecoq, Chelsea Nayan, Kiet Ngo, Philip R. Nicovich, Kat R. North, Tamina K. Ramirez, Jackie Swapp, Xana Waughman, Ali Williford, Shawn R. Olsen, Christof Koch, Michael A. Buice, View ORCID ProfileSaskia E. J. de Vries
doi: https://doi.org/10.1101/2020.08.10.244723
Joshua H. Siegle
1MindScope Program, Allen Institute, Seattle, WA
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Peter Ledochowitsch
1MindScope Program, Allen Institute, Seattle, WA
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Xiaoxuan Jia
1MindScope Program, Allen Institute, Seattle, WA
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Daniel Millman
1MindScope Program, Allen Institute, Seattle, WA
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Gabriel K. Ocker
1MindScope Program, Allen Institute, Seattle, WA
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Shiella Caldejon
1MindScope Program, Allen Institute, Seattle, WA
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Linzy Casal
1MindScope Program, Allen Institute, Seattle, WA
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Andrew Cho
1MindScope Program, Allen Institute, Seattle, WA
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Daniel J. Denman
2Allen Institute for Brain Science, Allen Institute, Seattle, WA
3University of Colorado Denver Anschutz Medical Campus, Aurora, CO
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Séverine Durand
1MindScope Program, Allen Institute, Seattle, WA
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Peter A. Groblewski
1MindScope Program, Allen Institute, Seattle, WA
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Greggory Heller
1MindScope Program, Allen Institute, Seattle, WA
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India Kato
1MindScope Program, Allen Institute, Seattle, WA
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Sara Kivikas
1MindScope Program, Allen Institute, Seattle, WA
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Jerome Lecoq
1MindScope Program, Allen Institute, Seattle, WA
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Chelsea Nayan
1MindScope Program, Allen Institute, Seattle, WA
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Kiet Ngo
2Allen Institute for Brain Science, Allen Institute, Seattle, WA
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Philip R. Nicovich
2Allen Institute for Brain Science, Allen Institute, Seattle, WA
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Kat R. North
1MindScope Program, Allen Institute, Seattle, WA
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Tamina K. Ramirez
1MindScope Program, Allen Institute, Seattle, WA
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Jackie Swapp
1MindScope Program, Allen Institute, Seattle, WA
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Xana Waughman
1MindScope Program, Allen Institute, Seattle, WA
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Ali Williford
1MindScope Program, Allen Institute, Seattle, WA
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Shawn R. Olsen
1MindScope Program, Allen Institute, Seattle, WA
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Christof Koch
1MindScope Program, Allen Institute, Seattle, WA
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Michael A. Buice
1MindScope Program, Allen Institute, Seattle, WA
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Saskia E. J. de Vries
1MindScope Program, Allen Institute, Seattle, WA
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  • ORCID record for Saskia E. J. de Vries
  • For correspondence: saskiad@alleninstitute.org
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Abstract

Extracellular electrophysiology and two-photon calcium imaging are widely used methods for measuring physiological activity with single-cell resolution across large populations of neurons in the brain. While these two modalities have distinct advantages and disadvantages, neither provides complete, unbiased information about the underlying neural population. Here, we compare evoked responses in visual cortex recorded in awake mice under highly standardized conditions using either imaging or electrophysiology. Across all stimulus conditions tested, we observe a larger fraction of responsive neurons in electrophysiology and higher stimulus selectivity in calcium imaging. This work explores which data transformations are most useful for explaining these modality-specific discrepancies. We show that the higher selectivity in imaging can be partially reconciled by applying a spikes-to-calcium forward model to the electrophysiology data. However, the forward model could not reconcile differences in responsiveness without sub-selecting neurons based on event rate or level of signal contamination. This suggests that differences in responsiveness more likely reflect neuronal sampling bias or cluster-merging artifacts during spike sorting of electrophysiological recordings, rather than flaws in event detection from fluorescence time series. This work establishes the dominant impacts of the two modalities’ respective biases on a set of functional metrics that are fundamental for characterizing sensory-evoked responses.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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 August 11, 2020.
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Reconciling functional differences in populations of neurons recorded with two-photon imaging and electrophysiology
Joshua H. Siegle, Peter Ledochowitsch, Xiaoxuan Jia, Daniel Millman, Gabriel K. Ocker, Shiella Caldejon, Linzy Casal, Andrew Cho, Daniel J. Denman, Séverine Durand, Peter A. Groblewski, Greggory Heller, India Kato, Sara Kivikas, Jerome Lecoq, Chelsea Nayan, Kiet Ngo, Philip R. Nicovich, Kat R. North, Tamina K. Ramirez, Jackie Swapp, Xana Waughman, Ali Williford, Shawn R. Olsen, Christof Koch, Michael A. Buice, Saskia E. J. de Vries
bioRxiv 2020.08.10.244723; doi: https://doi.org/10.1101/2020.08.10.244723
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Reconciling functional differences in populations of neurons recorded with two-photon imaging and electrophysiology
Joshua H. Siegle, Peter Ledochowitsch, Xiaoxuan Jia, Daniel Millman, Gabriel K. Ocker, Shiella Caldejon, Linzy Casal, Andrew Cho, Daniel J. Denman, Séverine Durand, Peter A. Groblewski, Greggory Heller, India Kato, Sara Kivikas, Jerome Lecoq, Chelsea Nayan, Kiet Ngo, Philip R. Nicovich, Kat R. North, Tamina K. Ramirez, Jackie Swapp, Xana Waughman, Ali Williford, Shawn R. Olsen, Christof Koch, Michael A. Buice, Saskia E. J. de Vries
bioRxiv 2020.08.10.244723; doi: https://doi.org/10.1101/2020.08.10.244723

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