Subcellular resolution three-dimensional light-field imaging with genetically encoded voltage indicators

Peter Quicke; Carmel L. Howe; Pingfan Song; Herman V. Jadan; Chenchen Song; Thomas Knöpfel; Mark Neil; Pier L. Dragotti; Simon R. Schultz; Amanda J. Foust

doi:10.1117/1.NPh.7.3.035006

Subcellular resolution three-dimensional light-field imaging with genetically encoded voltage indicators

Peter Quicke, Carmel L. Howe, Pingfan Song, Herman V. Jadan, Chenchen Song, Thomas Knöpfel, Mark Neil, Pier L. Dragotti, Simon R. Schultz^*, Amanda J. Foust^*

^*Corresponding author for this work

Department of Physics

Research output: Contribution to journal › Journal article › peer-review

26 Citations (Scopus)

Abstract

Significance: Light-field microscopy (LFM) enables high signal-to-noise ratio (SNR) and light efficient volume imaging at fast frame rates. Voltage imaging with genetically encoded voltage indicators (GEVIs) stands to particularly benefit from LFM's volumetric imaging capability due to high required sampling rates and limited probe brightness and functional sensitivity.

Aim: We demonstrate subcellular resolution GEVI light-field imaging in acute mouse brain slices resolving dendritic voltage signals in three spatial dimensions.

Approach: We imaged action potential-induced fluorescence transients in mouse brain slices sparsely expressing the GEVI VSFP-Butterfly 1.2 in wide-field microscopy (WFM) and LFM modes. We compared functional signal SNR and localization between different LFM reconstruction approaches and between LFM and WFM.

Results: LFM enabled three-dimensional (3-D) localization of action potential-induced fluorescence transients in neuronal somata and dendrites. Nonregularized deconvolution decreased SNR with increased iteration number compared to synthetic refocusing but increased axial and lateral signal localization. SNR was unaffected for LFM compared to WFM.

Conclusions: LFM enables 3-D localization of fluorescence transients, therefore eliminating the need for structures to lie in a single focal plane. These results demonstrate LFM's potential for studying dendritic integration and action potential propagation in three spatial dimensions.

Original language	English
Article number	035006
Number of pages	19
Journal	Neurophotonics
Volume	7
Issue number	3
DOIs	https://doi.org/10.1117/1.NPh.7.3.035006
Publication status	Published - Jul 2020

User-Defined Keywords

genetically encoded voltage indicator
light-field microscopy
voltage imaging

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10.1117/1.NPh.7.3.035006

Cite this

@article{e2774d79eeac4ef9bd3f73c1de67e9fd,

title = "Subcellular resolution three-dimensional light-field imaging with genetically encoded voltage indicators",

abstract = "Significance: Light-field microscopy (LFM) enables high signal-to-noise ratio (SNR) and light efficient volume imaging at fast frame rates. Voltage imaging with genetically encoded voltage indicators (GEVIs) stands to particularly benefit from LFM's volumetric imaging capability due to high required sampling rates and limited probe brightness and functional sensitivity. Aim: We demonstrate subcellular resolution GEVI light-field imaging in acute mouse brain slices resolving dendritic voltage signals in three spatial dimensions. Approach: We imaged action potential-induced fluorescence transients in mouse brain slices sparsely expressing the GEVI VSFP-Butterfly 1.2 in wide-field microscopy (WFM) and LFM modes. We compared functional signal SNR and localization between different LFM reconstruction approaches and between LFM and WFM. Results: LFM enabled three-dimensional (3-D) localization of action potential-induced fluorescence transients in neuronal somata and dendrites. Nonregularized deconvolution decreased SNR with increased iteration number compared to synthetic refocusing but increased axial and lateral signal localization. SNR was unaffected for LFM compared to WFM. Conclusions: LFM enables 3-D localization of fluorescence transients, therefore eliminating the need for structures to lie in a single focal plane. These results demonstrate LFM's potential for studying dendritic integration and action potential propagation in three spatial dimensions.",

keywords = "genetically encoded voltage indicator, light-field microscopy, voltage imaging",

author = "Peter Quicke and Howe, {Carmel L.} and Pingfan Song and Jadan, {Herman V.} and Chenchen Song and Thomas Kn{\"o}pfel and Mark Neil and Dragotti, {Pier L.} and Schultz, {Simon R.} and Foust, {Amanda J.}",

note = "Publisher Copyright: {\textcopyright} The Authors. Published by SPIE under a Creative Commons Attribution 4.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, including its DOI.",

year = "2020",

month = jul,

doi = "10.1117/1.NPh.7.3.035006",

language = "English",

volume = "7",

journal = "Neurophotonics",

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T1 - Subcellular resolution three-dimensional light-field imaging with genetically encoded voltage indicators

AU - Quicke, Peter

AU - Howe, Carmel L.

AU - Song, Pingfan

AU - Jadan, Herman V.

AU - Song, Chenchen

AU - Knöpfel, Thomas

AU - Neil, Mark

AU - Dragotti, Pier L.

AU - Schultz, Simon R.

AU - Foust, Amanda J.

N1 - Publisher Copyright: © The Authors. Published by SPIE under a Creative Commons Attribution 4.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, including its DOI.

PY - 2020/7

Y1 - 2020/7

N2 - Significance: Light-field microscopy (LFM) enables high signal-to-noise ratio (SNR) and light efficient volume imaging at fast frame rates. Voltage imaging with genetically encoded voltage indicators (GEVIs) stands to particularly benefit from LFM's volumetric imaging capability due to high required sampling rates and limited probe brightness and functional sensitivity. Aim: We demonstrate subcellular resolution GEVI light-field imaging in acute mouse brain slices resolving dendritic voltage signals in three spatial dimensions. Approach: We imaged action potential-induced fluorescence transients in mouse brain slices sparsely expressing the GEVI VSFP-Butterfly 1.2 in wide-field microscopy (WFM) and LFM modes. We compared functional signal SNR and localization between different LFM reconstruction approaches and between LFM and WFM. Results: LFM enabled three-dimensional (3-D) localization of action potential-induced fluorescence transients in neuronal somata and dendrites. Nonregularized deconvolution decreased SNR with increased iteration number compared to synthetic refocusing but increased axial and lateral signal localization. SNR was unaffected for LFM compared to WFM. Conclusions: LFM enables 3-D localization of fluorescence transients, therefore eliminating the need for structures to lie in a single focal plane. These results demonstrate LFM's potential for studying dendritic integration and action potential propagation in three spatial dimensions.

AB - Significance: Light-field microscopy (LFM) enables high signal-to-noise ratio (SNR) and light efficient volume imaging at fast frame rates. Voltage imaging with genetically encoded voltage indicators (GEVIs) stands to particularly benefit from LFM's volumetric imaging capability due to high required sampling rates and limited probe brightness and functional sensitivity. Aim: We demonstrate subcellular resolution GEVI light-field imaging in acute mouse brain slices resolving dendritic voltage signals in three spatial dimensions. Approach: We imaged action potential-induced fluorescence transients in mouse brain slices sparsely expressing the GEVI VSFP-Butterfly 1.2 in wide-field microscopy (WFM) and LFM modes. We compared functional signal SNR and localization between different LFM reconstruction approaches and between LFM and WFM. Results: LFM enabled three-dimensional (3-D) localization of action potential-induced fluorescence transients in neuronal somata and dendrites. Nonregularized deconvolution decreased SNR with increased iteration number compared to synthetic refocusing but increased axial and lateral signal localization. SNR was unaffected for LFM compared to WFM. Conclusions: LFM enables 3-D localization of fluorescence transients, therefore eliminating the need for structures to lie in a single focal plane. These results demonstrate LFM's potential for studying dendritic integration and action potential propagation in three spatial dimensions.

KW - genetically encoded voltage indicator

KW - light-field microscopy

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JO - Neurophotonics

JF - Neurophotonics

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Subcellular resolution three-dimensional light-field imaging with genetically encoded voltage indicators

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