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All-optical electrophysiology reveals excitation, inhibition, and neuromodulation in cortical layer 1

Linlin Z. Fan, Simon Kheifets, Urs L. Böhm, Kiryl D. Piatkevich, Hao Wu, Vicente Parot, Michael E. Xie, Edward S. Boyden, Anne E. Takesian, Adam E. Cohen
doi: https://doi.org/10.1101/614172
Linlin Z. Fan
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Simon Kheifets
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Urs L. Böhm
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Kiryl D. Piatkevich
2Media Lab and McGovern Institute for Brain Research, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
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Hao Wu
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Vicente Parot
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Michael E. Xie
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
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Edward S. Boyden
2Media Lab and McGovern Institute for Brain Research, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
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Anne E. Takesian
3Harvard Medical School, Boston, USA
4Massachusetts Eye and Ear Infirmary, Boston, USA
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Adam E. Cohen
1Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA, USA
5Department of Physics, Harvard University, Cambridge, MA USA
6Howard Hughes Medical Institute
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  • For correspondence: cohen@chemistry.harvard.edu
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Abstract

The stability of neural dynamics arises through a tight coupling of excitatory (E) and inhibitory (I) signals. Genetically encoded voltage indicators (GEVIs) can report both spikes and subthreshold dynamics in vivo, but voltage only reveals the combined effects of E and I synaptic inputs, not their separate contributions individually. Here we combine optical recording of membrane voltage with simultaneous optogenetic manipulation to probe E and I individually in barrel cortex Layer 1 (L1) neurons in awake mice. Our studies reveal how the L1 microcircuit integrates thalamocortical excitation, lateral inhibition and top-down neuromodulatory inputs. We develop a simple computational model of the L1 microcircuit which captures the main features of our data. Together, these results suggest a model for computation in L1 interneurons consistent with their hypothesized role in attentional gating of the underlying cortex. Our results demonstrate that all-optical electrophysiology can reveal basic principles of neural circuit function in vivo.

One Sentence Summary All-optical electrophysiology revealed the function in awake mice of an inhibitory microcircuit in barrel cortex Layer 1.

Footnotes

  • Revised manuscript contains numerical simulations of the Layer 1 microcircuit. See section on "Numerical model of L1 microcircuit", updated Fig. 5, Supplementary Figs. 10-14 and Tables 1&2.

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 May 23, 2019.
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All-optical electrophysiology reveals excitation, inhibition, and neuromodulation in cortical layer 1
Linlin Z. Fan, Simon Kheifets, Urs L. Böhm, Kiryl D. Piatkevich, Hao Wu, Vicente Parot, Michael E. Xie, Edward S. Boyden, Anne E. Takesian, Adam E. Cohen
bioRxiv 614172; doi: https://doi.org/10.1101/614172
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All-optical electrophysiology reveals excitation, inhibition, and neuromodulation in cortical layer 1
Linlin Z. Fan, Simon Kheifets, Urs L. Böhm, Kiryl D. Piatkevich, Hao Wu, Vicente Parot, Michael E. Xie, Edward S. Boyden, Anne E. Takesian, Adam E. Cohen
bioRxiv 614172; doi: https://doi.org/10.1101/614172

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