Widefield imaging of rapid pan-cortical voltage dynamics with an indicator evolved for one-photon microscopy

Xiaoyu Lu, Yunmiao Wang, Zhuohe Liu, Yueyang Gou, Dieter Jaeger () and François St-Pierre ()
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Xiaoyu Lu: Systems, Synthetic, and Physical Biology Program, Rice University
Yunmiao Wang: Neuroscience Graduate Program, Emory University
Zhuohe Liu: Department of Electrical and Computer Engineering, Rice University
Yueyang Gou: Department of Neuroscience, Baylor College of Medicine
Dieter Jaeger: Biology Department, Emory University
François St-Pierre: Systems, Synthetic, and Physical Biology Program, Rice University

Nature Communications, 2023, vol. 14, issue 1, 1-22

Abstract: Abstract Widefield imaging with genetically encoded voltage indicators (GEVIs) is a promising approach for understanding the role of large cortical networks in the neural coding of behavior. However, the limited performance of current GEVIs restricts their deployment for single-trial imaging of rapid neuronal voltage dynamics. Here, we developed a high-throughput platform to screen for GEVIs that combine fast kinetics with high brightness, sensitivity, and photostability under widefield one-photon illumination. Rounds of directed evolution produced JEDI-1P, a green-emitting fluorescent indicator with enhanced performance across all metrics. Next, we optimized a neonatal intracerebroventricular delivery method to achieve cost-effective and wide-spread JEDI-1P expression in mice. We also developed an approach to correct optical measurements from hemodynamic and motion artifacts effectively. Finally, we achieved stable brain-wide voltage imaging and successfully tracked gamma-frequency whisker and visual stimulations in awake mice in single trials, opening the door to investigating the role of high-frequency signals in brain computations.

Date: 2023
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DOI: 10.1038/s41467-023-41975-3

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