Sustained deep-tissue voltage recording using a fast indicator evolved for two-photon microscopy

Liu, Zhuohe; Lu, Xiaoyu; Villette, Vincent; Gou, Yueyang; Colbert, Kevin L.; Lai, Syeling; Guan, Sihui; Land, Michelle A.; Lee, Jihwan; Assefa, Tensae; Zollinger, Daniel R.; Korympidou, Maria M.; Vlasits, Anna; Pang, Michelle M; Su, Shiwei; Cai, Changjia; Froudarakis, Emmanouil; Zhou, Na; Patel, Saumil S.; Cw, Smith; Ayon, Annick; Bizouard, P.; Bradley, Jonathan; Franke, Katrin; Clandinin, Thomas R.; Giovannucci, Andrea; Tolias, Andreas S.; Reimer, Jacob; Dieudonné, Stéphane; St-Pierre, François

doi:10.1016/j.cell.2022.07.013

Cited by 81 publications

(86 citation statements)

References 85 publications

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“…2c ). We did not compare JEDI-1P to JEDI-2P, a GEVI evolved for two-photon microscopy, because JEDI-2P has comparable performance to ASAP3 under one-photon widefield imaging 42 .…”

Section: Resultsmentioning

confidence: 99%

“…Indicator properties -response amplitude, kinetics, brightness, and photostability -can be dependent on the illumination modality [39][40][41] . Therefore, we sought to develop a platform customized to screen GEVIs for widefield (one-photon) imaging, in contrast to our parallel efforts to screen under two-photon excitation 42 . Many indicator screening efforts illustrate that mutations can improve a performance metric that was evaluated during screening while impairing others that were not quantified 21 .…”

Section: Enabling Multiparametric Gevi Screening Under Widefield One-...mentioning

confidence: 99%

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Detecting rapid pan-cortical voltage dynamics in vivo with a brighter and faster voltage indicator

Wang

Gou

et al. 2022

Preprint

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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 slow kinetics of current GEVIs limit 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 whose performance is improved for 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 effectively correct optical measurements from hemodynamic and motion artifacts. 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.

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“…2c ). We did not compare JEDI-1P to JEDI-2P, a GEVI evolved for two-photon microscopy, because JEDI-2P has comparable performance to ASAP3 under one-photon widefield imaging 42 .…”

Section: Resultsmentioning

confidence: 99%

Section: Enabling Multiparametric Gevi Screening Under Widefield One-...mentioning

confidence: 99%

Detecting rapid pan-cortical voltage dynamics in vivo with a brighter and faster voltage indicator

Wang

Gou

et al. 2022

Preprint

Self Cite

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“…The lack of temporal resolution precludes longitudinal analyses of cellular dynamics and the screening for critical POD temporal properties, including photostability, response kinetics, and the peak amplitude of transient responses. 38,60 To mitigate this problem, custom microfluidic chips were designed to measure fluorescence before and after cells are presented with an analyte 61 or submitted to a photobleaching laser pulse. 62,63 The sorting speed of these devices is lower than that of conventional FACS systems by orders of magnitude.…”

Section: ■ Automating Multiwell Plate Screeningmentioning

confidence: 99%

Automating the High-Throughput Screening of Protein-Based Optical Indicators and Actuators

et al. 2022

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Over the last 25 years, protein engineers have developed an impressive collection of optical tools to interface with biological systems: indicators to eavesdrop on cellular activity and actuators to poke and prod native processes. To reach the performance level required for their downstream applications, protein-based tools are usually sculpted by iterative rounds of mutagenesis. In each round, libraries of variants are made and evaluated, and the most promising hits are then retrieved, sequenced, and further characterized. Early efforts to engineer protein-based optical tools were largely manual, suffering from low throughput, human error, and tedium. Here, we describe approaches to automating the screening of libraries generated as colonies on agar, multiwell plates, and pooled populations of single-cell variants. We also briefly discuss emerging approaches for screening, including cell-free systems and machine learning.

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“…VSD-based GEVIs offer comparatively lower signal-to-noise ratio and slower kinetics but are currently the best option for measuring responses in vivo . Among these, the ASAP family is very promising ( Villette et al, 2019 ), and the most recent variant, JEDI-2P, offers state-of-the-art kinetics, signal-to-noise ratio, and photostability under 2-photon excitation ( Liu et al, 2022 ). For example, JEDI-2P allowed successful in vivo 2-photon imaging of action potentials from neurons in neocortical layer 5 and long-duration dual recording of neighboring neurons in layer 2/3 ( Liu et al, 2022 ).…”

Section: Cell-type Specific Expression Of Genetically Encoded Voltage...mentioning

confidence: 99%

“…Among these, the ASAP family is very promising ( Villette et al, 2019 ), and the most recent variant, JEDI-2P, offers state-of-the-art kinetics, signal-to-noise ratio, and photostability under 2-photon excitation ( Liu et al, 2022 ). For example, JEDI-2P allowed successful in vivo 2-photon imaging of action potentials from neurons in neocortical layer 5 and long-duration dual recording of neighboring neurons in layer 2/3 ( Liu et al, 2022 ). As both VSD- and rhodopsin-based GEVIs improve, they will allow advanced optical interrogation of membrane voltage of specific neuronal subtypes in vivo .…”

Section: Cell-type Specific Expression Of Genetically Encoded Voltage...mentioning

confidence: 99%

Advances in approaches to study cell-type specific cortical circuits throughout development

Hanson

Wester²

2022

Front. Cell. Neurosci.

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Neurons in the neocortex and hippocampus are diverse and form synaptic connections that depend on their type. Recent work has improved our understanding of neuronal cell-types and how to target them for experiments. This is crucial for investigating cortical circuit architecture, as the current catalog of established cell-type specific circuit motifs is small relative to the diversity of neuronal subtypes. Some of these motifs are found throughout the cortex, suggesting they are canonical circuits necessary for basic computations. However, the extent to which circuit organization is stereotyped across the brain or varies by cortical region remains unclear. Cortical circuits are also plastic, and their organization evolves throughout each developmental stage. Thus, experimental access to neuronal subtypes with temporal control is essential for studying cortical structure and function. In this mini review, we highlight several recent advances to target specific neuronal subtypes and study their synaptic connectivity and physiology throughout development. We emphasize approaches that combine multiple techniques, provide examples of successful applications, and describe potential future applications of novel tools.

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Sustained deep-tissue voltage recording using a fast indicator evolved for two-photon microscopy

Cited by 81 publications

References 85 publications

Detecting rapid pan-cortical voltage dynamics in vivo with a brighter and faster voltage indicator

Detecting rapid pan-cortical voltage dynamics in vivo with a brighter and faster voltage indicator

Automating the High-Throughput Screening of Protein-Based Optical Indicators and Actuators

Advances in approaches to study cell-type specific cortical circuits throughout development

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