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Genetically Encoded Voltage Indicators

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Optogenetics

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1293))

Abstract

Optogenetic approaches combine the power to allocate optogenetic tools (proteins) to specific cell populations (defined genetically or functionally) and the use of light-based interfaces between biological wetware (cells and tissues) and hardware (controllers and recorders). The optogenetic toolbox contains two main compartments: tools to interfere with cellular processes and tools to monitor cellular events. Among the latter are genetically encoded voltage indicators (GEVIs). This chapter outlines the development, current state of the art and prospects of emerging optical GEVI imaging technologies.

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Abbreviations

2p:

Two-photon

AAV:

Adeno-associated virus

AMBER:

Autonomous molecular bioluminescent reporter

Arch:

Archaerhodopsin

CGH:

Computer-generated holography

CNS:

Central nervous system

cpFP:

Circularly permuted FP

DPA:

Dipicrylamine

FP:

Fluorescent protein

FRET:

Förster resonance energy transfer

GECI:

Genetically encoded calcium indicator

GEVI:

Genetically encoded voltage indicator

GFP:

Green fluorescent protein

GRIN:

Gradient index

NIR:

Near-infrared range

ROI:

Region of interest

SNR:

Signal-to-noise ratio

VSD:

Voltage-sensing domain

VSFP:

Voltage-sensitive fluorescent protein

References

  • Abdelfattah AS, Farhi SL, Zhao Y, Brinks D, Zou P, Ruangkittisakul A, Platisa J, Pieribone VA, Ballanyi K, Cohen AE, Campbell RE (2016) A bright and fast red fluorescent protein voltage Indicator that reports neuronal activity in organotypic brain slices. J Neurosci 36:2458–2472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdelfattah AS, Kawashima T, Singh A, Novak O, Liu H, Shuai Y, Huang YC, Campagnola L, Seeman SC, Yu J, Zheng J, Grimm JB, Patel R, Friedrich J, Mensh BD, Paninski L, Macklin JJ, Murphy GJ, Podgorski K, Lin BJ, Chen TW, Turner GC, Liu Z, Koyama M, Svoboda K, Ahrens MB, Lavis LD, Schreiter ER (2019a) Bright and photostable chemigenetic indicators for extended in vivo voltage imaging. Science 365:699–704

    Article  CAS  PubMed  Google Scholar 

  • Abdelfattah AS, Valenti R, Wong A, Koyama M, Kim DS, Schreiter ER (2019b) A general approach to engineer positive-going eFRET voltage indicators. bioRxiv 690925

    Google Scholar 

  • Adam Y, Kim JJ, Lou S, Zhao Y, Xie ME, Brinks D, Wu H, Mostajo-Radji MA, Kheifets S, Parot V, Chettih S, Williams KJ, Gmeiner B, Farhi SL, Linda M, Kelly Buchanan E, Kinsella I, Zhou D, Paninski L, Harvey CD, Zeng H, Arlotta P, Campbell RE, Adam E. Cohen. (2019) Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics. Nature 569:413–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aharoni D, Hoogland TM (2019) Circuit investigations with open-source miniaturized microscopes: past, present and future. Front Cell Neurosci 13:141

    Article  PubMed  PubMed Central  Google Scholar 

  • Akemann W, Mutoh H, Perron A, Rossier J, Knopfel T (2010) Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat Methods 7:643–649

    Article  CAS  PubMed  Google Scholar 

  • Akemann W, Mutoh H, Perron A, Park YK, Iwamoto Y, Knopfel T (2012) Imaging neural circuit dynamics with a voltage-sensitive fluorescent protein. J Neurophysiol 108:2323–2337

    Article  CAS  PubMed  Google Scholar 

  • Akemann W, Sasaki M, Mutoh H, Imamura T, Honkura N, Knopfel T (2013) Two-photon voltage imaging using a genetically encoded voltage indicator. Sci Rep 3:2231

    Article  PubMed  PubMed Central  Google Scholar 

  • Antic SD, Empson RM, Knopfel T (2016) Voltage imaging to understand connections and functions of neuronal circuits. J Neurophysiol 116:135–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bando Y, Grimm C, Cornejo VH, Yuste R (2019a) Genetic voltage indicators. BMC Biol 17:71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bando Y, Sakamoto M, Kim S, Ayzenshtat I, Yuste R (2019b) Comparative evaluation of genetically encoded voltage indicators. Cell Rep 26:802–13.e4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbera G, Liang B, Zhang L, Li Y, Lin DT (2019) A wireless miniScope for deep brain imaging in freely moving mice. J Neurosci Methods 323:56–60

    Article  PubMed  PubMed Central  Google Scholar 

  • Bayguinov PO, Ma Y, Gao Y, Zhao X, Jackson MB (2017) Imaging voltage in genetically defined neuronal subpopulations with a Cre recombinase-targeted hybrid voltage sensor. J Neurosci 37:9305–9319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck C, Gong Y (2019) A high-speed, bright, red fluorescent voltage sensor to detect neural activity. Sci Rep 9:15878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borden PY, Ortiz AD, Waiblinger C, Sederberg AJ, Morrissette AE, Forest CR, Jaeger D, Stanley GB (2017) Genetically expressed voltage sensor ArcLight for imaging large scale cortical activity in the anesthetized and awake mouse. Neurophotonics 4:031212

    Article  PubMed  PubMed Central  Google Scholar 

  • Carandini M, Shimaoka D, Rossi LF, Sato TK, Benucci A, Knopfel T (2015) Imaging the awake visual cortex with a genetically encoded voltage indicator. J Neurosci 35:53–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chamberland S, Yang HH, Pan MM, Evans SW, Guan S, Chavarha M, Yang Y, Salesse C, Wu H, Wu JC, Clandinin TR, Toth K, Lin MZ, St-Pierre F (2017) Fast two-photon imaging of subcellular voltage dynamics in neuronal tissue with genetically encoded indicators. Elife 6:e25690

    Article  PubMed  PubMed Central  Google Scholar 

  • Chan KY, Jang MJ, Yoo BB, Greenbaum A, Ravi N, Wu WL, Sanchez-Guardado L, Lois C, Mazmanian SK, Deverman BE, Gradinaru V (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat Neurosci 20:1172–1179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chanda B, Blunck R, Faria LC, Schweizer FE, Mody I, Bezanilla F (2005) A hybrid approach to measuring electrical activity in genetically specified neurons. Nat Neurosci 8:1619–1626

    Article  CAS  PubMed  Google Scholar 

  • Daigle TL, Madisen L, Hage TA, Valley MT, Knoblich U, Larsen RS, Takeno MM, Huang L, Gu H, Larsen R, Mills M, Bosma-Moody A, Siverts LA, Walker M, Graybuck LT, Yao Z, Fong O, Nguyen TN, Garren E, Lenz GH, Chavarha M, Pendergraft J, Harrington J, Hirokawa KE, Harris JA, Nicovich PR, McGraw MJ, Ollerenshaw DR, Smith KA, Baker CA, Ting JT, Sunkin SM, Lecoq J, Lin MZ, Boyden ES, Murphy GJ, da Costa NM, Waters J, Li L, Tasic B, Zeng H (2018) A suite of transgenic driver and reporter mouse lines with enhanced brain-cell-type targeting and functionality. Cell 174:465–80.e22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimitrov D, He Y, Mutoh H, Baker BJ, Cohen L, Akemann W, Knopfel T (2007) Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS One 2:e440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fagerholm ED, Scott G, Shew WL, Song C, Leech R, Knopfel T, Sharp DJ (2016) Cortical entropy, mutual information and scale-free dynamics in waking mice. Cereb Cortex 26:3945–3952

    Article  PubMed  PubMed Central  Google Scholar 

  • Foust AJ, Zampini V, Tanese D, Papagiakoumou E, Emiliani V (2015) Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures. Neurophotonics 2:021007

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukuchi-Shimogori T, Grove EA (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science 294:1071–1074

    Article  CAS  PubMed  Google Scholar 

  • Gautam SG, Perron A, Mutoh H, Knopfel T (2009) Exploration of fluorescent protein voltage probes based on circularly permuted fluorescent proteins. Front Neuroeng 2:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Y, Wagner MJ, Zhong Li J, Schnitzer MJ (2014) Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors. Nat Commun 5:3674

    Article  PubMed  Google Scholar 

  • Gong Y, Huang C, Li JZ, Grewe BF, Zhang Y, Eismann S, Schnitzer MJ (2015) High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor. Science 350:1361–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grenier V, Daws BR, Liu P, Miller EW (2019) Spying on neuronal membrane potential with genetically targetable voltage indicators. J Am Chem Soc 41(3):1349–1358

    Article  CAS  Google Scholar 

  • Grimm JB, English BP, Chen J, Slaughter JP, Zhang Z, Revyakin A, Patel R, Macklin JJ, Normanno D, Singer RH, Lionnet T, Lavis LD (2015) A general method to improve fluorophores for live-cell and single-molecule microscopy. Nat Methods 12(3):244–250, 3 p following 50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hillman EM, Voleti V, Patel K, Li W, Yu H, Perez-Campos C, Benezra SE, Bruno RM, Galwaduge PT (2018) High-speed 3D imaging of cellular activity in the brain using axially-extended beams and light sheets. Curr Opin Neurobiol 50:190–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochbaum DR, Zhao Y, Farhi SL, Klapoetke N, Werley CA, Kapoor V, Zou P, Kralj JM, Maclaurin D, Smedemark-Margulies N, Saulnier JL, Boulting GL, Straub C, Cho YK, Melkonian M, Wong GK, Harrison DJ, Murthy VN, Sabatini BL, Boyden ES, Campbell RE, Cohen AE (2014) All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat Methods 11:825–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inagaki S, Tsutsui H, Suzuki K, Agetsuma M, Arai Y, Jinno Y, Bai G, Daniels MJ, Okamura Y, Matsuda T, Nagai T (2017) Genetically encoded bioluminescent voltage indicator for multi-purpose use in wide range of bioimaging. Sci Rep 7:42398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inagaki S, Agetsuma M, Ohara S, Iijima T, Yokota H, Wazawa T, Arai Y, Nagai T (2019) Imaging local brain activity of multiple freely moving mice sharing the same environment. Sci Rep 9:7460

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin L, Han Z, Platisa J, Wooltorton JRA, Cohen LB, Pieribone VA (2012) Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 75:779–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kannan M, Vasan G, Huang C, Haziza S, Li JZ, Inan H, Schnitzer MJ, Pieribone VA (2018) Fast, in vivo voltage imaging using a red fluorescent indicator. Nat Methods 15:1108–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazemipour A, Novak O, Flickinger D, Marvin JS, Abdelfattah AS, King J, Borden PM, Kim JJ, Al-Abdullatif SH, Deal PE, Miller EW, Schreiter ER, Druckmann S, Svoboda K, Looger LL, Podgorski K (2019) Kilohertz frame-rate two-photon tomography. Nat Methods 16:778–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knopfel T (2012) Genetically encoded optical indicators for the analysis of neuronal circuits. Nat Rev Neurosci 13:687–700

    Article  PubMed  CAS  Google Scholar 

  • Knopfel T, Song C (2019) Optical voltage imaging in neurons: moving from technology development to practical tool. Nat Rev Neurosci 20:719–727

    Article  CAS  PubMed  Google Scholar 

  • Kost LA, Nikitin ES, Ivanova VO, Sung U, Putintseva EV, Chudakov DM, Balaban PM, Lukyanov KA, Bogdanov AM (2017) Insertion of the voltage-sensitive domain into circularly permuted red fluorescent protein as a design for genetically encoded voltage sensor. PLoS One 12:e0184225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE (2011) Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat Methods 9:90–95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lam AJ, St-Pierre F, Gong Y, Marshall JD, Cranfill PJ, Baird MA, McKeown MR, Wiedenmann J, Davidson MW, Schnitzer MJ, Tsien RY, Lin MZ (2012) Improving FRET dynamic range with bright green and red fluorescent proteins. Nat Methods 9:1005–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S, Geiller T, Jung A, Nakajima R, Song YK, Baker BJ (2017) Improving a genetically encoded voltage indicator by modifying the cytoplasmic charge composition. Sci Rep 7:8286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu M, Song C, Liang Y, Knopfel T, Zhou C (2019) Assessing spatiotemporal variability of brain spontaneous activity by multiscale entropy and functional connectivity. Neuroimage 198:198–220

    Article  PubMed  Google Scholar 

  • Lundby A, Mutoh H, Dimitrov D, Akemann W, Knopfel T (2008) Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci-VSP voltage-sensing movements. PLoS One 3:e2514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Madisen L, Garner AR, Shimaoka D, Chuong AS, Klapoetke NC, Li L, van der Bourg A, Niino Y, Egolf L, Monetti C, Gu H, Mills M, Cheng A, Tasic B, Nguyen TN, Sunkin SM, Benucci A, Nagy A, Miyawaki A, Helmchen F, Empson RM, Knopfel T, Boyden ES, Reid RC, Carandini M, Zeng H (2015) Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85:942–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Markram H, Muller E, Ramaswamy S, Reimann MW, Abdellah M, Sanchez CA, Ailamaki A, Alonso-Nanclares L, Antille N, Arsever S, Kahou GA, Berger TK, Bilgili A, Buncic N, Chalimourda A, Chindemi G, Courcol JD, Delalondre F, Delattre V, Druckmann S, Dumusc R, Dynes J, Eilemann S, Gal E, Gevaert ME, Ghobril JP, Gidon A, Graham JW, Gupta A, Haenel V, Hay E, Heinis T, Hernando JB, Hines M, Kanari L, Keller D, Kenyon J, Khazen G, Kim Y, King JG, Kisvarday Z, Kumbhar P, Lasserre S, Le Be JV, Magalhaes BR, Merchan-Perez A, Meystre J, Morrice BR, Muller J, Munoz-Cespedes A, Muralidhar S, Muthurasa K, Nachbaur D, Newton TH, Nolte M, Ovcharenko A, Palacios J, Pastor L, Perin R, Ranjan R, Riachi I, Rodriguez JR, Riquelme JL, Rossert C, Sfyrakis K, Shi Y, Shillcock JC, Silberberg G, Silva R, Tauheed F, Telefont M, Toledo-Rodriguez M, Trankler T, Van Geit W, Diaz JV, Walker R, Wang Y, Zaninetta SM, DeFelipe J, Hill SL, Segev I, Schurmann F (2015) Reconstruction and simulation of neocortical microcircuitry. Cell 163:456–492

    Article  CAS  PubMed  Google Scholar 

  • Marshall JD, Li JZ, Zhang Y, Gong Y, St-Pierre F, Lin MZ, Schnitzer MJ (2016) Cell-type-specific optical recording of membrane voltage dynamics in freely moving mice. Cell 167:1650–62.e15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng G, Liang Y, Sarsfield S, Jiang WC, Lu R, Dudman JT, Aponte Y, Ji N (2019) High-throughput synapse-resolving two-photon fluorescence microendoscopy for deep-brain volumetric imaging in vivo. eLife 8:e40805

    Article  PubMed  PubMed Central  Google Scholar 

  • Mishina Y, Mutoh H, Knopfel T (2012) Transfer of Kv3.1 voltage sensor features to the isolated Ci-VSP voltage-sensing domain. Biophys J 103:669–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishina Y, Mutoh H, Song C, Knopfel T (2014) Exploration of genetically encoded voltage indicators based on a chimeric voltage sensing domain. Front Mol Neurosci 7:78

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyamoto D, Murayama M (2016) The fiber-optic imaging and manipulation of neural activity during animal behavior. Neurosci Res 103:1–9

    Article  PubMed  Google Scholar 

  • Nobauer T, Skocek O, Pernia-Andrade AJ, Weilguny L, Traub FM, Molodtsov MI, Vaziri A (2017) Video rate volumetric Ca2+ imaging across cortex using seeded iterative demixing (SID) microscopy. Nat Methods 14:811–818

    Article  CAS  PubMed  Google Scholar 

  • Perron A, Mutoh H, Launey T, Knopfel T (2009) Red-shifted voltage-sensitive fluorescent proteins. Chem Biol 16:1268–1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piatkevich KD, Jung EE, Straub C, Linghu C, Park D, Suk HJ, Hochbaum DR, Goodwin D, Pnevmatikakis E, Pak N, Kawashima T, Yang CT, Rhoades JL, Shemesh O, Asano S, Yoon YG, Freifeld L, Saulnier JL, Riegler C, Engert F, Hughes T, Drobizhev M, Szabo B, Ahrens MB, Flavell SW, Sabatini BL, Boyden ES (2018) A robotic multidimensional directed evolution approach applied to fluorescent voltage reporters. Nat Chem Biol 14:352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piatkevich KD, Bensussen S, Tseng HA, Shroff SN, Lopez-Huerta VG, Park D, Jung EE, Shemesh OA, Straub C, Gritton HJ, Romano MF, Costa E, Sabatini BL, Fu Z, Boyden ES, Han X (2019) Population imaging of neural activity in awake behaving mice. Nature 574:413–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quicke P, Song C, McKimm EJ, Milosevic MM, Howe CL, Neil M, Schultz SR, Antic SD, Foust AJ, Knopfel T (2019) Single-neuron level one-photon voltage imaging with sparsely targeted genetically encoded voltage indicators. Front Cell Neurosci 13:39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinn TA, Camelliti P, Rog-Zielinska EA, Siedlecka U, Poggioli T, O'Toole ET, Knopfel T, Kohl P (2016) Electrotonic coupling of excitable and nonexcitable cells in the heart revealed by optogenetics. Proc Natl Acad Sci U S A 113:14852–14857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237–246

    Article  CAS  PubMed  Google Scholar 

  • Sakai R, Repunte-Canonigo V, Raj CD, Knopfel T (2001) Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein. Eur J Neurosci 13:2314–2318

    Article  CAS  PubMed  Google Scholar 

  • Scott G, Fagerholm ED, Mutoh H, Leech R, Sharp DJ, Shew WL, Knopfel T (2014) Voltage imaging of waking mouse cortex reveals emergence of critical neuronal dynamics. J Neurosci 34:16611–16620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeman SC, Campagnola L, Davoudian PA, Hoggarth A, Hage TA, Bosma-Moody A, Baker CA, Lee JH, Mihalas S, Teeter C, Ko AL, Ojemann JG, Gwinn RP, Silbergeld DL, Cobbs C, Phillips J, Lein E, Murphy G, Koch C, Zeng H, Jarsky T (2018) Sparse recurrent excitatory connectivity in the microcircuit of the adult mouse and human cortex. eLife 7:e37349

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel MS, Isacoff EY (1997) A genetically encoded optical probe of membrane voltage. Neuron 19:735–741

    Article  CAS  PubMed  Google Scholar 

  • Skocek O, Nobauer T, Weilguny L, Traub FM, Xia CN, Molodtsov MI, Grama A, Yamagata M, Aharoni D, Cox DD, Golshani P, Vaziri A (2018) High-speed volumetric imaging of neuronal activity in freely moving rodents. Nat Methods 15:429–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song C, Do QB, Antic SD, Knopfel T (2017) Transgenic strategies for sparse but strong expression of genetically encoded voltage and calcium indicators. Int J Mol Sci 18:1461

    Article  PubMed Central  CAS  Google Scholar 

  • Song C, Piscopo DM, Niell CM, Knopfel T (2018) Cortical signatures of wakeful somatosensory processing. Sci Rep 8:11977

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srinivasan P, Griffin NM, Joshi P, Thakur D, Nguyen-Le A, McCotter S, Jain A, Saeidi M, Kulkarni P, Eisdorfer J, Rothman J, Montell C, Theogarajan L 2019 An autonomous molecular bioluminescent reporter (AMBER) for voltage imaging in freely moving animals. bioRxiv, 845198

    Google Scholar 

  • St-Pierre F, Marshall JD, Yang Y, Gong Y, Schnitzer MJ, Lin MZ (2014) High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci 17:884–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundukova M, Prifti E, Bucci A, Kirillova K, Serrao J, Reymond L, Umebayashi M, Hovius R, Riezman H, Johnsson K, Heppenstall PA (2019) A chemogenetic approach for the optical monitoring of voltage in neurons. Angew Chem Int Ed Engl 58:2341–2344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sung U, Sepehri-Rad M, Piao HH, Jin L, Hughes T, Cohen LB, Baker BJ (2015) Developing fast fluorescent protein voltage sensors by optimizing FRET interactions. PLoS One 10:e0141585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865–872

    Article  CAS  PubMed  Google Scholar 

  • Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008) Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5:683–685

    Article  CAS  PubMed  Google Scholar 

  • van Opbergen CJM, Koopman CD, Kok BJM, Knopfel T, Renninger SL, Orger MB, Vos MA, van Veen TAB, Bakkers J, de Boer TP (2018) Optogenetic sensors in the zebrafish heart: a novel in vivo electrophysiological tool to study cardiac arrhythmogenesis. Theranostics 8:4750–4764

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Villette V, Chavarha M, Dimov IK, Bradley J, Pradhan L, Mathieu B, Evans SW, Chamberland S, Shi D, Yang R, Kim BB, Ayon A, Jalil A, St-Pierre F, Schnitzer MJ, Bi G, Toth K, Ding J, Dieudonne S, Lin MZ (2019) Ultrafast two-photon imaging of a high-gain voltage Indicator in awake behaving mice. Cell 179:1590–608.e23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Zhang Z, Chanda B, Jackson MB (2010) Improved probes for hybrid voltage sensor imaging. Biophys J 99:2355–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng H, Horie K, Madisen L, Pavlova MN, Gragerova G, Rohde AD, Schimpf BA, Liang Y, Ojala E, Kramer F, Roth P, Slobodskaya O, Dolka I, Southon EA, Tessarollo L, Bornfeldt KE, Gragerov A, Pavlakis GN, Gaitanaris GA (2008) An inducible and reversible mouse genetic rescue system. PLoS Genet 4:e1000069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zou P, Zhao Y, Douglass AD, Hochbaum DR, Brinks D, Werley CA, Harrison DJ, Campbell RE, Cohen AE (2014) Bright and fast multicoloured voltage reporters via electrochromic FRET. Nat Commun 5:4625

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Work in our laboratory is supported by grants from the BRAIN initiative (US National Institutes of Health, U01MH109091, U01NS099573).

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Authors and Affiliations

  1. Laboratory for Neuronal Circuit Dynamics, Imperial College London, London, UK

    Irene Mollinedo-Gajate, Chenchen Song & Thomas Knöpfel

Authors
  1. Irene Mollinedo-Gajate
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  2. Chenchen Song
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  3. Thomas Knöpfel
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Correspondence to Thomas Knöpfel .

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Editors and Affiliations

  1. The Institute for Solid State Physics, The University of Tokyo, Kashiwa, Japan

    Hiromu Yawo

  2. OptoBioTechnology Research Center, Nagoya Institute of Technology, Nagoya, Japan

    Hideki Kandori

  3. National Institutes of Natural Sciences, Tokyo, Japan

    Amane Koizumi

  4. Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan

    Ryoichiro Kageyama

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Mollinedo-Gajate, I., Song, C., Knöpfel, T. (2021). Genetically Encoded Voltage Indicators. In: Yawo, H., Kandori, H., Koizumi, A., Kageyama, R. (eds) Optogenetics. Advances in Experimental Medicine and Biology, vol 1293. Springer, Singapore. https://doi.org/10.1007/978-981-15-8763-4_12

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