GCaMP – a Family of Single-Fluorophore Genetically Encoded Calcium Indicators
- Autores: Erofeev A.1, Vinokurov E.1, Vlasova O.1, Bezprozvanny I.1,2
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Afiliações:
- Laboratory of molecular neurodegeneration, Institute of Biomedical Systems and Biotechnology, Peter the Great St. Petersburg Polytechnic University
- Department of Physiology, University of Texas Southwestern Medical Center at Dallas
- Edição: Volume 109, Nº 7 (2023)
- Páginas: 819-843
- Seção: ОБЗОРНЫЕ И ПРОБЛЕМНЫЕ СТАТЬИ
- URL: https://journals.rcsi.science/0869-8139/article/view/137962
- DOI: https://doi.org/10.31857/S0869813923070038
- EDN: https://elibrary.ru/XHKZHO
- ID: 137962
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Resumo
Single fluorophore genetically encoded calcium indicators (GECIs) such as GCaMP are widely utilized tools for investigating neuronal activity. Their primary advantage lies in their capacity to provide real-time and highly sensitive responses to fluctuations in intracellular calcium ion concentrations. This characteristic is of significant importance when studying neuronal processes and ensembles, wherein calcium signals play a crucial role in information transmission. This comprehensive review focuses on the GCaMP family, encompassing an analysis of their various types, distinctive features, and potential applications for visualizing neuronal activity. Special attention is dedicated to the ongoing advancements in GCaMP technology, particularly the endeavors to expand their spectral properties and enhance their capability to detect high-frequency spike activity.
Palavras-chave
Sobre autores
A. Erofeev
Laboratory of molecular neurodegeneration, Institute of Biomedical Systems and Biotechnology,Peter the Great St. Petersburg Polytechnic University
Autor responsável pela correspondência
Email: alexandr.erofeew@gmail.com
Russia, St. Petersburg
E. Vinokurov
Laboratory of molecular neurodegeneration, Institute of Biomedical Systems and Biotechnology,Peter the Great St. Petersburg Polytechnic University
Email: alexandr.erofeew@gmail.com
Russia, St. Petersburg
O. Vlasova
Laboratory of molecular neurodegeneration, Institute of Biomedical Systems and Biotechnology,Peter the Great St. Petersburg Polytechnic University
Email: alexandr.erofeew@gmail.com
Russia, St. Petersburg
I. Bezprozvanny
Laboratory of molecular neurodegeneration, Institute of Biomedical Systems and Biotechnology,Peter the Great St. Petersburg Polytechnic University; Department of Physiology, University of Texas Southwestern Medical Center at Dallas
Email: alexandr.erofeew@gmail.com
Russia, St. Petersburg; United States of America, Dallas, TX
Bibliografia
- Grienberger C, Konnerth A (2012) Imaging calcium in neurons. Neuron 73: 862–885. https://doi.org/10.1016/j.neuron.2012.02.011
- Russell JT (2011) Imaging calcium signals in vivo: a powerful tool in physiology and pharmacology. Br J Pharmacol 163: 1605–1625. https://doi.org/10.1111/j.1476-5381.2010.00988.x
- Ghosh A, Greenberg ME (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268: 239–247. https://doi.org/10.1126/science.7716515
- Kawamoto EM, Vivar C, Camandola S (2012) Physiology and pathology of calcium signaling in the brain. Front Pharmacol 3: 61. https://doi.org/10.3389/fphar.2012.00061
- Tsien RY, Pozzan T, Rink TJ (1982) Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol 94: 325–334. https://doi.org/10.1083/jcb.94.2.325
- Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440–3450.
- Tsien RY (1981) A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290: 527–528. https://doi.org/10.1038/290527a0
- Inoue M (2021) Genetically encoded calcium indicators to probe complex brain circuit dynamics in vivo. Neurosci Res 169: 2–8. https://doi.org/10.1016/j.neures.2020.05.013
- Reck-Peterson SL, Derr ND, Stuurman N (2010) Imaging single molecules using total internal reflection fluorescence microscopy (TIRFM). Cold Spring Harb Protoc 2010: pdb top73. https://doi.org/10.1101/pdb.top73
- Toseland CP (2013) Fluorescent labeling and modification of proteins. J Chem Biol 6: 85–95. https://doi.org/10.1007/s12154-013-0094-5
- Renz M (2013) Fluorescence microscopy-a historical and technical perspective. Cytometry A 83: 767–779. https://doi.org/10.1002/cyto.a.22295
- Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger L, Svoboda K, Kim DS (2013) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499: 295–300. https://doi.org/10.1038/nature12354
- Lin MZ, Schnitzer MJ (2016) Genetically encoded indicators of neuronal activity. Nat Neurosci 19: 1142–1153. https://doi.org/10.1038/nn.4359
- Carafoli E (2003) The calcium-signalling saga: tap water and protein crystals. Nat Rev Mol Cell Biol 4: 326–332. https://doi.org/10.1038/nrm1073
- Pchitskaya E, Popugaeva E, Bezprozvanny I (2018) Calcium signaling and molecular mechanisms underlying neurodegenerative diseases. Cell Calcium 70: 87–94. https://doi.org/10.1016/j.ceca.2017.06.008
- Supnet C, Bezprozvanny I (2010) Neuronal calcium signaling, mitochondrial dysfunction, and Alzheimer’s disease. J Alzheimers Dis 20 Suppl 2: S487–S498. https://doi.org/10.3233/JAD-2010-100306
- Sabatini BL, Svoboda K (2000) Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408: 589–593. https://doi.org/10.1038/35046076
- Kim TH, Schnitzer MJ (2022) Fluorescence imaging of large-scale neural ensemble dynamics. Cell 185: 9–41. https://doi.org/10.1016/j.cell.2021.12.007
- Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K (2004) Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE 2004: pl5. https://doi.org/10.1126/stke.2192004pl5
- Tank DW, Sugimori M, Connor JA, Llinas RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242: 773–777. https://doi.org/10.1126/science.2847315
- Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388: 882–887. https://doi.org/10.1038/42264
- Rose T, Goltstein PM, Portugues R, Griesbeck O (2014) Putting a finishing touch on GECIs. Front Mol Neurosci 7: 88. https://doi.org/10.3389/fnmol.2014.00088
- Ashley CC (1969) Aequorin-monitored calcium transients in single Maia muscle fibres. J Physiol 203: 32P–33P.
- Ashley CC, Ridgway EB (1968) Simultaneous recording of membrane potential, calcium transient and tension in single muscle fibers. Nature 219: 1168–1169. https://doi.org/10.1038/2191168a0
- Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59: 223–239. https://doi.org/10.1002/jcp.1030590302
- Mank M, Griesbeck O (2008) Genetically encoded calcium indicators. Chem Rev 108: 1550–1564. https://doi.org/10.1021/cr078213v
- Heim R, Tsien RY (1996) Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6: 178–182. https://doi.org/10.1016/s0960-9822(02)00450-5
- Porumb T, Yau P, Harvey TS, Ikura M (1994) A calmodulin-target peptide hybrid molecule with unique calcium-binding properties. Protein Eng 7: 109–115. https://doi.org/10.1093/protein/7.1.109
- Romoser VA, Hinkle PM, Persechini A (1997) Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence. A new class of fluorescent indicators. J Biol Chem 272: 13270–13274. https://doi.org/10.1074/jbc.272.20.13270
- Siegel MS, Isacoff EY (1997) A genetically encoded optical probe of membrane voltage. Neuron 19: 735–741. https://doi.org/10.1016/s0896-6273(00)80955-1
- Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192–195. https://doi.org/10.1038/28190
- Thestrup T, Litzlbauer J, Bartholomaus I, Mues M, Russo L, Dana H, Kovalchuk Y, Liang Y, Kalamakis G, Laukat Y, Becker S, Witte G, Geiger A, Allen T, Rome LC, Chen TW, Kim DS, Garaschuk O, Griesinger C, Griesbeck O (2014) Optimized ratiometric calcium sensors for functional in vivo imaging of neurons and T lymphocytes. Nat Methods 11: 175–182. https://doi.org/10.1038/nmeth.2773
- Palmer AE, Tsien RY (2006) Measuring calcium signaling using genetically targetable fluorescent indicators. Nat Protoc 1: 1057–1065. https://doi.org/10.1038/nprot.2006.172
- Mank M, Santos AF, Direnberger S, Mrsic-Flogel TD, Hofer SB, Stein V, Hendel T, Reiff DF, Levelt C, Borst A, Bonhoeffer T, Hubener M, Griesbeck O (2008) A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5: 805–811. https://doi.org/10.1038/nmeth.1243
- Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101: 10554–10559. https://doi.org/10.1073/pnas.0400417101
- Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR (2000) Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26: 583–594. https://doi.org/10.1016/s0896-6273(00)81196-4
- Boulin T, Hobert O (2012) From genes to function: the C. elegans genetic toolbox. Wiley Interdiscip Rev Dev Biol 1: 114–137. https://doi.org/10.1002/wdev.1
- Higashijima S, Masino MA, Mandel G, Fetcho JR (2003) Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 90: 3986–3997. https://doi.org/10.1152/jn.00576.2003
- Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112: 271–282. https://doi.org/10.1016/s0092-8674(03)00004-7
- Hasan MT, Friedrich RW, Euler T, Larkum ME, Giese G, Both M, Duebel J, Waters J, Bujard H, Griesbeck O, Tsien RY, Nagai T, Miyawaki A, Denk W (2004) Functional fluorescent Ca2+ indicator proteins in transgenic mice under TET control. PLoS Biol 2: e163. https://doi.org/10.1371/journal.pbio.0020163
- Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875–881. https://doi.org/10.1038/nmeth.1398
- Heider B, Nathanson JL, Isacoff EY, Callaway EM, Siegel RM (2010) Two-photon imaging of calcium in virally transfected striate cortical neurons of behaving monkey. PLoS One 5: e13829. https://doi.org/10.1371/journal.pone.0013829
- Yin L, Masella B, Dalkara D, Zhang J, Flannery JG, Schaffer DV, Williams DR, Merigan WH (2014) Imaging light responses of foveal ganglion cells in the living macaque eye. J Neurosci 34: 6596–665. https://doi.org/10.1523/JNEUROSCI.4438-13.2014
- Mollinedo-Gajate I, Song C, Knopfel T (2019) Genetically Encoded Fluorescent Calcium and Voltage Indicators. Handb Exp Pharmacol 260: 209–229. https://doi.org/10.1007/164_2019_299
- Mao T, O’Connor DH, Scheuss V, Nakai J, Svoboda K (2008) Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS One 3: e1796. https://doi.org/10.1371/journal.pone.0001796
- Stosiek C, Garaschuk O, Holthoff K, Konnerth A 2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A 100: 7319–7324. https://doi.org/10.1073/pnas.1232232100
- Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM (2013) Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494: 238–242. https://doi.org/10.1038/nature11846
- Bozza T, McGann JP, Mombaerts P, Wachowiak M (2004) In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42: 9–21. https://doi.org/10.1016/s0896-6273(04)00144-8
- Kaifosh P, Lovett-Barron M, Turi GF, Reardon TR, Losonczy A (2013) Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat Neurosci 16: 1182–1184. https://doi.org/10.1038/nn.3482
- Knopfel T (2012) Genetically encoded optical indicators for the analysis of neuronal circuits. Nat Rev Neurosci 13: 687–700. https://doi.org/10.1038/nrn3293
- Steinmetz NA, Aydin C, Lebedeva A, Okun M, Pachitariu M, Bauza M, Beau M, Bhagat J, Bohm C, Broux M, Chen S, Colonell J, Gardner R J, Karsh B, Kloosterman F, Kostadinov D, Mora-Lopez C, O’Callaghan J, Park J, Putzeys J, Sauerbrei B, van Daal R JJ, Vollan AZ, Wang S, Welkenhuysen M, Ye Z, Dudman JT, Dutta B, Hantman AW, Harris KD, Lee A, Moser EI, O’Keefe J, Renart A, Svoboda K, Hausser M, Haesler S, Carandini M, Harris T D (2021) Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings. Science 372. https://doi.org/10.1126/science.abf4588
- Erofeev A, Antifeev I, Bolshakova A, Bezprozvanny I, Vlasova O (2022) In Vivo Penetrating Microelectrodes for Brain Electrophysiology. Sensors (Basel) 22. https://doi.org/10.3390/s22239085
- Margolis DJ, Lutcke H, Schulz K, Haiss F, Weber B, Kugler S, Hasan MT, Helmchen F (2012) Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nat Neurosci 15: 1539–1546. https://doi.org/10.1038/nn.3240
- Patriarchi T, Cho JR, Merten K, Howe MW, Marley A, Xiong WH, Folk RW, Broussard G J, Liang R, Jang MJ, Zhong H, Dombeck D, von Zastrow M, Nimmerjahn A, Gradinaru V, Williams JT, Tian L (2018) Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors. Science 360. https://doi.org/10.1126/science.aat4422
- Sabatini BL, Tian L (2020) Imaging Neurotransmitter and Neuromodulator Dynamics In Vivo with Genetically Encoded Indicators. Neuron 108: 17–32. https://doi.org/10.1016/j.neuron.2020.09.036
- Emiliani V, Cohen AE, Deisseroth K, Hausser M (2015) All-Optical Interrogation of Neural Circuits. J Neurosci 35: 13917–13926. https://doi.org/10.1523/JNEUROSCI.2916-15.2015
- Kuhn B, Ozden I, Lampi Y, Hasan MT, Wang SS (2012) An amplified promoter system for targeted expression of calcium indicator proteins in the cerebellar cortex. Front Neural Circuits 6: 49. https://doi.org/10.3389/fncir.2012.00049
- Resendez SL, Jennings JH, Ung RL, Namboodiri VM, Zhou ZC, Otis JM, McHenry JA, Kosyk O, Stuber GD (2016) Visualization of cortical, subcortical and deep brain neural circuit dynamics during naturalistic mammalian behavior with head-mounted microscopes and chronically implanted lenses. Nat Protoc 11: 566–597. https://doi.org/10.1038/nprot.2016.021
- Bedbrook CN, Deverman BE, Gradinaru V (2018) Viral Strategies for Targeting the Central and Peripheral Nervous Systems. Annu Rev Neurosci 41: 323–348. https://doi.org/10.1146/annurev-neuro-080317-062048
- Haery L, Deverman BE, Matho KS, Cetin A, Woodard K, Cepko C, Guerin KI, Rego MA, Ersing I, Bachle SM, Kamens J, Fan M (2019) Adeno-Associated Virus Technologies and Methods for Targeted Neuronal Manipulation. Front Neuroanat 13: 93. https://doi.org/10.3389/fnana.2019.00093
- Chan KY, Jang MJ, Yoo BB, Greenbaum A, Ravi N, Wu WL, Sanchez-Guardado L, Lois C, Mazmanian SK, Deverman BE, Gradinaru C (2017) Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat Neurosci 20: 1172–1179. https://doi.org/10.1038/nn.4593
- Allen WE, Kauvar IV, Chen MZ, Richman EB, Yang SJ, Chan K, Gradinaru V, Deverman BE, Luo L, Deisseroth K (2017) Global Representations of Goal-Directed Behavior in Distinct Cell Types of Mouse Neocortex. Neuron 94: 891–907 e896. https://doi.org/10.1016/j.neuron.2017.04.017
- Helmchen F, Imoto K, Sakmann B (1996) Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys J 70: 1069–1081. https://doi.org/10.1016/S0006-3495(96)79653-4
- Helmchen F, Borst JG, Sakmann B (1997) Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72: 1458–1471. https://doi.org/10.1016/S0006-3495(97)78792-7
- Yang Y, Liu N, He Y, Liu Y, Ge L, Zou L, Song S, Xiong W, Liu X (2018) Improved calcium sensor GCaMP-X overcomes the calcium channel perturbations induced by the calmodulin in GCaMP. Nat Commun 9: 1504. https://doi.org/10.1038/s41467-018-03719-6
- Jurado LA, Chockalingam PS, Jrrett HW (1999) Apocalmodulin. Physiol Rev 79: 661–682. https://doi.org/10.1152/physrev.1999.79.3.661
- Marvin JS, Borghuis BG, Tian L, Cichon J, Harnett MT, Akerboom J, Gordus A, Renninger SL, Chen TW, Bargmann CI, Orger MB, Schreiter ER, Demb JB, Gan WB, Hires SA, Looger LL (2013) An optimized fluorescent probe for visualizing glutamate neurotransmission. Nat Methods 10: 162–170. https://doi.org/10.1038/nmeth.2333
- Zhao Y, Araki S, Wu J, Teramoto T, Chang YF, Nakano M, Abdelfattah AS, Fujiwara M, Ishihara T, Nagai T, Campbell RE (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333: 1888–1891. https://doi.org/10.1126/science.1208592
- Dana H, Mohar B, Sun Y, Narayan S, Gordus A, Hasseman JP, Tsegaye G, Holt GT, Hu A, Walpita D, Patel R, Macklin JJ, Bargmann CI, Ahrens MB, Schreiter ER, Jayaraman V, Looger LL, Svoboda K, Kim DS (2016) Sensitive red protein calcium indicators for imaging neural activity. Elife 5. https://doi.org/10.7554/eLife.12727
- Wu SY, Shen Y, Shkolnikov I, Campbell RE (2022) Fluorescent Indicators For Biological Imaging of Monatomic Ions. Front Cell Dev Biol 10: 885440. https://doi.org/10.3389/fcell.2022.885440
- Shen Y, Wu SY, Rancic V, Aggarwal A, Qian Y, Miyashita SI, Ballanyi K, Campbell RE, Dong M (2019) Genetically encoded fluorescent indicators for imaging intracellular potassium ion concentration. Commun Biol 2: 18. https://doi.org/10.1038/s42003-018-0269-2
- Helassa N, Podor B, Fine A, Torok (2016) Design and mechanistic insight into ultrafast calcium indicators for monitoring intracellular calcium dynamics. Sci Rep 6: 38276. https://doi.org/10.1038/srep38276
- Badura A, Sun XR, Giovannucci A, Lynch LA, Wang SS (2014) Fast calcium sensor proteins for monitoring neural activity. Neurophotonics 1: 025008. https://doi.org/10.1117/1.NPh.1.2.025008
- Bovetti S, Moretti C, Fellin T (2014) Mapping brain circuit function in vivo using two-photon fluorescence microscopy. Microsc Res Tech 77: 492–501. https://doi.org/10.1002/jemt.22342
- Baird GS, Zacharias DA, Tsien RY (1999) Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 96: 11241–11246. https://doi.org/10.1073/pnas.96.20.11241
- Nagai T, Sawano A, Park ES, Miyawaki A (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc Natl Acad Sci U S A 98: 3197–3202. https://doi.org/10.1073/pnas.051636098
- Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat Biotechnol 19: 137–141. https://doi.org/10.1038/84397
- Souslova EA, Belousov VV, Lock JG, Stromblad S, Kasparov S, Bolshakov AP, Pinelis V G, Labas YA, Lukyanov S, Mayr LM, Chudakov DM (2007) Single fluorescent protein-based Ca2+ sensors with increased dynamic range. BMC Biotechnol 7: 37. https://doi.org/10.1186/1472-6750-7-37
- Fletcher ML, Masurkar AV, Xing J, Imamura F, Xiong W, Nagayama S, Mutoh H, Greer C, Knopfel T, Chen WR (2009) Optical imaging of postsynaptic odor representation in the glomerular layer of the mouse olfactory bulb. J Neurophysiol 102: 817–830. https://doi.org/10.1152/jn.00020.2009
- Dombeck DA, Harvey CD, Tian L, Looger LL, Tank DW (2010) Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat Neurosci 13: 1433–1440. https://doi.org/10.1038/nn.2648
- Akerboom J, Rivera JD, Guilbe MM, Malave EC, Hernandez HH, Tian L, Hires SA, Marvin JS, Looger LL, Schreiter ER (2009) Crystal structures of the GCaMP calcium sensor reveal the mechanism of luorescence signal change and aid rational design. J Biol Chem 284: 6455–6464. https://doi.org/10.1074/jbc.M807657200
- Iseppon F, Linley JE, Wood JN (2022) Calcium imaging for analgesic drug discovery. Neurobiol Pain 11: 100083. https://doi.org/10.1016/j.ynpai.2021.100083
- Muto A, Ohkura M, Kotani T, Higashijima S, Nakai J, Kawakami K (2011) Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish. Proc Natl Acad Sci U S A 108: 5425 –5430. https://doi.org/10.1073/pnas.1000887108
- Chen Q, Cichon J, Wang W, Qiu L, Lee SJ, Campbell NR, Destefino N, Goard MJ, Fu Z, Yasuda R, Looger LL, Arenkiel BR, Gan WB, Feng G (2012) Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76: 297–308. https://doi.org/10.1016/j.neuron.2012.07.011
- Ouzounov DG, Wang T, Wu C, Xu C (2019) GCaMP6 DeltaF/F dependence on the excitation wavelength in 3-photon and 2-photon microscopy of mouse brain activity. Biomed Opt Express 10: 3343–3352. https://doi.org/10.1364/BOE.10.003343
- Hires SA, Tian L, Looger LL (2008) Reporting neural activity with genetically encoded calcium indicators. Brain Cell Biol 36: 69–86. https://doi.org/10.1007/s11068-008-9029-4
- Perez Koldenkova V, Nagai T (2013) Genetically encoded Ca(2+) indicators: properties and evaluation. Biochim Biophys Acta 1833: 1787–1797. https://doi.org/10.1016/j.bbamcr.2013.01.011
- Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J (2005) Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem 77: 5861–5869. https://doi.org/10.1021/ac0506837
- Tallini YN, Ohkura M, Choi BR, Ji G, Imoto K, Doran R, Lee J, Plan P, Wilson J, Xin HB, Sanbe A, Gulick J, Mathai J, Robbins J, Salama G, Nakai J, Kotlikoff MI (2006) Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc Natl Acad Sci U S A 103: 4753–4758. https://doi.org/10.1073/pnas.0509378103
- Sun XR, Badura A, Pacheco DA, Lynch LA, Schneider ER, Taylor MP, Hogue IB, Enquist LW, Murthy M, Wang SS (2013) Fast GCaMPs for improved tracking of neuronal activity. Nat Commun 4: 2170. https://doi.org/10.1038/ncomms3170
- Shindo A, Hara Y, Yamamoto TS, Ohkura M, Nakai J, Ueno N (2010) Tissue-tissue interaction-triggered calcium elevation is required for cell polarization during Xenopus gastrulation. PLoS One 5: e8897. https://doi.org/10.1371/journal.pone.0008897
- Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderon NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32: 13819–13840. https://doi.org/10.1523/JNEUROSCI.2601-12.2012
- Dana H, Sun Y, Mohar B, Hulse BK, Kerlin AM, Hasseman JP, Tsegaye G, Tsang A, Wong A, Patel R, Macklin JJ, Chen Y, Konnerth A, Jayaraman V, Looger LL, Schreiter ER, Svoboda K, Kim DS (2019) High-performance calcium sensors for imaging activity in neuronal populations and microcompartments. Nat Methods 16: 649–657. https://doi.org/10.1038/s41592-019-0435-6
- Zhang Y, Looger LL (2023) Fast and sensitive GCaMP calcium indicators for neuronal imaging. J Physiol 10: 1113/JP283832. https://doi.org/10.1113/JP283832
- Broussard GJ, Liang R, Tian L (2014) Monitoring activity in neural circuits with genetically encoded indicators. Front Mol Neurosci 7: 97. https://doi.org/10.3389/fnmol.2014.00097
- Ohkura M, Sasaki T, Sadakari J, Gengyo-Ando K, Kagawa-Nagamura Y, Kobayashi C, Ikegaya Y, Nakai J (2012) Genetically encoded green fluorescent Ca2+ indicators with improved detectability for neuronal Ca2+ signals. PLoS One 7: e51286. https://doi.org/10.1371/journal.pone.0051286
- Muto A, Ohkura M, Abe G, Nakai J, Kawakami K (2013) Real-time visualization of neuronal activity during perception. Curr Biol 23: 307–311. https://doi.org/10.1016/j.cub.2012.12.040
- Shiba Y, Gomibuchi T, Seto T, Wada Y, Ichimura H, Tanaka Y, Ogasawara T, Okada K, Shiba N, Sakamoto K, Ido D, Shiina T, Ohkura M, Nakai J, Uno N, Kazuki Y, Oshimura M, Minami I, Ikeda U (2016) Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature 538: 388–391. https://doi.org/10.1038/nature19815
- Sakamoto M, Inoue M, Takeuchi A, Kobari S, Yokoyama T, Horigane SI, Takemoto-Kimura S, Abe M, Sakimura K, Kano M, Kitamura K, Fujii H, Bito H (2022) A Flp-dependent G-CaMP9a transgenic mouse for neuronal imaging in vivo. Cell Rep Methods 2: 100168. https://doi.org/10.1016/j.crmeth.2022.100168
- Helassa N, Zhang XH, Conte I, Scaringi J, Esposito E, Bradley J, Carter T, Ogden D, Morad M, Torok K (2015) Fast-Response Calmodulin-Based Fluorescent Indicators Reveal Rapid Intracellular Calcium Dynamics. Sci Rep 5: 15978. https://doi.org/10.1038/srep15978
- Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485: 471–477. https://doi.org/10.1038/nature11057
- Dunn TW, Mu Y, Narayan S, Randlett O, Naumann EA, Yang CT, Schier AF, Freeman J, Engert F, Ahrens M (2016) Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion. Elife 5: e12741. https://doi.org/10.7554/eLife.12741
- Venkatachalam V, Ji N, Wang X, Clark C, Mitchell JK, Klein M, Tabone CJ, Florman J, Ji H, Greenwood J, Chisholm AD, Srinivasan J, Alkema M, Zhen M, Samuel AD (2016) Pan-neuronal imaging in roaming Caenorhabditis elegans. Proc Natl Acad Sci U S A 113: E1082–E1088. https://doi.org/10.1073/pnas.1507109113
- Nguyen JP, Shipley FB, Linder AN, Plummer GS, Liu M, Setru SU, Shaevitz JW, Leifer AM (2016) Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans. Proc Natl Acad Sci U S A 113: E1074–E1081. https://doi.org/10.1073/pnas.1507110112
- Peters AJ, Chen SX, Komiyama T (2014) Emergence of reproducible spatiotemporal activity during motor learning. Nature 510: 263–267. https://doi.org/10.1038/nature13235
- Ziv Y, Burns L, Cocker ED, Hamel EO, Ghosh KK, Kitch LJ, El Gamal A, Schnitzer MJ (2013) Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci 16: 264–266. https://doi.org/10.1038/nn.3329
- Lovett-Barron M, Kaifosh P, Kheirbek MA, Danielson N, Zaremba JD, Reardon TR, Turi GF, Hen R, Zemelman BV, Losonczy A (2014) Dendritic inhibition in the hippocampus supports fear learning. Science 343: 857–863. https://doi.org/10.1126/science.1247485
- Siegel F, Lohmann C (2013) Probing synaptic function in dendrites with calcium imaging. Exp Neurol 242: 27–32. https://doi.org/10.1016/j.expneurol.2012.02.007
- Kotlikoff MI (2007) Genetically encoded Ca2+ indicators: using genetics and molecular design to understand complex physiology. J Physiol 578: 55–67. https://doi.org/10.1113/jphysiol.2006.120212
- Diez-Garcia J, Matsushita S, Mutoh H, Nakai J, Ohkura M, Yokoyama J, Dimitrov D, Knopfel T (2005) Activation of cerebellar parallel fibers monitored in transgenic mice expressing a fluorescent Ca2+ indicator protein. Eur J Neurosci 22: 627–635. https://doi.org/10.1111/j.1460-9568.2005.04250.x
- Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW (2012) A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32: 3131–3141. https://doi.org/10.1523/JNEUROSCI.4469-11.2012
- Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE (2014) Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron 82: 1263–1270. https://doi.org/10.1016/j.neuron.2014.04.038
- O'Connor DH, Peron SP, Huber D, Svoboda K (2010) Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67: 1048–1061. https://doi.org/10.1016/j.neuron.2010.08.026
- Huber D, Gutnisky DA, Peron S, O’Connor DH, Wiegert JS, Tian L, Oertner TG, Looger LL, Svoboda K (2012) Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484: 473–478. https://doi.org/10.1038/nature11039
- Mittmann W, Wallace DJ, Czubayko U, Herb JT, Schaefer AT, Looger LL, Denk W, Kerr JN (2011) Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat Neurosci 14: 1089–1093. https://doi.org/10.1038/nn.2879
- Borghuis BG, Tian L, Xu Y, Nikonov SS, Vardi N, Zemelman BV, Looger LL (2011) Imaging light responses of targeted neuron populations in the rodent retina. J Neurosci 31: 2855–2867. https://doi.org/10.1523/JNEUROSCI.6064-10.2011
- Del Bene F, Wyart C, Robles E, Tran A, Looger L, Scott EK, Isacoff EY, Baier H (2010) Filtering of visual information in the tectum by an identified neural circuit. Science 330: 669–673. https://doi.org/10.1126/science.1192949
- Chiappe ME, Seelig JD, Reiser MB, Jayaraman V (2010) Walking modulates speed sensitivity in Drosophila motion vision. Curr Biol 20: 1470–1475. https://doi.org/10.1016/j.cub.2010.06.072
- Akerboom J, Carreras Calderon N, Tian L, Wabnig S, Prigge M, Tolo J, Gordus A, Orger MB, Severi KE, Macklin JJ, Patel R, Pulver SR, Wardill TJ, Fischer E, Schuler C, Chen T W, Sarkisyan KS, Marvin JS, Bargmann CI, Kim DS, Kugler S, Lagnado L, Hegemann P, Gottschalk A, Schreiter ER, Looger LL (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6: 2. https://doi.org/10.3389/fnmol.2013.00002
- Melom JE, Akbergenova Y, Gavornik JP, Littleton JT (2013) Spontaneous and evoked release are independently regulated at individual active zones. J Neurosci 33: 17253–17263. https://doi.org/10.1523/JNEUROSCI.3334-13.2013
- Cichon J, Gan WB (2015) Branch-specific dendritic Ca(2+) spikes cause persistent synaptic plasticity. Nature 520: 180–185. https://doi.org/10.1038/nature14251
- Sheffield ME, Dombeck DA (2015) Calcium transient prevalence across the dendritic arbour predicts place field properties. Nature 517: 200–204. https://doi.org/10.1038/nature13871
- Sun W, Tan Z, Mensh BD, Ji N (2016) Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs. Nat Neurosci 19: 308–315. https://doi.org/10.1038/nn.4196
- Aharoni D, Khakh BS, Silva AJ, Golshani P (2019) All the light that we can see: a new era in miniaturized microscopy. Nat Methods 16: 11–13. https://doi.org/10.1038/s41592-018-0266-x
- Boyd AM, Kato HK, Komiyama T, Isaacson JS (2015) Broadcasting of cortical activity to the olfactory bulb. Cell Rep 10: 1032–1039. https://doi.org/10.1016/j.celrep.2015.01.047
- Dana H, Chen TW, Hu A, Shields BC, Guo C, Looger LL, Kim DS, Svoboda K (2014) Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS One 9: e108697. https://doi.org/10.1371/journal.pone.0108697
- Hinckley CA, Alaynick WA, Gallarda BW, Hayashi M, Hilde KL, Driscoll SP, Dekker JD, Tucker HO, Sharpee TO, Pfaff S (2015) Spinal Locomotor Circuits Develop Using Hierarchical Rules Based on Motorneuron Position and Identity. Neuron 87: 1008–1021. https://doi.org/10.1016/j.neuron.2015.08.005
- Theis L, Berens P, Froudarakis E, Reimer J, Roman Roson M, Baden T, Euler T, Tolias A S, Bethge ER (2016) Benchmarking Spike Rate Inference in Population Calcium Imaging. Neuron 90: 471–482. https://doi.org/10.1016/j.neuron.2016.04.014
- Heckscher ES, Zarin AA, Faumont S, Clark MQ, Manning L, Fushiki A, Schneider-Mizell CM, Fetter RD, Truman JW, Zwart M F, Landgraf M, Cardona A, Lockery SR, Doe CQ (2015) Even-Skipped(+) Interneurons Are Core Components of a Sensorimotor Circuit that Maintains Left-Right Symmetric Muscle Contraction Amplitude. Neuron 88: 314–329. https://doi.org/10.1016/j.neuron.2015.09.009
- Grover D, Katsuki T, Greenspan RJ (2016) Flyception: imaging brain activity in freely walking fruit flies. Nat Methods 13: 569–572. https://doi.org/10.1038/nmeth.3866
- Inoue M, Takeuchi A, Manita S, Horigane SI, Sakamoto M, Kawakami R, Yamaguchi K, Otomo K, Yokoyama H, Kim R, Yokoyama T, Takemoto-Kimura S, Abe M, Okamura M, Kondo Y, Quirin S, Ramakrishnan C, Imamura T, Sakimura K, Nemoto T, Kano M, Fujii H, Deisseroth K, Kitamura K, Bito H (2019) Rational Engineering of XCaMPs, a Multicolor GECI Suite for In Vivo Imaging of Complex Brain Circuit Dynamics. Cell 177: 1346–1360 e1324. https://doi.org/10.1016/j.cell.2019.04.007
- Mohr MA, Bushey D, Aggarwal A, Marvin JS, Kim JJ, Marquez EJ, Liang Y, Patel R, Macklin JJ, Lee CY, Tsang A, Tsegaye G, Ahrens AM, Chen JL, Kim DS, Wong AM, Looger LL, Schreiter ER, Podgorski K (2020) jYCaMP: an optimized calcium indicator for two-photon imaging at fiber laser wavelengths. Nat Methods 17: 694–697. https://doi.org/10.1038/s41592-020-0835-7
- Shcherbakova DM (2021) Near-infrared and far-red genetically encoded indicators of neuronal activity. J Neurosci Methods 362: 109314. https://doi.org/10.1016/j.jneumeth.2021.109314
- Qian Y, Piatkevich KD, Mc Larney B, Abdelfattah AS, Mehta S, Murdock MH, Gottschalk S, Molina RS, Zhang W, Chen Y, Wu J, Drobizhev M, Hughes TE, Zhang J, Schreiter ER, Shoham S, Razansky D, Boyden ES, Campbell RE (2019) A genetically encoded near-infrared fluorescent calcium ion indicator. Nat Methods 16: 171–174. https://doi.org/10.1038/s41592-018-0294-6
- Shemetov AA, Monakhov MV, Zhang Q, Canton-Josh JE, Kumar M, Chen M, Matlashov ME, Li X, Yang W, Nie L, Shcherbakova DM, Kozorovitskiy Y, Yao J, Ji N, Verkhusha VV (2021) A near-infrared genetically encoded calcium indicator for in vivo imaging. Nat Biotechnol 39: 368–377. https://doi.org/10.1038/s41587-020-0710-1
- Shen Y, Dana H, Abdelfattah AS, Patel R, Shea J, Molina R S, Rawal B, Rancic V, Chang YF, Wu L, Chen Y, Qian Y, Wiens MD, Hambleton N, Ballanyi K, Hughes TE, Drobizhev M, Kim DS, Koyama M, Schreiter ER, Campbell R E (2018) A genetically encoded Ca(2+) indicator based on circularly permutated sea anemone red fluorescent protein eqFP578. BMC Biol 16: 9. https://doi.org/10.1186/s12915-018-0480-0
- Sonoda K, Matsui T, Bito H, Ohki K (2018) Astrocytes in the mouse visual cortex reliably respond to visual stimulation. Biochem Biophys Res Commun 505: 1216–1222. https://doi.org/10.1016/j.bbrc.2018.10.027
- Bindocci E, Savtchouk I, Liaudet N, Becker D, Carriero G, Volterra A (2017) Three-dimensional Ca2+ imaging advances understanding of astrocyte biology. Science 356. https://doi.org/10.1126/science.aai8185
- Yap KL, Kim J, Truong K, Sherman M, Yuan T, Ikura M (2000) Calmodulin target database. J Struct Funct Genomics 1: 8–14. https://doi.org/10.1023/a:1011320027914