Development of optical methods for real-time whole-brain functional imaging of zebrafish neuronal activity

Export citation

Selected format

Usage statistics policy

  • 13Full-text Downloads

Cita come:
Turrini, L.; 2020; Development of optical methods for real-time whole-brain functional imaging of zebrafish neuronal activity. Firenze, Firenze University Press.


Distributori


Indici e aggregatori bibliometrici

Development of optical methods for real-time whole-brain functional imaging of zebrafish neuronal activity

Lapo Turrini
University of Florence, Italy - ORCID: 0000-0003-2519-7893

+ More about the authors
DOI: 10.36253/978-88-5518-070-2 Series: Premio Tesi di Dottorato ISSN 2612-8039 (print) - ISSN 2612-8020 (online)

FUP Scientific Cloud for Books

© 2020 Author(s)
Published by Firenze University Press

Content licence CC BY 4.0
Metadata licence CC0 1.0

Each one of us in his life has, at least once, smelled the scent of roses, read one canto of Dante’s Commedia or listened to the sound of the sea from a shell. All of this is possible thanks to the astonishing capabilities of an organ, such as the brain, that allows us to collect and organize perceptions coming from sensory organs and to produce behavioural responses accordingly. Studying an operating brain in a non-invasive way is extremely difficult in mammals, and particularly in humans. In the last decade, a small teleost fish, zebrafish (Danio rerio), has been making its way into the field of neurosciences. The brain of a larval zebrafish is made up of 'only' 100000 neurons and it’s completely transparent, making it possible to optically access it. Here, taking advantage of the best of currently available technology, we devised optical solutions to investigate the dynamics of neuronal activity throughout the entire brain of zebrafish larvae.

Read more

Keywords: zebrafish, calcium imaging, light-sheet microscopy, epilepsy, behaviour

Formats

Print

Publication year: 2020

Price: 12,90 €

Pages: 200

ISSN print: 2612-8039

ISBN: 978-88-5518-069-6

Printed edition forthcoming

Order now

5% Discount (or more using a coupon)

PDF

Publication year: 2020

Pages: 200

ISSN online: 2612-8020

e-ISBN: 978-88-5518-070-2

DOI: 10.36253/978-88-5518-070-2

Download PDF

© 2020 Author(s)
Content licence CC BY 4.0
Metadata licence CC0 1.0

XML

Publication year: 2020

ISSN online: 2612-8020

e-ISBN: 978-88-5518-071-9

DOI: 10.36253/978-88-5518-070-2

Download XML

© 2020 Author(s)
Content licence CC BY 4.0
Metadata licence CC0 1.0

  1. Abraham, E., Palevitch, O., Gothilf, Y., and Zohar, Y. (2009). The zebrafish as a model system for forebrain GnRH neuronal development. Gen Comp Endocrinol 164, 151-160 10.1016/j.ygcen.2009.01.012
  2. Afrikanova, T., Serruys, A.S., Buenafe, O.E., Clinckers, R., Smolders, I., De Witte, P.A., Crawford, A.D., and Esguerra, C.V. (2013). Validation of the zebrafish pentylenetetrazol seizure model: locomotor versus electrographic responses to antiepileptic drugs. PLoS One 8, e54166 10.1371/journal.pone.0054166
  3. Ahrens, M.B., Orger, M.B., Robson, D.N., Li, J.M., and Keller, P.J. (2013). Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10, 413-420 10.1038/nmeth.2434
  4. Akerboom, J., Chen, T.W., Wardill, T.J., Tian, L., Marvin, J.S., Mutlu, S., Calderon, N.C., Esposti, F., Borghuis, B.G., Sun, X.R., Gordus, A., Orger, M.B., Portugues, R., Engert, F., Macklin, J.J., Filosa, A., Aggarwal, A., Kerr, R.A., Takagi, R., Kracun, S., Shigetomi, E., Khakh, B.S., Baier, H., Lagnado, L., Wang, S.S., Bargmann, C.I., Kimmel, B.E., Jayaraman, V., Svoboda, K., Kim, D.S., Schreiter, E.R., and Looger, L.L. (2012). Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32, 13819-13840 10.1523/JNEUROSCI.2601-12.2012
  5. Akerboom, J., Rivera, J.D., Guilbe, M.M., Malave, E.C., Hernandez, H.H., Tian, L., Hires, S.A., Marvin, J.S., Looger, L.L., and Schreiter, E.R. (2009). Crystal structures of the GCaMP calcium sensor reveal the mechanism of fluorescence signal change and aid rational design. J Biol Chem 284, 6455-6464 10.1074/jbc.M807657200
  6. Allegra Mascaro, A.L., Conti, E., Lai, S., Di Giovanna, A.P., Spalletti, C., Alia, C., Panarese, A., Scaglione, A., Sacconi, L., Micera, S., Caleo, M., and Pavone, F.S. (2019). Combined Rehabilitation Promotes the Recovery of Structural and Functional Features of Healthy Neuronal Networks after Stroke. Cell Rep 28, 3474-3485 e3476 10.1016/j.celrep.2019.08.062
  7. Attili, S., and Hughes, S.M. (2014). Anaesthetic tricaine acts preferentially on neural voltage-gated sodium channels and fails to block directly evoked muscle contraction. PLoS One 9, e103751 10.1371/journal.pone.0103751
  8. Attwell, D., Buchan, A.M., Charpak, S., Lauritzen, M., Macvicar, B.A., and Newman, E.A. (2010). Glial and neuronal control of brain blood flow. Nature 468, 232-243 10.1038/nature09613
  9. Azevedo, F.A., Carvalho, L.R., Grinberg, L.T., Farfel, J.M., Ferretti, R.E., Leite, R.E., Jacob Filho, W., Lent, R., and Herculano-Houzel, S. (2009). Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513, 532-541 10.1002/cne.21974
  10. Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (1999). Circular permutation and receptor insertion within green fluorescent proteins. Proc Natl Acad Sci U S A 96, 11241-11246
  11. Baker, P.F., Hodgkin, A.L., and Ridgway, E.B. (1971). Depolarization and calcium entry in squid giant axons. J Physiol 218, 709-755
  12. Baraban, S.C., Dinday, M.T., and Hortopan, G.A. (2013). Drug screening in Scn1a zebrafish mutant identifies clemizole as a potential Dravet syndrome treatment. Nat Commun 4, 2410 10.1038/ncomms3410
  13. Baraban, S.C., Taylor, M.R., Castro, P.A., and Baier, H. (2005). Pentylenetetrazole induced changes in zebrafish behavior, neural activity and c-fos expression. Neuroscience 131, 759-768 10.1016/j.neuroscience.2004.11.031
  14. Barbazuk, W.B., Korf, I., Kadavi, C., Heyen, J., Tate, S., Wun, E., Bedell, J.A., Mcpherson, J.D., and Johnson, S.L. (2000). The syntenic relationship of the zebrafish and human genomes. Genome Res 10, 1351-1358
  15. Bargmann, C.I. (1998). Neurobiology of the Caenorhabditis elegans genome. Science 282, 2028-2033
  16. Baumgart, E., and Kubitscheck, U. (2012). Scanned light sheet microscopy with confocal slit detection. Opt Express 20, 21805-21814 10.1364/OE.20.021805
  17. Baxendale, S., Holdsworth, C.J., Meza Santoscoy, P.L., Harrison, M.R., Fox, J., Parkin, C.A., Ingham, P.W., and Cunliffe, V.T. (2012). Identification of compounds with anti-convulsant properties in a zebrafish model of epileptic seizures. Dis Model Mech 5, 773-784 10.1242/dmm.010090
  18. Blader, P., and Strahle, U. (2000). Zebrafish developmental genetics and central nervous system development. Hum Mol Genet 9, 945-951
  19. Burgess, N., and O'keefe, J. (2003). Neural representations in human spatial memory. Trends Cogn Sci 7, 517-519
  20. Candelier, R., Murmu, M.S., Romano, S.A., Jouary, A., Debregeas, G., and Sumbre, G. (2015). A microfluidic device to study neuronal and motor responses to acute chemical stimuli in zebrafish. Sci Rep 5, 12196 10.1038/srep12196
  21. Chaigneau, E., Ronzitti, E., Gajowa, M.A., Soler-Llavina, G.J., Tanese, D., Brureau, A.Y., Papagiakoumou, E., Zeng, H., and Emiliani, V. (2016). Two-Photon Holographic Stimulation of ReaChR. Front Cell Neurosci 10, 234 10.3389/fncel.2016.00234
  22. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W., and Prasher, D.C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805
  23. Chattoraj, M., King, B.A., Bublitz, G.U., and Boxer, S.G. (1996). Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer. Proc Natl Acad Sci U S A 93, 8362-8367
  24. Chen, B.R., Kozberg, M.G., Bouchard, M.B., Shaik, M.A., and Hillman, E.M. (2014). A critical role for the vascular endothelium in functional neurovascular coupling in the brain. J Am Heart Assoc 3, e000787 10.1161/JAHA.114.000787
  25. Chen, T.W., Wardill, T.J., Sun, Y., Pulver, S.R., Renninger, S.L., Baohan, A., Schreiter, E.R., Kerr, R.A., Orger, M.B., Jayaraman, V., Looger, L.L., Svoboda, K., and Kim, D.S. (2013). Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 10.1038/nature12354
  26. Chen, Y., Glaser, A., and Liu, J.T. (2017). Bessel-beam illumination in dual-axis confocal microscopy mitigates resolution degradation caused by refractive heterogeneities. J Biophotonics 10, 68-74 10.1002/jbio.201600196
  27. Chhabria, K., Plant, K., Bandmann, O., Wilkinson, R., Martin, C., Kugler, E., Armitage, P., Santoscoy, P., Cunliffe, V.T., Huisken, J., Mcgown, A., Ramesh, R., Chico, T., and Howarth, C. (2018). The effect of Hyperglycemia on neurovascular coupling and cerebrovascular patterning in zebrafish. Journal of Cerebral Blood Flow and Metabolism
  28. Chitalia, R., Mueller, J., Fu, H.L., Whitley, M.J., Kirsch, D.G., Brown, J.Q., Willett, R., and Ramanujam, N. (2016). Algorithms for differentiating between images of heterogeneous tissue across fluorescence microscopes. Biomed Opt Express 7, 3412-3424 10.1364/BOE.7.003412
  29. Cho, S.J., Byun, D., Nam, T.S., Choi, S.Y., Lee, B.G., Kim, M.K., and Kim, S. (2017). Zebrafish as an animal model in epilepsy studies with multichannel EEG recordings. Sci Rep 7, 3099 10.1038/s41598-017-03482-6
  30. Cong, L., Wang, Z., Chai, Y., Hang, W., Shang, C., Yang, W., Bai, L., Du, J., Wang, K., and Wen, Q. (2017). Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio). Elife 6, 10.7554/eLife.28158
  31. Conti, E., Allegra Mascaro, A.L., and Pavone, F.S. (2019). Large Scale Double-Path Illumination System with Split Field of View for the All-Optical Study of Inter-and Intra-Hemispheric Functional Connectivity on Mice. Methods Protoc 2, 10.3390/mps2010011
  32. Craggs, T.D. (2009). Green fluorescent protein: structure, folding and chromophore maturation. Chem Soc Rev 38, 2865-2875 10.1039/b903641p
  33. Creaser C.W. (1934). The technique of handling the zebrafish (Brachydanio rerio) for the production of eggs which are favourable for embryological research and are available at any specified time throughout the year. Copeia 159-161
  34. Crocini, C., Ferrantini, C., Coppini, R., Scardigli, M., Yan, P., Loew, L.M., Smith, G., Cerbai, E., Poggesi, C., Pavone, F.S., and Sacconi, L. (2016). Optogenetics design of mechanistically-based stimulation patterns for cardiac defibrillation. Sci Rep 6, 35628 10.1038/srep35628
  35. Cubitt, A.B., Heim, R., Adams, S.R., Boyd, A.E., Gross, L.A., and Tsien, R.Y. (1995). Understanding, improving and using green fluorescent proteins. Trends Biochem Sci 20, 448-455
  36. Dekens, M.P., Foulkes, N.S., and Tessmar-Raible, K. (2017). Instrument design and protocol for the study of light controlled processes in aquatic organisms, and its application to examine the effect of infrared light on zebrafish. PLoS One 12, e0172038 10.1371/journal.pone.0172038
  37. Denk, W., Strickler, J.H., and Webb, W.W. (1990). Two-photon laser scanning fluorescence microscopy. Science 248, 73-76
  38. Dinday, M.T., and Baraban, S.C. (2015). Large-Scale Phenotype-Based Antiepileptic Drug Screening in a Zebrafish Model of Dravet Syndrome. eNeuro 2, 10.1523/ENEURO.0068-15.2015
  39. Dombeck, D.A., Harvey, C.D., Tian, L., Looger, L.L., and Tank, D.W. (2010). Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat Neurosci 13, 1433-1440 10.1038/nn.2648
  40. Duchen, M.R. (1999). Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J Physiol 516 ( Pt 1), 1-17
  41. Dunn, T.W., Gebhardt, C., Naumann, E.A., Riegler, C., Ahrens, M.B., Engert, F., and Del Bene, F. (2016). Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish. Neuron 89, 613-628 10.1016/j.neuron.2015.12.021
  42. Dunn, T.W., Mu, Y., Narayan, S., Randlett, O., Naumann, E.A., Yang, C.T., Schier, A.F., Freeman, J., Engert, F., and Ahrens, M.B. (2016). Brain-wide mapping of neural activity controlling zebrafish exploratory locomotion. Elife 5, e12741 10.7554/eLife.12741
  43. Dunsby, C. (2008). Optically sectioned imaging by oblique plane microscopy. Opt Express 16, 20306-20316
  44. Durnin, J. (1987). Exact solution for nondiffracting beams. Journal of the Optical Society of America A 4, 651-654
  45. Durnin, J., Miceli, J., Jr., and Eberly, J.H. (1987). Diffraction-free beams. Phys Rev Lett 58, 1499-1501 10.1103/PhysRevLett.58.1499
  46. Eimon, P.M., Ghannad-Rezaie, M., De Rienzo, G., Allalou, A., Wu, Y., Gao, M., Roy, A., Skolnick, J., and Yanik, M.F. (2018). Brain activity patterns in high-throughput electrophysiology screen predict both drug efficacies and side effects. Nat Commun 9, 219 10.1038/s41467-017-02404-4
  47. Emran, F., Rihel, J., Adolph, A.R., and Dowling, J.E. (2010). Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A 107, 6034-6039 10.1073/pnas.0914718107
  48. Ernst, L.D., and Boudreau, E.A. (2016). Recent advances in epilepsy management. Curr Opin Anaesthesiol 29, 558-562 10.1097/ACO.0000000000000376
  49. Ester, M., Kriegel, H., Sander, J., and Xu, X. (1996). A density-based algorithm for discovering clusters in large spatial databases with noise. Proceeding of the Second International Conference on Knowledge Discovery and Data Mining KDD-96, 226-231
  50. Ferrer, I., Soriano, E., Del Rio, J.A., Alcantara, S., and Auladell, C. (1992). Cell death and removal in the cerebral cortex during development. Prog Neurobiol 39, 1-43
  51. Finlay, B.L., and Slattery, M. (1983). Local differences in the amount of early cell death in neocortex predict adult local specializations. Science 219, 1349-1351
  52. Fosque, B.F., Sun, Y., Dana, H., Yang, C.T., Ohyama, T., Tadross, M.R., Patel, R., Zlatic, M., Kim, D.S., Ahrens, M.B., Jayaraman, V., Looger, L.L., and Schreiter, E.R. (2015). Neural circuits. Labeling of active neural circuits in vivo with designed calcium integrators. Science 347, 755-760 10.1126/science.1260922
  53. Freeman, J., Vladimirov, N., Kawashima, T., Mu, Y., Sofroniew, N.J., Bennett, D.V., Rosen, J., Yang, C.T., Looger, L.L., and Ahrens, M.B. (2014). Mapping brain activity at scale with cluster computing. Nat Methods 11, 941-950 10.1038/nmeth.3041
  54. Friedrich, J., Zhou, P., and Paninski, L. (2017). Fast online deconvolution of calcium imaging data. PLoS Comput Biol 13, e1005423 10.1371/journal.pcbi.1005423
  55. Galland, R., Grenci, G., Aravind, A., Viasnoff, V., Studer, V., and Sibarita, J.B. (2015). 3D high- and super-resolution imaging using single-objective SPIM. Nat Methods 12, 641-644 10.1038/nmeth.3402
  56. Garcia-Campmany, L., Stam, F.J., and Goulding, M. (2010). From circuits to behaviour: motor networks in vertebrates. Curr Opin Neurobiol 20, 116-125 10.1016/j.conb.2010.01.002
  57. Gebhardt, J.C., Suter, D.M., Roy, R., Zhao, Z.W., Chapman, A.R., Basu, S., Maniatis, T., and Xie, X.S. (2013). Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat Methods 10, 421-426 10.1038/nmeth.2411
  58. Gee, K.R., Brown, K.A., Chen, W.N., Bishop-Stewart, J., Gray, D., and Johnson, I. (2000). Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes. Cell Calcium 27, 97-106 10.1054/ceca.1999.0095
  59. Go, C., and Snead, O.C., 3rd (2008). Pharmacologically intractable epilepsy in children: diagnosis and preoperative evaluation. Neurosurg Focus 25, E2 10.3171/FOC/2008/25/9/E2
  60. Goldman D.E. (1943). Potential, Impedance, and Rectification in Membranes. J Gen Physiol 27, 37-60
  61. Golgi, C. (1885). Sulla fina anatomia degli organi centrali del sistema nervoso.
  62. Göppert-Mayer, M. (1931). Uber elementarakte mit zwei quantensprüngen. Ann Phys 9, 273-294
  63. Granato, M., and Nusslein-Volhard, C. (1996). Fishing for genes controlling development. Curr Opin Genet Dev 6, 461-468
  64. Greenberg, D.S., Houweling, A.R., and Kerr, J.N. (2008). Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci 11, 749-751 10.1038/nn.2140
  65. Grynkiewicz, G., Poenie, M., and Tsien, R.Y. (1985). A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 3440-3450
  66. Guggiana-Nilo, D.A., and Engert, F. (2016). Properties of the Visible Light Phototaxis and UV Avoidance Behaviors in the Larval Zebrafish. Front Behav Neurosci 10, 160 10.3389/fnbeh.2016.00160
  67. Ha, T., and Tinnefeld, P. (2012). Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu Rev Phys Chem 63, 595-617 10.1146/annurev-physchem-032210-103340
  68. Haesemeyer, M., Robson, D.N., Li, J.M., Schier, A.F., and Engert, F. (2018). A Brain-wide Circuit Model of Heat-Evoked Swimming Behavior in Larval Zebrafish. Neuron 98, 817-831 e816 10.1016/j.neuron.2018.04.013
  69. Hallett, M., and Carbone, E. (1972). Studies of calcium influx into squid giant axons with aequorin. J Cell Physiol 80, 219-226 10.1002/jcp.1040800208
  70. Hastings J.W., and Morin J.G. (1969). Comparative biochemestry of calcium-activated photoproteins from the ctenophore, Mnemiopsis and the coelenterates Aequorea, Obelia, Pelagia and Renilla. Biology Bulletin 137, 402
  71. Hatta, K., and Kimmel, C.B. (1993). Midline structures and central nervous system coordinates in zebrafish. Perspect Dev Neurobiol 1, 257-268
  72. Hayashi, Y., Yawata, S., Funabiki, K., and Hikida, T. (2017). In vivo calcium imaging from dentate granule cells with wide-field fluorescence microscopy. PLoS One 12, e0180452 10.1371/journal.pone.0180452
  73. Heim, R., Cubitt, A.B., and Tsien, R.Y. (1995). Improved green fluorescent. Nature 373, 663-664
  74. Heim, R., Prasher, D.C., and Tsien, R.Y. (1994). Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc Natl Acad Sci U S A 91, 12501-12504
  75. Heim, R., and Tsien, R.Y. (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr Biol 6, 178-182
  76. Hewapathirane, D.S., Dunfield, D., Yen, W., Chen, S., and Haas, K. (2008). In vivo imaging of seizure activity in a novel developmental seizure model. Exp Neurol 211, 480-488 10.1016/j.expneurol.2008.02.012
  77. Higashijima, S., Mandel, G., and Fetcho, J.R. (2004). Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J Comp Neurol 480, 1-18 10.1002/cne.20278
  78. Hodgkin, A.L., and Huxley, A.F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117, 500-544
  79. Hodgkin, A.L., and Katz, B. (1949). The effect of sodium ions on the electrical activity of the giant axon of the squid. Journal of Physiology 108, 37-77
  80. Holtmaat, A., Bonhoeffer, T., Chow, D.K., Chuckowree, J., De Paola, V., Hofer, S.B., Hubener, M., Keck, T., Knott, G., Lee, W.C., Mostany, R., Mrsic-Flogel, T.D., Nedivi, E., Portera-Cailliau, C., Svoboda, K., Trachtenberg, J.T., and Wilbrecht, L. (2009). Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat Protoc 4, 1128-1144 10.1038/nprot.2009.89
  81. Hong, S., Lee, P., Baraban, S.C., and Lee, L.P. (2016). A Novel Long-term, Multi-Channel and Non-invasive Electrophysiology Platform for Zebrafish. Sci Rep 6, 28248 10.1038/srep28248
  82. Hortopan, G.A., Dinday, M.T., and Baraban, S.C. (2010). Zebrafish as a model for studying genetic aspects of epilepsy. Dis Model Mech 3, 144-148 10.1242/dmm.002139
  83. Howe, K., Clark, M.D., Torroja, C.F., Torrance, J., Berthelot, C., Muffato, M., Collins, J.E., Humphray, S., Mclaren, K., Matthews, L., Mclaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J.C., Koch, R., Rauch, G.J., White, S., Chow, W., Kilian, B., Quintais, L.T., Guerra-Assuncao, J.A., Zhou, Y., Gu, Y., Yen, J., Vogel, J.H., Eyre, T., Redmond, S., Banerjee, R., Chi, J., Fu, B., Langley, E., Maguire, S.F., Laird, G.K., Lloyd, D., Kenyon, E., Donaldson, S., Sehra, H., Almeida-King, J., Loveland, J., Trevanion, S., Jones, M., Quail, M., Willey, D., Hunt, A., Burton, J., Sims, S., Mclay, K., Plumb, B., Davis, J., Clee, C., Oliver, K., Clark, R., Riddle, C., Elliot, D., Threadgold, G., Harden, G., Ware, D., Begum, S., Mortimore, B., Kerry, G., Heath, P., Phillimore, B., Tracey, A., Corby, N., Dunn, M., Johnson, C., Wood, J., Clark, S., Pelan, S., Griffiths, G., Smith, M., Glithero, R., Howden, P., Barker, N., Lloyd, C., Stevens, C., Harley, J., Holt, K., Panagiotidis, G., Lovell, J., Beasley, H., Henderson, C., Gordon, D., Auger, K., Wright, D., Collins, J., Raisen, C., Dyer, L., Leung, K., Robertson, L., Ambridge, K., Leongamornlert, D., Mcguire, S., Gilderthorp, R., Griffiths, C., Manthravadi, D., Nichol, S., Barker, G., et al. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503 10.1038/nature12111
  84. Huang, R.Q., Bell-Horner, C.L., Dibas, M.I., Covey, D.F., Drewe, J.A., and Dillon, G.H. (2001). Pentylenetetrazole-induced inhibition of recombinant gamma-aminobutyric acid type A (GABA(A)) receptors: mechanism and site of action. J Pharmacol Exp Ther 298, 986-995
  85. Huisken, J., and Stainier, D.Y. (2007). Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM). Opt Lett 32, 2608-2610
  86. Huisken, J., and Stainier, D.Y. (2009). Selective plane illumination microscopy techniques in developmental biology. Development 136, 1963-1975 10.1242/dev.022426
  87. Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J., and Stelzer, E.H. (2004). Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007-1009 10.1126/science.1100035
  88. Inouye S., and Sasaki S. (2006). Blue fluorescent protein from the calcium-sensitive photoprotein aequorin: catalytic properties for the oxidation of coelenterazine as an oxygenase. FEBS Letters 580, 1977-1982
  89. Itoh, M., Kim, C.H., Palardy, G., Oda, T., Jiang, Y.J., Maust, D., Yeo, S.Y., Lorick, K., Wright, G.J., Ariza-Mcnaughton, L., Weissman, A.M., Lewis, J., Chandrasekharappa, S.C., and Chitnis, A.B. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev Cell 4, 67-82
  90. Jia, H., Rochefort, N.L., Chen, X., and Konnerth, A. (2011). In vivo two-photon imaging of sensory-evoked dendritic calcium signals in cortical neurons. Nat Protoc 6, 28-35 10.1038/nprot.2010.169
  91. Johnson F.H., Shimomura O., and Saiga Y. (1962). Action of cyanide on Cypridina luciferin. J Cell Comp Physiol 59, 265-272
  92. Johnson F.H., Shimomura O., Saiga Y., Gershman L.C., Reynolds G.T., and Waters J.R. (1962). Quantum efficiency of Cypridina luminescence, with a note on that of Aequorea. Journal of Cellular and Comparative Physiology 60, 85-103
  93. Jones, J.M., and Gellert, M. (2004). The taming of a transposon: V(D)J recombination and the immune system. Immunol Rev 200, 233-248 10.1111/j.0105-2896.2004.00168.x
  94. Jorgensen P.L., Hakansson K.O., and Karlish S.J. (2003). Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol 65, 817-849 10.1146/annurev.physiol.65.092101.142558
  95. Kalueff, A.V., Gebhardt, M., Stewart, A.M., Cachat, J.M., Brimmer, M., Chawla, J.S., Craddock, C., Kyzar, E.J., Roth, A., Landsman, S., Gaikwad, S., Robinson, K., Baatrup, E., Tierney, K., Shamchuk, A., Norton, W., Miller, N., Nicolson, T., Braubach, O., Gilman, C.P., Pittman, J., Rosemberg, D.B., Gerlai, R., Echevarria, D., Lamb, E., Neuhauss, S.C., Weng, W., Bally-Cuif, L., Schneider, H., and Consortium, Z.N.R. (2013). Towards a comprehensive catalog of zebrafish behavior 1.0 and beyond. Zebrafish 10, 70-86 10.1089/zeb.2012.0861
  96. Kandel, E.R. (2013). Principles of neural science. New York: McGraw-Hill.
  97. Kasha, M. (1950). Characterization of electronic transitions in complex molecules. Discussion of the Faraday Society 9, 14-19
  98. Kawakami, K. (2007). Tol2: a versatile gene transfer vector in vertebrates. Genome Biol 8 Suppl 1, S7 10.1186/gb-2007-8-s1-s7
  99. Kawashima, T., Zwart, M.F., Yang, C.T., Mensh, B.D., and Ahrens, M.B. (2016). The Serotonergic System Tracks the Outcomes of Actions to Mediate Short-Term Motor Learning. Cell 167, 933-946 e920 10.1016/j.cell.2016.09.055
  100. Keller, P.J., Schmidt, A.D., Wittbrodt, J., and Stelzer, E.H. (2008). Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322, 1065-1069 10.1126/science.1162493
  101. Kim, D.H., Kim, J., Marques, J.C., Grama, A., Hildebrand, D.G.C., Gu, W., Li, J.M., and Robson, D.N. (2017). Pan-neuronal calcium imaging with cellular resolution in freely swimming zebrafish. Nat Methods 14, 1107-1114 10.1038/nmeth.4429
  102. Kimmel, C.B. (1989). Genetics and early development of zebrafish. Trends Genet 5, 283-288
  103. Kimmel, C.B. (1993). Patterning the brain of the zebrafish embryo. Annu Rev Neurosci 16, 707-732 10.1146/annurev.ne.16.030193.003423
  104. Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev Dyn 203, 253-310 10.1002/aja.1002030302
  105. Krzic, U., Gunther, S., Saunders, T.E., Streichan, S.J., and Hufnagel, L. (2012). Multiview light-sheet microscope for rapid in toto imaging. Nat Methods 9, 730-733 10.1038/nmeth.2064
  106. Lakowicz, J.R. (2006). Principles of Fluorescence Spectroscopy. Springer.
  107. Leung, L.C., Wang, G.X., and Mourrain, P. (2013). Imaging zebrafish neural circuitry from whole brain to synapse. Front Neural Circuits 7, 76 10.3389/fncir.2013.00076
  108. Li B., Shahid R., Peshkepija P., and Zimmer M. (2012). Water diffusion in and out of the β-barrel of GFP and the fast maturing fluorescent protein, TurboGFP. Chemical Physiology 392, 143-148
  109. Li, Y., Van Hooser, S.D., Mazurek, M., White, L.E., and Fitzpatrick, D. (2008). Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952-956 10.1038/nature07417
  110. Lin, J.Y., Knutsen, P.M., Muller, A., Kleinfeld, D., and Tsien, R.Y. (2013). ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat Neurosci 16, 1499-1508 10.1038/nn.3502
  111. Lin, X., Wang, S., Yu, X., Liu, Z., Wang, F., Li, W.T., Cheng, S.H., Dai, Q., and Shi, P. (2015). High-throughput mapping of brain-wide activity in awake and drug-responsive vertebrates. Lab Chip 15, 680-689 10.1039/c4lc01186d
  112. Liu, S., Zhang, D., Liu, S., Feng, D., Peng, H., and Cai, W. (2016). Rivulet: 3D Neuron Morphology Tracing with Iterative Back-Tracking. Neuroinformatics 14, 387-401 10.1007/s12021-016-9302-0
  113. Llinas, R., and Nicholson, C. (1975). Calcium role in depolarization-secretion coupling: an aequorin study in squid giant synapse. Proc Natl Acad Sci U S A 72, 187-190
  114. Looger, L.L., and Griesbeck, O. (2012). Genetically encoded neural activity indicators. Curr Opin Neurobiol 22, 18-23 10.1016/j.conb.2011.10.024
  115. Ma, H., Harris, S., Rahmani, R., Lacefield, C.O., Zhao, M., Daniel, A.G., Zhou, Z., Bruno, R.M., Berwick, J., and Schwartz, T.H. (2014). Wide-field in vivo neocortical calcium dye imaging using a convection-enhanced loading technique combined with simultaneous multiwavelength imaging of voltage-sensitive dyes and hemodynamic signals. Neurophotonics 1, 015003 10.1117/1.NPh.1.1.015003
  116. Ma, Y., Shaik, M.A., Kim, S.H., Kozberg, M.G., Thibodeaux, D.N., Zhao, H.T., Yu, H., and Hillman, E.M. (2016). Wide-field optical mapping of neural activity and brain haemodynamics: considerations and novel approaches. Philos Trans R Soc Lond B Biol Sci 371, 10.1098/rstb.2015.0360
  117. Magiorkinis, E., Sidiropoulou, K., and Diamantis, A. (2010). Hallmarks in the history of epilepsy: epilepsy in antiquity. Epilepsy and Behavior 17, 103-108
  118. Makino, H., Ren, C., Liu, H., Kim, A.N., Kondapaneni, N., Liu, X., Kuzum, D., and Komiyama, T. (2017). Transformation of Cortex-wide Emergent Properties during Motor Learning. Neuron 94, 880-890 e888 10.1016/j.neuron.2017.04.015
  119. Meyer, M., Dhamne, S.C., Lacoursiere, C.M., Tambunan, D., Poduri, A., and Rotenberg, A. (2016). Microarray Noninvasive Neuronal Seizure Recordings from Intact Larval Zebrafish. PLoS One 11, e0156498 10.1371/journal.pone.0156498
  120. Minta, A., Kao, J.P., and Tsien, R.Y. (1989). Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J Biol Chem 264, 8171-8178
  121. Mione, M., Baldessari, D., Deflorian, G., Nappo, G., and Santoriello, C. (2008). How neuronal migration contributes to the morphogenesis of the CNS: insights from the zebrafish. Dev Neurosci 30, 66-81
  122. Miyawaki, A., Llopis, J., Heim, R., Mccaffery, J.M., Adams, J.A., Ikura, M., and Tsien, R.Y. (1997). Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887 10.1038/42264
  123. Morin J.G., and Hastings J.W. (1971). Energy transfer in a bioluminescent system. Journal of Cellular Physiology 77, 313-318
  124. Morise, H., Shimomura, O., Johnson, F.H., and Winant, J. (1974). Intermolecular energy transfer in the bioluminescent system of Aequorea. Biochemistry 13, 2656-2662
  125. Mueller, T. (2012). What is the Thalamus in Zebrafish? Front Neurosci 6, 64 10.3389/fnins.2012.00064
  126. Muotri, A.R., and Gage, F.H. (2006). Generation of neuronal variability and complexity. Nature 441, 1087-1093 10.1038/nature04959
  127. Nagai, T., Sawano, A., Park, E.S., and Miyawaki, A. (2001). Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc Natl Acad Sci U S A 98, 3197-3202
  128. Nakai, J., Ohkura, M., and Imoto, K. (2001). A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19, 137-141 10.1038/84397
  129. Naumann, E.A., Fitzgerald, J.E., Dunn, T.W., Rihel, J., Sompolinsky, H., and Engert, F. (2016). From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response. Cell 167, 947-960 e920 10.1016/j.cell.2016.10.019
  130. Naumann, E.A., Kampff, A.R., Prober, D.A., Schier, A.F., and Engert, F. (2010). Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 13, 513-520 10.1038/nn.2518
  131. Nernst, W. (1888). On the kinetics of substances in solution. Zeitschrift für Physikalische Chemie 2, 613-622, 634-637
  132. Ngugi, A.K., Bottomley, C., Kleinschmidt, I., Sander, J.W., and Newton, C.R. (2010). Estimation of the burden of active and life-time epilepsy: a meta-analytic approach. Epilepsia 51, 883-890 10.1111/j.1528-1167.2009.02481.x
  133. Nobrega, M.A., and Pennacchio, L.A. (2004). Comparative genomic analysis as a tool for biological discovery. J Physiol 554, 31-39 10.1113/jphysiol.2003.050948
  134. Noebels, J.L. (2003). The biology of epilepsy genes. Annu Rev Neurosci 26, 599-625 10.1146/annurev.neuro.26.010302.081210
  135. Ohki, K., Chung, S., Ch'ng, Y.H., Kara, P., and Reid, R.C. (2005). Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597-603 10.1038/nature03274
  136. Ohkura, M., Matsuzaki, M., Kasai, H., Imoto, K., and Nakai, J. (2005). Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem 77, 5861-5869 10.1021/ac0506837
  137. Olson, H.E., Poduri, A., and Pearl, P.L. (2014). Genetic forms of epilepsies and other paroxysmal disorders. Seminars in neurology 34, 266-279
  138. Oppenheim, R.W. (1991). Cell death during development of the nervous system. Annu Rev Neurosci 14, 453-501 10.1146/annurev.ne.14.030191.002321
  139. Ormo, M., Cubitt, A.B., Kallio, K., Gross, L.A., Tsien, R.Y., and Remington, S.J. (1996). Crystal structure of the Aequorea victoria green fluorescent protein. Science 273, 1392-1395
  140. Pakkenberg, B., Pelvig, D., Marner, L., Bundgaard, M.J., Gundersen, H.J., Nyengaard, J.R., and Regeur, L. (2003). Aging and the human neocortex. Exp Gerontol 38, 95-99
  141. Panier, T., Romano, S.A., Olive, R., Pietri, T., Sumbre, G., Candelier, R., and Debregeas, G. (2013). Fast functional imaging of multiple brain regions in intact zebrafish larvae using selective plane illumination microscopy. Front Neural Circuits 7, 65 10.3389/fncir.2013.00065
  142. Pedersen, P.L., and Carofoli, E. (1987). Ion motive ATPases. Ubiquity, properties, and significance to cell function. Trends in Biochemical Science 12, 146-150
  143. Pisanello, F., Mandelbaum, G., Pisanello, M., Oldenburg, I.A., Sileo, L., Markowitz, J.E., Peterson, R.E., Della Patria, A., Haynes, T.M., Emara, M.S., Spagnolo, B., Datta, S.R., De Vittorio, M., and Sabatini, B.L. (2017). Dynamic illumination of spatially restricted or large brain volumes via a single tapered optical fiber. Nat Neurosci 20, 1180-1188 10.1038/nn.4591
  144. Portugues, R., Feierstein, C.E., Engert, F., and Orger, M.B. (2014). Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 81, 1328-1343 10.1016/j.neuron.2014.01.019
  145. Porumb, T., Yau, P., Harvey, T.S., and Ikura, M. (1996). A calmodulin-target peptide hybrid molecule with unique calcium-binding properties. Protein Engineering 7, 109-115
  146. Power, R.M., and Huisken, J. (2017). A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat Methods 14, 360-373 10.1038/nmeth.4224
  147. Pozzan, T., Arslan, P., Tsien, R.Y., and Rink, T.J. (1982). Anti-immunoglobulin, cytoplasmic free calcium, and capping in B lymphocytes. J Cell Biol 94, 335-340
  148. Prasher, D.C., Eckenrode, V.K., Ward, W.W., Prendergast, F.G., and Cormier, M.J. (1992). Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229-233
  149. Ramòn Y Cajal, S. (1917). Recuerdos de mi vida. Imprenta y libreria de Nicolas Moya
  150. Randlett, O., Wee, C.L., Naumann, E.A., Nnaemeka, O., Schoppik, D., Fitzgerald, J.E., Portugues, R., Lacoste, A.M., Riegler, C., Engert, F., and Schier, A.F. (2015). Whole-brain activity mapping onto a zebrafish brain atlas. Nat Methods 12, 1039-1046 10.1038/nmeth.3581
  151. Ridgway, E.B., and Ashley, C.C. (1967). Calcium transients in single muscle fibers. Biochem Biophys Res Commun 29, 229-234
  152. Ringer, S. (1883). A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. Journal of Physiology 29-43
  153. Robles, E., Smith, S.J., and Baier, H. (2011). Characterization of genetically targeted neuron types in the zebrafish optic tectum. Front Neural Circuits 5, 1 10.3389/fncir.2011.00001
  154. Romano, S.A., Pietri, T., Perez-Schuster, V., Jouary, A., Haudrechy, M., and Sumbre, G. (2015). Spontaneous neuronal network dynamics reveal circuit's functional adaptations for behavior. Neuron 85, 1070-1085 10.1016/j.neuron.2015.01.027
  155. Rosch, R.E., Hunter, P.R., Baldeweg, T., Friston, K.J., and Meyer, M.P. (2018). Calcium imaging and dynamic causal modelling reveal brain-wide changes in effective connectivity and synaptic dynamics during epileptic seizures. PLoS Comput Biol 14, e1006375 10.1371/journal.pcbi.1006375
  156. Rose, A. (1946). A unified approach to the performance of photographic film, television pickup tubes and the human eye. J Soc Motion Pict Eng 47, 273-294
  157. Sabatini, B., Oertner, T.G., and Svoboda, K. (2002). The life cycle of Ca2+ ions in dendritic spines. Neuron 33, 439-452
  158. Safford, W.E. (1915). Annual Report of the Board of Reagents of the Smithsonin Institution. 271-298
  159. Shimomura, O. (2005). The discovery of aequorin and green fluorescent protein. J Microsc 217, 1-15 10.1111/j.0022-2720.2005.01441.x
  160. Shimomura O. (1979). Structure of the chromophore of Aequorea green fluorescent protein. FEBS Letters 104, 220-222
  161. Shimomura O., and Johnson F.H. (1970). Calcium binding, quantum yield, and emitting molecule in aequorin biolumnescence. Nature 227, 1356-1357
  162. Shimomura O., Johnson F.H., and Saiga Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59, 223-239
  163. Siedentopf, H., and Zsigmondy, R. (1902). Über sichtbarmachung und größenbestimmung ultramikoskopischer teilchen, mit besonderer anwendung auf goldrubingläser. Annualen der Physik 315, 1-39
  164. Silasi, G., Xiao, D., Vanni, M.P., Chen, A.C., and Murphy, T.H. (2016). Intact skull chronic windows for mesoscopic wide-field imaging in awake mice. J Neurosci Methods 267, 141-149 10.1016/j.jneumeth.2016.04.012
  165. Silvestri, L. (2012). Confocal ultramicroscopy: micron-scale neuroanatomy of the entire mouse brain. Doctoral dissertation, Università degli Studi di Firenze.
  166. Silvestri, L., Bria, A., Sacconi, L., Iannello, G., and Pavone, F.S. (2012). Confocal light sheet microscopy: micron-scale neuroanatomy of the entire mouse brain. Opt Express 20, 20582-20598 10.1364/OE.20.020582
  167. Stafstorm, C.E. (2010). Mechanisms of action of antiepileptic drugs: the search for synergy. Curr Opin Neurol 23, 157-163
  168. Stewart, A.M., Desmond, D., Kyzar, E., Gaikwad, S., Roth, A., Riehl, R., Collins, C., Monnig, L., Green, J., and Kalueff, A.V. (2012). Perspectives of zebrafish models of epilepsy: what, how and where next? Brain Res Bull 87, 135-143 10.1016/j.brainresbull.2011.11.020
  169. Stinnakre, J., and Tauc, L. (1973). Calcium influx in active Aplysia neurons detected by injected aequorin. Nature New Biology 242,
  170. Streisinger, G., Walker, C., Dower, N., Knauber, D., and Singer, F. (1981). Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291, 293-296
  171. Sullivan, M.R., Nimmerjahn, A., Sarkisov, D.V., Helmchen, F., and Wang, S.S. (2005). In vivo calcium imaging of circuit activity in cerebellar cortex. J Neurophysiol 94, 1636-1644 10.1152/jn.01013.2004
  172. Sumbre, G., Muto, A., Baier, H., and Poo, M.M. (2008). Entrained rhythmic activities of neuronal ensembles as perceptual memory of time interval. Nature 456, 102-106 10.1038/nature07351
  173. Tallini, Y.N., Ohkura, M., Choi, B.R., Ji, G., Imoto, K., Doran, R., Lee, J., Plan, P., Wilson, J., Xin, H.B., Sanbe, A., Gulick, J., Mathai, J., Robbins, J., Salama, G., Nakai, J., and Kotlikoff, M.I. (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 10.1073/pnas.0509378103
  174. Tao, L., Lauderdale, J.D., and Sornborger, A.T. (2011). Mapping Functional Connectivity between Neuronal Ensembles with Larval Zebrafish Transgenic for a Ratiometric Calcium Indicator. Front Neural Circuits 5, 2 10.3389/fncir.2011.00002
  175. Tian, L., Hires, S.A., Mao, T., Huber, D., Chiappe, M.E., Chalasani, S.H., Petreanu, L., Akerboom, J., Mckinney, S.A., Schreiter, E.R., Bargmann, C.I., Jayaraman, V., Svoboda, K., and Looger, L.L. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6, 875-881 10.1038/nmeth.1398
  176. Tokunaga, M., Imamoto, N., and Sakata-Sogawa, K. (2008). Highly inclined thin illumination enables clear single-molecule imaging in cells. Nature Methods 5, 159-161
  177. Tomer, R., Khairy, K., Amat, F., and Keller, P.J. (2012). Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nat Methods 9, 755-763 10.1038/nmeth.2062
  178. Tomer, R., Lovett-Barron, M., Kauvar, I., Andalman, A., Burns, V.M., Sankaran, S., Grosenick, L., Broxton, M., Yang, S., and Deisseroth, K. (2015). SPED Light Sheet Microscopy: Fast Mapping of Biological System Structure and Function. Cell 163, 1796-1806 10.1016/j.cell.2015.11.061
  179. Tsien, R.Y. (1980). New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19, 2396-2404
  180. Tsien, R.Y. (1981). A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290, 527-528
  181. Tsien, R.Y., Pozzan, T., and Rink, T.J. (1982). Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol 94, 325-334
  182. Turrini, L., Fornetto, C., Marchetto, G., Mullenbroich, M.C., Tiso, N., Vettori, A., Resta, F., Masi, A., Mannaioni, G., Pavone, F.S., and Vanzi, F. (2017). Optical mapping of neuronal activity during seizures in zebrafish. Sci Rep 7, 3025 10.1038/s41598-017-03087-z
  183. Valeur, B., and Berberan-Santos M.N. (2011). A Brief History of Fluorescence and Phosphorescence before the Emergence of Quantum Theory. Journal of Chemical Education 88, 731-738 10.1021/ed100182h
  184. Vanni, M.P., and Murphy, T.H. (2014). Mesoscale transcranial spontaneous activity mapping in GCaMP3 transgenic mice reveals extensive reciprocal connections between areas of somatomotor cortex. J Neurosci 34, 15931-15946 10.1523/JNEUROSCI.1818-14.2014
  185. Verveer, P.J., Swoger, J., Pampaloni, F., Greger, K., Marcello, M., and Stelzer, E.H. (2007). High-resolution three-dimensional imaging of large specimens with light sheet-based microscopy. Nat Methods 4, 311-313 10.1038/nmeth1017
  186. Vladimirov, N., Mu, Y., Kawashima, T., Bennett, D.V., Yang, C.T., Looger, L.L., Keller, P.J., Freeman, J., and Ahrens, M.B. (2014). Light-sheet functional imaging in fictively behaving zebrafish. Nat Methods 11, 883-884 10.1038/nmeth.3040
  187. Voie, A.H., Burns, D.H., and Spelman, F.A. (1993). Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological specimens. J Microsc 170, 229-236
  188. Wang, Q., Shui, B., Kotlikoff, M.I., and Sondermann, H. (2008). Structural basis for calcium sensing by GCaMP2. Structure 16, 1817-1827 10.1016/j.str.2008.10.008
  189. Ward, W.W., Prentice, H.J., Roth, A.F., Cody, C.W., and Reeves, C.S. (1982). Spectral perturbations of the aequorea green-fluorescent protein. Photochem Photobiol 35, 803-808
  190. Weisenburger, S., and Vaziri, A. (2018). A Guide to Emerging Technologies for Large-Scale and Whole-Brain Optical Imaging of Neuronal Activity. Annu Rev Neurosci 41, 431-452 10.1146/annurev-neuro-072116-031458
  191. Werley, C.A., Chien, M.P., and Cohen, A.E. (2017). Ultrawidefield microscope for high-speed fluorescence imaging and targeted optogenetic stimulation. Biomed Opt Express 8, 5794-5813 10.1364/BOE.8.005794
  192. Westerfield, M. (1993). The zebrafish book : a guide for the laboratory use of zebrafish (Brachydanio rerio). Eugene, OR: M. Westerfield.
  193. Williams, D.A., Fogarty, K.E., Tsien, R.Y., and Fay, F.S. (1985). Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature 318, 558-561
  194. Williams, R.P.J. (1999). Calcium: the developing role of its chemestry in biological evolution. In Calcium as a Cellular Regulator (Carofoli E. & Klee C., eds). 3-27
  195. Winter, M.J., Redfern, W.S., Hayfield, A.J., Owen, S.F., Valentin, J.P., and Hutchinson, T.H. (2008). Validation of a larval zebrafish locomotor assay for assessing the seizure liability of early-stage development drugs. J Pharmacol Toxicol Methods 57, 176-187 10.1016/j.vascn.2008.01.004
  196. Winter, M.J., Windell, D., Metz, J., Matthews, P., Pinion, J., Brown, J.T., Hetheridge, M.J., Ball, J.S., Owen, S.F., Redfern, W.S., Moger, J., Randall, A.D., and Tyler, C.R. (2017). 4-dimensional functional profiling in the convulsant-treated larval zebrafish brain. Sci Rep 7, 6581 10.1038/s41598-017-06646-6
  197. Wolf, S., Dubreuil, A.M., Bertoni, T., Bohm, U.L., Bormuth, V., Candelier, R., Karpenko, S., Hildebrand, D.G.C., Bianco, I.H., Monasson, R., and Debregeas, G. (2017). Sensorimotor computation underlying phototaxis in zebrafish. Nat Commun 8, 651 10.1038/s41467-017-00310-3
  198. Wu, P., Sui, C., and Huang, W. (2014). Theoretical analysis of a quasi-Bessel beam for laser ablation. Photonics Research 2, 82-86
  199. Xiao, D., Vanni, M.P., Mitelut, C.C., Chan, A.W., Ledue, J.M., Xie, Y., Chen, A.C., Swindale, N.V., and Murphy, T.H. (2017). Mapping cortical mesoscopic networks of single spiking cortical or sub-cortical neurons. Elife 6, 10.7554/eLife.19976
  200. Yokoe, H., and Meyer, T. (1996). Spatial dynamics of GFP-tagged proteins investigated by local fluorescence enhancement. Nat Biotechnol 14, 1252-1256 10.1038/nbt1096-1252
  201. Zdebik, A.A., Mahmood, F., Stanescu, H.C., Kleta, R., Bockenhauer, D., and Russell, C. (2013). Epilepsy in kcnj10 morphant zebrafish assessed with a novel method for long-term EEG recordings. PLoS One 8, e79765 10.1371/journal.pone.0079765
  202. Zheng, Q., Jockusch, S., Zhou, Z., and Blanchard, S.C. (2014). The contribution of reactive oxygen species to the photobleaching of organic fluorophores. Photochem Photobiol 90, 448-454 10.1111/php.12204