Optical developments for optogenetics

Biology of the Cell

Volumn 105, Issue 10, 2013, Pages 443-464

  Papagiakoumou, Eirini ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Digital holography; Generalised phase contrast; Illumination methods; Optogenetics; Spatio temporal focusing

Indexed keywords

FLUORESCENT DYE;

AMPLITUDE MODULATION; BRAIN NERVE CELL; BRAIN REGION; CONFOCAL LASER MICROSCOPY; DIGITAL IMAGING; ELECTRODE; ELECTROSTIMULATION; FIBER OPTICS; FLUORESCENCE IMAGING; HOLOGRAPHY; HUMAN; ILLUMINATION; LASER; LIGHT EMITTING DIODE; LIQUID CRYSTAL; MOLECULAR IMAGING; MOLECULAR PROBE; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROMONITORING; NEUROSCIENCE; NONHUMAN; OPTOGENETICS; PHASE CONTRAST MICROSCOPY; PHASE TRANSITION; PHOTOACTIVATION; PHOTOSTIMULATION; PRIORITY JOURNAL; REVIEW;

DIGITAL HOLOGRAPHY; GENERALISED PHASE CONTRAST; ILLUMINATION METHODS; OPTOGENETICS; SPATIO-TEMPORAL FOCUSING;

ANIMALS; HUMANS; NEURONS; OPTICAL IMAGING; OPTOGENETICS;

EID: 84885185702     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201200087     Document Type: Review

References (182)

1. Acker, C.D., Yan, P. and Loew, L.M. (2011) Single-voxel recording of voltage transients in dendritic spines. Biophys. J. 101, L11-L13
2. Adamantidis, A.R., Zhang, F., Aravanis, A.M., Deisseroth, K. and De Lecea, L. (2007) Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420-424
3. Akemann, W., Mutoh, H., Perron, A., Rossier, J. and Knöpfel, T. (2010) Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 7, 643-649
4. Akerboom, J., Chen, T.-W., Wardill, T.J., Tian, L., Marvin, J.S., Mutlu, S., Calderón, 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
5. Andrasfalvy, B.K., Zemelman, B.V., Tang, J. and Vaziri, A. (2010) Two-photon single-cell optogenetic control of neuronal activity by sculpted light. Proc. Natl. Acad. Sci. U. S. A. 107, 11981-11986
6. Anikeeva, P., Andalman, A.S., Witten, I., Warden, M., Goshen, I., Grosenick, L., Gunaydin, L.a, Frank, L.M. and Deisseroth, K. (2012) Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15, 163-170
7. Anselmi, F., Ventalon, C., Bègue, A., Ogden, D. and Emiliani, V. (2011) Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning. Proc. Natl. Acad. Sci. U. S. A. 108, 19504-19509
8. Aravanis, A.M., Wang, L.P., Zhang, F., Meltzer, L.A., Mogri, M.Z., Schneider, M.B. and Deisseroth, K. (2007) An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J. Neural Eng. 4, S143-S156
9. Arrenberg, A.B., Stainier, D.Y.R., Baier, H. and Huisken, J. (2010) Optogenetic control of cardiac function. Science 330, 971-974
10. Arrizón, V. and Testorf, M. (1997) Efficiency limit of spatially quantized Fourier array illuminators. Opt. Lett. 22, 197-199
11. Ashkin, A. and Dziedzic, J.M. (1987) Optical trapping and manipulation of viruses and bacteria. Science 235, 1517
12. Ashkin, A., Dziedzic, J.M., Bjorkholm, J.E. and Chu, S. (1986) Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11, 288-290
13. Axelrod, D. (1981) Cell-substrate contacts illuminated by total internal reflection fluorescence. J. Cell Biol. 89, 141-145
14. Banghart, M., Borges, K., Isacoff, E., Trauner, D. and Kramer, R.H. (2004) Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7, 1381-1386
15. Bernstein, J., Garrity, P. and Boyden, E. (2011) Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr. Opin. Neurobiol. 22, 61-71
16. Botcherby, E.J., Juskaitis, R., Booth, M.J. and Wilson, T. (2007) Aberration-free optical refocusing in high numerical aperture microscopy. Opt. Lett. 32, 2007-2009
17. Botcherby, E.J., Smith, C.W., Kohl, M.M., Débarre, D., Booth, M.J., Juskaitis, R., Paulsen, O. and Wilson, T. (2012) Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates. Proc. Natl. Acad. Sci. U. S. A. 109, 2919-2924
18. Bozinovic, N., Ventalon, C., Ford, T. and Mertz, J. (2008) Fluorescence endomicroscopy with structured illumination. Opt. Express. 16, 4603-4610
19. Bruegmann, T., Malan, D., Hesse, M., Beiert, T., Fuegemann, C.J., Fleischmann, B.K. and Sasse, P. (2010) Optogenetic control of heart muscle in vitro and in vivo. Nat. Methods 7, 897-900
20. Bundschuh, S.T., Zhu, P., Schärer, Y.-P.Z. and Friedrich, R.W. (2012) Dopaminergic modulation of mitral cells and odor responses in the zebrafish olfactory bulb. J. Neurosci. 32, 6830-6840
21. Busskamp, V., Duebel, J., Balya, D., Fradot, M., Viney, T.J., Siegert, S., Groner, A.C., Cabuy, E., Forster, V., Seeliger, M., Biel, M., Humphries, P., Paques, M., Mohand-Said, S., Trono, D., Deisseroth K., Sahel J.A., Picaud S. and Roska B. (2010) Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329, 413-417
22. Buzsáki, G. (2004) Large-scale recording of neuronal ensembles. Nat. Neurosci. 7, 446-451
23. Callaway, E.M. and Katz, L.C. (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. U. S. A. 90, 7661-7665
24. Cardin, J.A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H. and Moore, C.I. (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667
25. Chanda, B., Blunck, R., Faria, L.C., Schweizer, F.E., Mody, I. and Bezanilla, F. (2005) A hybrid approach to measuring electrical activity in genetically specified neurons. Nat. Neurosci. 8, 1619-1626
26. Chen, Q., Cichon, J., Wang, W., Qiu, L., Lee, S.-J.R., Campbell, N.R., DeStefino, N., Goard, M.J., Fu, Z., Yasuda, R., Looger, L.L., Arenkiel, B.R., Gan, W.B. and Feng, G. (2012) Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76, 297-308
27. Čižmár, T. and Dholakia, K. (2011) Shaping the light transmission through a multimode optical fibre: complex transformation analysis and applications in biophotonics. Opt. Express. 19, 18871-18884
28. Čižmár, T. and Dholakia, K. (2012) Exploiting multimode waveguides for pure fibre-based imaging. Nat. Commun. 3, 1027
29. 2+ imaging. J. Am. Chem. Soc. 134, 14923-14931
30. Curtis, J.E., Koss, B.A. and Grier, D.G. (2002) Dynamic holographic optical tweezers. Opt. Commun. 207, 169
31. Dal Maschio, M., De Stasi, A.M., Benfenati, F. and Fellin, T. (2011) Three-dimensional in vivo scanning microscopy with inertia-free focus control. Opt. Lett. 36, 3503-3505
32. Dal Maschio, M., Difato, F., Beltramo, R., Blau, A., Benfenati, F. and Fellin, T. (2010) Simultaneous two-photon imaging and photo-stimulation with structured light illumination. Opt. Express. 18, 18720-18731
33. Dana, H. and Shoham, S. (2011) Numerical evaluation of temporal focusing characteristics in transparent and scattering media. Opt. Express. 19, 4937-4948
34. Dana, H. and Shoham, S. (2012a) Numerical evaluation of temporal focusing characteristics in transparent and scattering media: erratum. Opt. Express. 20, 28281
35. Dana, H. and Shoham, S. (2012b) Remotely scanned multiphoton temporal focusing by axial grism scanning. Opt. Lett. 37, 2913-2915
36. Daria, V.R., Stricker, C., Bowman, R., Redman, S. and Bachor, H.A. (2009) Arbitrary multisite two-photon excitation in four dimensions. Appl. Phys. Lett. 95, 93701
37. Débarre, D., Botcherby, E. and Watanabe, T. (2009) Image-based adaptive optics for two-photon microscopy. Opt. Lett. 34, 2495-2497
38. Degenaar, P., Grossman, N., Memon, M.A., Burrone, J., Dawson, M., Drakakis, E., Neil, M. and Nikolic, K. (2009) Optobionic vision - a new genetically enhanced light on retinal prosthesis. J. Neural Eng. 6, 035007
39. Deisseroth, K., Feng, G., Majewska, A.K., Miesenböck, G., Ting, A. and Schnitzer, M.J. (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 26, 10380-10386
40. Denk, W., Strickler, J.H. and Webb, W.W. (1990) Two-photon laser scanning fluorescence microscopy. Science 248, 73-76
41. Depuy, S.D., Kanbar, R., Coates, M.B., Stornetta, R.L. and Guyenet, P.G. (2011) Control of breathing by raphe obscurus serotonergic neurons in mice. J. Neurosci. 31, 1981-1990
42. Dhawale, A.K., Hagiwara, A., Bhalla, U.S., Murthy, V.N. and Albeanu, D.F. (2010) Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat. Neurosci. 13, 1404-1412
43. Di Leonardo, R. and Bianchi, S. (2011) Hologram transmission through multi-mode optical fibers. Opt. Express. 19, 1867-1869
44. Di Leonardo, R., Ianni, F. and Ruocco, G. (2007) Computer generation of optimal holograms for optical trap arrays. Opt. Express. 15, 1913-1922
45. Dimitrov, D., He, Y., Mutoh, H., Baker, B.J., Cohen, L., Akemann, W. and Knöpfel, T. (2007) Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS One 2, e440
46. 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
47. Du, R., Bi, K., Zeng, S., Li, D., Xue, S. and Luo, Q. (2009) Analysis of fast axial scanning scheme using temporal focusing with acousto-optic deflectors. J. Mod. Opt. 56, 81-84
48. Durst, M.E., Zhu, G. and Xu, C. (2006) Simultaneous spatial and temporal focusing for axial scanning. Opt. Express. 14, 12243-12254
49. Durst, M.E., Zhu, G. and Xu, C. (2008) Simultaneous spatial and temporal focusing in nonlinear microscopy. Opt. Commun. 281, 1796-1805
50. Fan, G.Y., Fujisaki, H., Miyawaki, A., Tsay, R.K., Tsien, R.Y. and Ellisman, M.H. (1999) Video-rate scanning two-photon excitation fluorescence microscopy and ratio imaging with cameleons. Biophys. J. 76, 2412-2420
51. Farber, I.C. and Grinvald, A. (1983) Identification of presynaptic neurons by laser photostimulation. Science 222, 1025-1027
52. Feldbauer, K., Zimmermann, D., Pintschovius, V., Spitz, J., Bamann, C. and Bamberg, E. (2009) Channelrhodopsin-2 is a leaky proton pump. Proc. Natl. Acad. Sci. U. S. A. 106, 12317-12322
53. Fisher, J.A., Barchi, J.R., Welle, C.G., Kim, G.-H., Kosterin, P., Obaid, A.L., Yodh, A.G., Contreras, D. and Salzberg, B.M. (2008) Two-photon excitation of potentiometric probes enables optical recording of action potentials from mammalian nerve terminals in situ. J. Neurophysiol. 99, 1545-1553
54. Fork, R. (1971) Laser stimulation of nerve cells in aplysia. Science 3, 907-908
55. Fortin, D., Banghart, M. and Dunn, T. (2008) Photochemical control of endogenous ion channels and cellular excitability. Nat. Methods 5, 331-338
56. Gasparini, S. and Magee, J.C. (2006) State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 2088-2100
57. Gerchberg, R.W. and Saxton, W.O. (1972) A pratical algorithm for the determination of the phase from image and diffraction pictures. Optik 35, 237-246
58. Glückstad, J. (1996) Phase contrast image synthesis. Opt. Commun. 130, 225-230
59. Glückstad, J. and Mogensen, P.C. (2001) Optimal phase contrast in common-path interferometry. Appl. Optics 40, 268-282
60. Go, M.A., Ng, P.-F., Bachor, H.a and Daria, V.R. (2011) Optimal complex field holographic projection. Opt. Lett. 36, 3073-3075
61. Go, M.A., Stricker, C., Redman, S., Bachor, H.-A. and Daria, V.R. (2012) Simultaneous multi-site two-photon photostimulation in three dimensions. J. Biophotonics 5, 745-753
62. Göbel, W., Kampa, B.M. and Helmchen, F. (2006) Imaging cellular network dynamics in three dimensions using fast 3D laser scanning. Nat. Methods 4, 73-79
63. Golan, L., Reutsky, I., Farah, N. and Shoham, S. (2009) Design and characteristics of holographic neural photo-stimulation systems. J. Neural Eng. 6, 66004
64. Golan, L. and Shoham, S. (2009) Speckle elimination using shift-averaging in high-rate holographic projection. Opt. Express. 17, 1330-1339
65. Gradinaru, V., Thompson, K.R., Zhang, F., Mogri, M., Kay, K., Schneider, M.B. and Deisseroth, K. (2007) Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27, 14231-14238
66. Grossman, N., Poher, V., Grubb, M.S., Kennedy, G.T., Nikolic, K., McGovern, B., Palmini, R.B., Gong, Z., Drakakis, E.M., Neil, M.A., Dawson, M.D., Burrone, J. and Degenaar, P. (2010) Multi-site optical excitation using ChR2 and micro-LED array. J. Neural Eng. 7, 16004
67. Guo, Z.V, Hart, A.C. and Ramanathan, S. (2009) Optical interrogation of neural circuits in Caenorhabditis elegans. Nat. Methods 6, 891-896
68. Gutierrez, D.V, Mark, M.D., Masseck, O., Maejima, T., Kuckelsberg, D., Hyde, R.a, Krause, M., Kruse, W. and Herlitze, S. (2011) Optogenetic control of motor coordination by Gi/o protein-coupled vertebrate rhodopsin in cerebellar Purkinje cells. J. Biol. Chem. 286, 25848-25858
69. Hamill, O.P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391, 85-100
70. Heim, R., Cubitt, A.B. and Tsien, R.Y. (1995) Improved green fluorescence. Nature 373, 663-664
71. 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
72. Helmchen, F. and Denk, W. (2005) Deep tissue two-photon microscopy. Nat. Methods 2, 932-940
73. Hirase, H., Nikolenko, V., Goldberg, J.H. and Yuste, R. (2002) Multiphoton stimulation of neurons. J. Neurobiol. 51, 237-247
74. Hopt, a and Neher, E. (2001) Highly nonlinear photodamage in two-photon fluorescence microscopy. Biophys. J. 80, 2029-2036
75. Huber, D., Petreanu, L., Ghitani, N., Ranade, S., Hromadka, T., Mainen, Z. and Svoboda, K. (2008) Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451, 61-64
76. Jesacher, A. and Booth, M.J. (2010) Parallel direct laser writing in three dimensions with spatially dependent aberration correction. Opt. Express. 18, 21090-21099
77. Jesacher, A., Maurer, C., Schwaighofer, A., Bernet, S. and Ritsch-Marte, M. (2008) Full phase and amplitude control of holographic optical tweezers with high efficiency. Opt. Express. 16, 4479-4486
78. Kasparov, S. and Herlitze, S. (2013) Optogenetics at a crossroads? Exp. Physiol. 98, 971-972
79. Katona, G., Szalay, G., Maák, P., Kaszás, A., Veress, M., Hillier, D., Chiovini, B., Vizi, E.S., Roska, B. and Rózsa, B. (2012) Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes. Nat. Methods 9, 201-208
80. Katz, L.C. and Dalva, M.B. (1994) Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54, 205-218
81. Katz, O., Small, E., Bromberg, Y. and Silberberg, Y. (2011) Focusing and compression of ultrashort pulses through scattering media. Nat. Photon. 5, 372-377
82. 2+-permeable channelrhodopsin CatCh. Nat. Neurosci. 14, 513-518
83. Knapczyk, M. and Krishnan, A. (2005) High-resolution pulse shaper based on arrays of digital micromirrors. IEEE Photonic. Tech. L. 17, 2200-2202
84. Knöpfel, T. (2012) Genetically encoded optical indicators for the analysis of neuronal circuits. Nat. Rev. Neurosci. 13, 687-700
85. Ko, H., Hofer, S.B., Pichler, B., Buchanan, K.a, Sjöström, P.J. and Mrsic-Flogel, T.D. (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87-91
86. Kravitz, A.V, Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K. and Kreitzer, A.C. (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622-626
87. Kuhn, B., Denk, W. and Bruno, R.M. (2008) In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc. Natl. Acad. Sci. U. S. A. 105, 7588-7593
88. Lee, J.H., Durand, R., Gradinaru, V., Zhang, F., Goshen, I., Kim, D.-S., Fenno, L.E., Ramakrishnan, C. and Deisseroth, K. (2010) Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465, 788-792
89. Leifer, A.M., Fang-Yen, C., Gershow, M., Alkema, M.J. and Samuel, A.D.T. (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat. Methods 8, 147-152
90. Levitz, J., Pantoja, C., Gaub, B., Janovjak, H., Reiner, A., Hoagland, A., Schoppik, D., Kane, B., Stawski, P., Schier, A.F., Trauner, D. and Isacoff, E.Y. (2013) Optical control of metabotropic glutamate receptors. Nat. Neurosci. 16, 507-516
91. Li, N., Downey, J.E., Bar-Shir, A., Gilad, A.a, Walczak, P., Kim, H., Joel, S.E., Pekar, J.J., Thakor, N.V. and Pelled, G. (2011) Optogenetic-guided cortical plasticity after nerve injury. Proc. Natl. Acad. Sci. U. S. A. 108, 8838-8843
92. Li, D., Hérault, K., Isacoff, E.Y., Oheim, M. and Ropert, N. (2012) Optogenetic activation of LiGluR-expressing astrocytes evokes anion channel-mediated glutamate release. J. Physiol. 590, 855-873
93. Liesener, J., Reicherter, M., Haist, T. and Tiziani, H.J. (2000) Multi-functional optical tweezers using computer-generated holograms. Opt. Commun. 185, 77-82
94. Lin, J.Y., Lin, M.Z., Steinbach, P. and Tsien, R.Y. (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96, 1803-1814
95. Liu, X., Ramirez, S., Pang, P.T., Puryear, C.B., Govindarajan, A., Deisseroth, K. and Tonegawa, S. (2012) Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484, 381-385
96. Losavio, B.E., Iyer, V. and Saggau, P. (2009) Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices. J. Biomed. Opt. 14, 064033
97. Losonczy, A., Zemelman, B.V, Vaziri, A. and Magee, J.C. (2010) Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 13, 967-972
98. Lutz, C., Otis, T.S., DeSars, V., Charpak, S., Digregorio, D.A. and Emiliani, V. (2008) Holographic photolysis of caged neurotransmitters. Nat. Methods 5, 821-827
99. Mao, T., O'Connor, D.H., Scheuss, V., Nakai, J. and Svoboda, K. (2008) Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS One 3, e1796
100. Matar, S., Golan, L. and Shoham, S. (2011) Reduction of two-photon holographic speckle using shift-averaging. Opt. Express. 19, 25891-25899
101. Mattis, J., Tye, K.M., Ferenczi, E.a, Ramakrishnan, C., Shea, D.J.O., Prakash, R., Gunaydin, L.a, Hyun, M., Fenno, L.E., Gradinaru, V., Yizhar, O. and Deisseroth, K. (2012) Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 9, 159-172
102. McAlinden, N., Massoubre, D., Richardson, E., Gu, E., Sakata, S., Dawson, M.D. and Mathieson, K. (2013) Thermal and optical characterization of micro-LED probes for in vivo optogenetic neural stimulation. Opt. Lett. 38, 992-994
103. Miesenböck, G. (2009) The optogenetic catechism. Science 326, 395-399
104. Mohanty, S.K., Reinscheid, R.K., Liu, X., Okamura, N., Krasieva, T.B. and Berns, M.W. (2008) In-depth activation of channelrhodopsin 2-sensitized excitable cells with high spatial resolution using two-photon excitation with a near-infrared laser microbeam cell culture. Biophys. J. 95, 3916-3926
105. Nagel, G., Brauner, M., Liewald, J.F., Adeishvili, N., Bamberg, E. and Gottschalk, A. (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279-2284
106. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P. and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. U. S. A. 100, 13940-13945
107. 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
108. Nguyen, Q.T., Callamaras, N., Hsieh, C. and Parker, I. (2001) Construction of a two-photon microscope for video-rate Ca(2+) imaging. Cell Calcium 30, 383-393
109. Nikolenko, V., Watson, B.O., Araya, R., Woodruff, A., Peterka, D.S. and Yuste, R. (2008) SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators. Front. Neural Circuit. 2, 5
110. Oheim, M., Beaurepaire, E., Chaigneau, E., Mertz, J. and Charpak, S. (2001) Two-photon microscopy in brain tissue: parameters influencing the imaging depth. J. Neurosci. Methods 111, 29-37
111. Oron, D., Papagiakoumou, E., Anselmi, F. and Emiliani, V. (2012) Two-photon optogenetics. Prog. Brain Res. 196, 119-143
112. Oron, D. and Silberberg, Y. (2005) Harmonic generation with temporally focused ultrashort pulses. J. Opt. Soc. Am. B 22, 2660-2663
113. Oron, D., Tal, E. and Silberberg, Y. (2005) Scanningless depth-resolved microscopy. Opt. Express. 13, 1468-1476
114. Otsu, Y., Bormuth, V., Wong, J., Mathieu, B., Dugue, G.P., Feltz, A. and Dieudonne, S. (2008) Optical monitoring of neuronal activity at high frame rate with a digital random-access multiphoton (RAMP) microscope. J. Neurosci. Methods 173, 259-270
115. Packer, A.M., Peterka, D.S., Hirtz, J.J., Prakash, R., Deisseroth, K. and Yuste, R. (2012) Two-photon optogenetics of dendritic spines and neural circuits. Nat. Methods 9, 1202-1205
116. Palima, D. and Glückstad, J. (2008) Comparison of generalized phase contrast and computer generated holography for laser image projection. Opt. Express 16, 5338-5349
117. Palima, D. and Daria, V.R. (2006) Effect of spurious diffraction orders in arbitrary multifoci patterns produced via phase-only holograms. Appl. Optics 45, 6689-6693
118. Palima, D. and Daria, V.R. (2007) Holographic projection of arbitrary light patterns with a suppressed zero-order beam. Appl. Optics 46, 4197-4201
119. Panda, S., Nayak, S.K., Campo, B., Walker, J.R., Hogenesch, J.B. and Jegla, T. (2005) Illumination of the melanopsin signaling pathway. Science 307, 600-604
120. Papagiakoumou, E., Anselmi, F., Bègue, A., de Sars, V., Glückstad, J., Isacoff, E.Y. and Emiliani, V. (2010) Scanless two-photon excitation of channelrhodopsin-2. Nat. Methods 7, 848-854
121. Papagiakoumou, E., Bègue, A., Leshem, B., Schwartz, O., Stell, B.M., Bradley, J., Oron, D. and Emiliani, V. (2013) Functional patterned multiphoton excitation deep inside scattering tissue. Nat. Photon. 7, 274-278
122. Papagiakoumou, E., de Sars, V., Emiliani, V. and Oron, D. (2009) Temporal focusing with spatially modulated excitation. Opt. Express. 17, 5391-5401
123. Papagiakoumou, E., de Sars, V., Oron, D. and Emiliani, V. (2008) Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses. Opt. Express. 16, 22039-22047
124. Petreanu, L., Huber, D., Sobczyk, A. and Svoboda, K. (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663-668
125. Petreanu, L., Mao, T., Sternson, S.M. and Svoboda, K. (2009) The subcellular organization of neocortical excitatory connections. Nature 457, 1142-1145
126. Piccolino, M. (2006) Luigi Galvani's path to animal electricity. C. R. Biol. 329, 303-318
127. Polosukhina, A., Litt, J., Tochitsky, I., Nemargut, J., Sychev, Y., De Kouchkovsky, I., Huang, T., Borges, K., Trauner, D., Van Gelder, R.N. and Kramer, R.H. (2012) Photochemical restoration of visual responses in blind mice. Neuron 75, 271-282
128. Prakash, R., Yizhar, O., Grewe, B., Ramakrishnan, C., Wang, N., Goshen, I., Packer, A.M., Peterka, D.S., Yuste, R., Schnitzer, M.J. and Deisseroth, K. (2012) Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat. Methods 9, 1171-1179
129. Qiu, X., Kumbalasiri, T., Carlson, S.M., Wong, K.Y., Krishna, V., Provencio, I. and Berson, D.M. (2005) Induction of photosensitivity by heterologous expression of melanopsin. Nature 433, 745-749
130. Reddy, G.D., Kelleher, K., Fink, R. and Saggau, P. (2008) Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity. Nat. Neurosci. 11, 713-720
131. Reddy, G.D. and Saggau, P. (2005) Fast three-dimensional laser scanning scheme using acousto-optic deflectors. J. Biomed. Opt. 10, 64038
132. Reicherter, M., Haist, T., Wagemann, E.U. and Tiziani, H.J. (1999) Optical particle trapping with computer-generated holograms written on a liquid-crystal display. Opt. Lett. 24, 608-610
133. Reutsky-Gefen, I., Golan, L., Farah, N., Schejter, A., Tsur, L., Brosh, I. and Shoham, S. (2013) Holographic optogenetic stimulation of patterned neuronal activity for vision restoration. Nat. Commun. 4, 1509
134. Rickgauer, J.P. and Tank, D.W. (2009) Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. U. S. A. 106, 15025-15030
135. Rochefort, N.L., Garaschuk, O., Milos, R.-I., Narushima, M., Marandi, N., Pichler, B., Kovalchuk, Y. and Konnerth, A. (2009) Sparsification of neuronal activity in the visual cortex at eye-opening. Proc. Natl. Acad. Sci. U. S. A. 106, 15049-15054
136. Ronzitti, E., Guillon, M., De Sars, V. and Emiliani, V. (2012) LCoS nematic SLM characterization and modeling for diffraction efficiency optimization, zero and ghost orders suppression. Opt. Express. 20, 17843-17855
137. Royer, S., Zemelman, B.V, Barbic, M., Losonczy, A., Buzsáki, G. and Magee, J.C. (2010) Multi-array silicon probes with integrated optical fibers: light-assisted perturbation and recording of local neural circuits in the behaving animal. Eur. J. Neursci. 31, 2279-2291
138. Rueckel, M., Mack-Bucher, J.a and Denk, W. (2006) Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing. Proc. Natl. Acad. Sci. U. S. A. 103, 17137-17142
139. Sakai, S., Ueno, K., Ishizuka, T. and Yawo, H. (2013) Parallel and patterned optogenetic manipulation of neurons in the brain slice using a DMD-based projector. Neurosci. Res. 75, 59-64
140. Salomé, R., Kremer, Y., Dieudonné, S., Léger, J.-F., Krichevsky, O., Wyart, C., Chatenay, D. and Bourdieu, L. (2006) Ultrafast random-access scanning in two-photon microscopy using acousto-optic deflectors. J. Neurosci. Methods 154, 161-174
141. Santos, M.D., Mohammadi, M.H., Yang, S., Liang, C.W., Kao, J.P.Y., Alger, B.E., Thompson, S.M. and Tang, C.-M. (2012) Dendritic hold and read: a gated mechanism for short term information storage and retrieval. PLoS One 7, e37542
142. Scanziani, M. and Hausser, M. (2009) Electrophysiology in the age of light. Nature 461, 930-939
143. Shoham, S., O'Connor, D.H., Sarkisov, D.V. and Wang, S.S. (2005) Rapid neurotransmitter uncaging in spatially defined patterns. Nat. Methods 2, 837-843
144. Siegel, M. and Isacoff, E. (1997) A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741
145. Sohal, V.S., Zhang, F., Yizhar, O. and Deisseroth, K. (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702
146. Stirman, J.N., Crane, M.M., Husson, S.J., Gottschalk, A. and Lu, H. (2012) A multispectral optical illumination system with precise spatiotemporal control for the manipulation of optogenetic reagents. Nat. Protoc. 7, 207-220
147. Stirman, J.N., Crane, M.M., Husson, S.J., Wabnig, S., Schultheis, C., Gottschalk, A. and Lu, H. (2011) Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat. Methods 8, 153-158
148. Straub, A., Durst, M.E. and Xu, C. (2011) High speed multiphoton axial scanning through an optical fiber in a remotely scanned temporal focusing setup. Biomed. Opt. Express. 2, 80-88
149. Stuart, G.J. and Sakmann, B. (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72
150. Stuart, G., Schiller, J. and Sakmann, B. (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505(Pt 3), 617-632
151. Suchowski, H., Oron, D., Silberberg, Y., Suchowski Oron, D. and Silberberg, Y.H. (2006) Generation of a dark nonlinear focus by spatio-temporal coherent control. Opt. Commun. 264, 482-487
152. 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
153. Tsai, H.C., Zhang, F., Adamantidis, A., Stuber, G.D., Bonci, A., De Lecea, L. and Deisseroth, K. (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084
154. Vaziri, A. and Emiliani, V. (2012) Reshaping the optical dimension in optogenetics. Curr. Opin. Neurobiol. 22, 128-137
155. Vellekoop, I.M. and Mosk, A.P. (2007) Focusing coherent light through opaque strongly scattering media. Opt. Lett. 32, 2309-2311
156. Volgraf, M., Gorostiza, P., Numano, R., Kramer, R.H., Isacoff, E.Y. and Trauner, D. (2006) Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat. Chem. Biol. 2, 47-52
157. Wang, K., Liu, Y., Li, Y., Guo, Y., Song, P., Zhang, X., Zeng, S. and Wang, Z. (2011) Precise spatiotemporal control of optogenetic activation using an acousto-optic device. PLoS One 6, e28468
158. Wang, H., Peca, J., Matsuzaki, M., Matsuzaki, K., Noguchi, J., Qiu, L., Wang, D., Zhang, F., Boyden, E., Deisseroth, K., Kasai, H., Hall, W.C., Feng, G. and Augustine, G.J. (2007a) High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 104, 8143-8148
159. Wang, S., Szobota, S., Wang, Y., Volgraf, M., Liu, Z., Sun, C., Trauner, D., Isacoff, E.Y. and Zhang, X. (2007b) All optical interface for parallel, remote and spatiotemporal control of neuronal activity. Nano Lett. 7, 3859-3863
160. Wang, J., Wagner, F., Borton, D.a, Zhang, J., Ozden, I., Burwell, R.D., Nurmikko, A.V, Van Wagenen, R., Diester, I. and Deisseroth, K. (2012) Integrated device for combined optical neuromodulation and electrical recording for chronic in vivo applications. J. Neural Eng. 9, 016001
161. Watt, A.J., Cuntz, H., Mori, M., Nusser, Z., Sjöström, P.J. and Häusser, M. (2009) Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat. Neurosci. 12, 463-473
162. Wilson, N.R., Runyan, C.a, Wang, F.L. and Sur, M. (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488, 343-348
163. Wilt, B.A, Burns, L.D., Wei Ho, E.T., Ghosh, K.K., Mukamel, E.A and Schnitzer, M.J. (2009) Advances in light microscopy for neuroscience. Annu. Rev. Neurosci. 32, 435-506
164. Witten, I.B., Lin, S.-C., Brodsky, M., Prakash, R., Diester, I., Anikeeva, P., Gradinaru, V., Ramakrishnan, C. and Deisseroth, K. (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677-1681
165. Wyart, C., Del Bene, F., Warp, E., Scott, E.K., Trauner, D., Baier, H. and Isacoff, E.Y. (2009) Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461, 407-410
166. Yan, P., Acker, C.D., Zhou, W.-L., Lee, P., Bollensdorff, C., Negrean, A., Lotti, J., Sacconi, L., Antic, S.D., Kohl, P., Mansvelder, H.D., Pavone, F.S. and Loew, L.M. (2012) Palette of fluorinated voltage-sensitive hemicyanine dyes. Proc. Natl. Acad. Sci. U. S. A. 109, 20443-20448
167. Yang, S., Papagiakoumou, E., Guillon, M., De Sars, V., Tang, C.M. and Emiliani, V. (2011) Three-dimensional holographic photostimulation of the dendritic arbor. J. Neural Eng. 8, 46002
168. Yizhar, O., Fenno, L.E., Davidson, T.J., Mogri, M. and Deisseroth, K. (2011) Optogenetics in neural systems. Neuron 71, 9-34
169. Zahid, M., Velez-Fort, M., Papagiakoumou, E., Ventalon, C., Angulo, M.C. and Emiliani, V. (2010) Holographic photolysis for multiple cell stimulation in mouse hippocampal slices. PLoS One 5, e9431
170. Zemelman, B., Lee, G., Ng, M. and Miesenböck, G. (2002) Selective photostimulation of genetically chARGed neurons. Neuron 33, 15-22
171. Zemelman, B.V, Nesnas, N., Lee, G.a and Miesenbock, G. (2003) Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. U. S. A. 100, 1352-1357
172. Zernike, F. (1955) How I discovered phase contrast. Science 121, 345-349
173. Zhang, F., Gradinaru, V., Adamantidis, A.R., Durand, R., Airan, R.D., De Lecea, L. and Deisseroth, K. (2010) Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 5, 439-456
174. Zhang, Y., Holbro, N. and Oertner, T.G. (2008) Optical induction of plasticity at single synapses reveals input-specific accumulation of alphaCaMKII. Proc. Natl. Acad. Sci. U. S. A. 105, 12039-12044
175. Zhang, J., Laiwalla, F. and Kim, J. (2009) Integrated device for optical stimulation and spatiotemporal electrical recording of neural activity in light-sensitized brain tissue. J. Neural Eng. 6, 055007
176. Zhang, Y.P. and Oertner, T.G. (2007) Optical induction of synaptic plasticity using a light-sensitive channel. Nat. Methods 4, 139-141
177. Zhang, F., Wang, L.P., Boyden, E.S. and Deisseroth, K. (2006) Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3, 785-792
178. Zhang, F., Wang, L.P., Brauner, M., Liewald, J.F., Kay, K., Watzke, N., Wood, P.G., Bamberg, E., Nagel, G., Gottschalk, A. and Deisseroth, K. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446, 633-639
179. Zhu, P., Fajardo, O., Shum, J., Zhang Schärer, Y.-P. and Friedrich, R.W. (2012) High-resolution optical control of spatiotemporal neuronal activity patterns in zebrafish using a digital micromirror device. Nat. Protoc. 7, 1410-1425
180. Zhu, G., Van Howe, J., Durst, M., Zipfel, W. and Xu, C. (2005) Simultaneous spatial and temporal focusing of femtosecond pulses. Opt. Express. 13, 2153-2159
181. Zipfel, W.R., Williams, R.M. and Webb, W.W. (2003) Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369-1377
182. Zorzos, A., Boyden, E.S. and Fonstad, C.G. (2010) A multi-waveguide implantable probe for light delivery to sets of distributed brain targets. Opt. Lett. 35, 4133-4135