Two-photon holographic stimulation of ReaChR

Frontiers in Cellular Neuroscience

Volumn 10, Issue OCT2016, 2016, Pages

  Chaigneau, Emmanueiie ^a   Ronzitti, Emiliano ^a   Gajowa, Marta A ^a   Soler Llavina, Gilberto J ^b   Tanese, Dimitrii ^a   Brureau, Anthony Y B ^a   Papagiakoumou, Eirini ^a,c   Zeng, Hongkui ^b   Emiliani, Valentina ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b Aiien Institute for Brain Science   (United States)

^c INSERM   (France)

Author keywords

2 photon excitation; Action potential generation; Computer generated holography; Cortex; Neuroscience; Opsin; Optogenetics

Indexed keywords

ACTION POTENTIAL; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FLUORESCENCE; HOLOGRAPHY; MALE; MORPHOLOGY; MOUSE; NONHUMAN; OPTOGENETICS; SPATIOTEMPORAL ANALYSIS; STIMULATION;

EID: 84992487412     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2016.00234     Document Type: Article

References (39)

1. Adamantidis, A., Arber, S., Bains, J. S., Bamberg, E., Bonci, A., Buzsaki, G., et al. (2015). Optogenetics: 10 years after ChR2 in neurons-views from the community. Nat. Neurosci. 18, 1202-1212. doi: 10.1038/nn.4106.
2. Akerboom, J., Chen, T.-W., Wardill, T. J., Tian, L., Marvin, J. S., Mutlu, S., et al. (2012). Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging. J. Neurosci. 32, 13819-13840. doi: 10.1523/JNEUR0SCI.2601-12.2012.
3. 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. doi: 10.1073/pnas.1006620107.
4. Bañas, A., Palima, D., Villangca, M., Aabo, T., and Glüückstad, J. (2014). GPC light shaper for speckle-free one-and two-photon contiguous pattern excitation. Opt. Express 22, 5299-5310. doi: 10.1364/0e.22.005299.
5. Bègue, A., Papagiakoumou, E., Leshem, B., Conti, R., Enke, L., Oron, D., et al. (2013). Two-photon excitation in scattering media by spatiotemporally shaped beams and their application in optogenetic stimulation. Biomed. Opt. Express 4, 2869-2879. doi: 10.1364/Boe.4.002869.
6. Beierlein, M., Gibson, J. R., and Connors, B. W. (2003). Two dynamically distinct inhibitory networks in layer 4of the neocortex. J. Neurophysiol. 90,2987-3000. doi: 10.1152/jn.00283.2003.
7. Bovetti, S., and Fellin, T. (2015). Optical dissection ofbrain circuits with patterned illumination through the phase modulation of light. J. Neurosci. Methods 241, 66-77. doi: 10.1016/j.jneumeth.2014.12.002.
8. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268. doi: 10.1038/nn1525.
9. Castelló, A., Álvarez, E., and Carrasco, L. (2011). The multifaceted poliovirus 2A protease: regulation of gene expression by picornavirus proteases. J. Biomed. Biotechnol 2011:369-648. doi: 10.1155/2011/369648.
10. Chaigneau, E., Wright, A. J., Poland, S. P., Girkin, J. M., and Silver, R. A. (2011). Impact of wavefront distortion and scattering on 2-photon microscopy in mammalian brain tissue. Opt. Express 19, 6540-6552. doi: 10.1364/OE.19.022755.
11. Conti, R., Assayag, O., de Sars, V., Guillon, M., and Emiliani, V. (2016). Computer generated holography with intensity-graded patterns. Front. Cell. Neurosci. 10:236. doi: 10.3389/fncel.2016.00236.
12. Dana, H., Mohar, B., Sun, Y., Narayan, S., Gordus, A., Hasseman, J. P., et al. (2016). Sensitive red protein calcium indicators for imaging neural activity. Elife 5:e12727. doi: 10.7554/eLife.12727.
13. Emiliani, V., Cohen, A. E., Deisseroth, K., and Häusser, M. (2015). All- optical interrogation of neural circuits. J. Neurosci. 35, 13917-13926. doi: 10.1523/JNEUROSCI.2916-15.2015.
14. 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. doi: 10.1073/pnas.0905852106.
15. Gluckstad, J. (1996). Phase contrast image synthesis. Opt. Commun. 130, 225-230. doi: 10.1016/0030-4018(96)00339-2.
16. Hernandez, O., Guillon, M., Papagiakoumou, E., and Emiliani, V. (2014). Zero- order suppression for two-photon holographic excitation. Opt. Lett. 39, 5953-5956. doi: 10.1364/OL.39.005953.
17. Hooks, B. M., Lin, J. Y., Guo, C., and Svoboda, K. (2015). Dual-channel circuit mapping reveals sensorimotor convergence in the primary motor cortex. J. Neurosci. 35,4418-4426. doi: 10.1523/JNEUR0SCI.3741-14.2015.
18. Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., et al. (2014). Independent optical excitation of distinct neural populations. Nat. Methods 11, 338-346. doi: 10.1038/nmeth.2836.
19. 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. doi: 10.1038/nn.3502.
20. 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. doi: 10.1038/nmeth.1241.
21. Mattis, J., Tye, K. M., Ferenczi, E. A., Ramakrishnan, C., O'Shea, D. J., Prakash, R., et al. (2012). Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 9, 159-172. doi: 10.1038/nmeth.1808.
22. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., et al. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. U.S.A. 100, 13940-13945. doi: 10.1073/pnas.1936192100.
23. 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. doi: 10.1038/nmeth.2249.
24. Packer, A. M., Russell, L. E., Dalgleish, H. W. P., and Häusser, M. (2015). Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo. Nat. Methods 12, 140-146. doi: 10.1038/nmeth.3217.
25. Palima, D., and Glückstad, J. (2008). Multi-wavelength spatial light shaping using generalized phase contrast. Opt. Express 16, 1331-1342. doi: 10.1364/OE.16.001331.
26. Papagiakoumou, E. (2013). Optical developments for optogenetics. Biol. Cell 105, 443-464. doi: 10.1111/boc.201200087.
27. Papagiakoumou, E., Anselmi, F., Begue, A., de Sars, V., Gluckstad, J., Isacoff, E. Y., et al. (2010). Scanless two-photon excitation of channelrhodopsin-2. Nat. Methods 7, 848-854. doi: 10.1038/nmeth.1505.
28. Papagiakoumou, E., Begue, A., Leshem, B., Schwartz, O., Stell, B. M., Bradley, J., et al. (2013). Functional patterned multiphoton excitation deep inside scattering tissue. Nat. Phot. 7, 274-278. doi: 10.1038/nphoton.2013.9.
29. Peron, S., and Svoboda, K. (2011). From cudgel to scalpel: toward precise neural control with optogenetics. Nat. Methods 8, 30-34. doi: 10.1038/nmeth.f.325.
30. Prakash, R., Yizhar, O., Grewe, B., Ramakrishnan, C., Wang, N., Goshen, I., et al. (2012). Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat. Methods 9, 1171-1179. doi: 10.1038/nmeth.2215.
31. Rickgauer, J. P., Deisseroth, K., and Tank, D. W. (2014). Simultaneous cellular- resolution optical perturbation and imaging of place cell firing fields. Nat. Neurosci. 17, 1816-1824. doi: 10.1038/nn.3866.
32. 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. doi: 10.1073/pnas.0907084106.
33. Ronzitti, E., Conti, R., Papagiakoumou, E., Tanese, D., Zampini, V., Chaigneau, E., et al. (2016). Sub-millisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos. BioRxiv 1, 1-22. doi: 10.1101/062182.
34. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N. G., Palmer, A. E., and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572. doi: 10.1038/nbt1037.
35. Theer, P., and Denk, W. (2006). On the fundamental imaging-depth limit in two- photon microscopy. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 23, 3139-3149. doi: 10.1364/JOSAA.23.003139.
36. Xu, C., and Webb, W. W. (1996). Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm. J. Opt. Soc. Am. B. 13, 481-491. doi: 10.1364/Josab.13.000481.
37. Xu, X., Roby, K. D., and Callaway, E. M. (2006). Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J. Comp. Neurol. 499, 144-160. doi: 10.1002/cne.21101.
38. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'Shea, D. J., et al. (2011). Neocortical excitation / inhibition balance in information processing and social dysfunction. Nature 477, 171-178. doi: 10.1038/nature10360.
39. Zipfel, W. R., Williams, R. M., and Webb, W. W. (2003). Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369-1377. doi: 10.1038/nbt899