In vivo application of optogenetics for neural circuit analysis

ACS Chemical Neuroscience

Volumn 3, Issue 8, 2012, Pages 577-584

  Han, Xue ^a  

^a Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; OPSIN; PARVOVIRUS VECTOR; POTASSIUM CHANNEL; RETINOL; RHODOPSIN;

BRAIN ELECTROPHYSIOLOGY; BRAIN SIZE; CELL ACTIVATION; CELL ACTIVITY; CELL FUNCTION; CHLAMYDOMONAS REINHARDTII; DNA MODIFICATION; ELECTRODE; GENE EXPRESSION; GENETICS; HALORUBRUM SODOMENSE; HEAT; ILLUMINATION; IN VITRO STUDY; IN VIVO STUDY; ION TRANSPORT; ISOMERIZATION; LIGHT; NATRONOMONAS PHARAONIS; NERVE CELL NETWORK; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; OPTOGENETIC; OXYGENATION; PHOTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; REVIEW; SYNAPSE; TISSUE INJURY; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ELECTRODES; ELECTROPHYSIOLOGICAL PHENOMENA; GENETIC VECTORS; HUMANS; ION CHANNELS; LIGHT; MOLECULAR PROBES; NERVE NET; NEURONS; OPSINS; PHOTIC STIMULATION; RHODOPSIN; SIGNAL TRANSDUCTION; VIRUSES;

EID: 84865094135     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300065j     Document Type: Review

References (69)

1. 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
2. Zhang, F., Vierock, J., Yizhar, O., Fenno, L. E., Tsunoda, S., Kianianmomeni, A., Prigge, M., Berndt, A., Cushman, J., Polle, J., Magnuson, J., Hegemann, P., and Deisseroth, K. (2011) The microbial opsin family of optogenetic tools Cell 147, 1446-1457
3. Bernstein, J. G. and Boyden, E. S. (2011) Optogenetic tools for analyzing the neural circuits of behavior Trends Cognit. Sci. 15, 592-600
4. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., and Deisseroth, K. (2011) Optogenetics in neural systems Neuron 71, 9-34
5. Miesenbock, G. (2011) Optogenetic control of cells and circuits Annu. Rev. Cell Dev. Biol. 27, 731-758
6. Knopfel, T. and Boyden, E. S., Eds. (2012) Optogenetics: Tools for Controlling and Monitoring Neuronal Activity, Vol. 196, Elsevier.
7. Chow, B. Y., Han, X., and Boyden, E. S. (2012) Genetically encoded molecular tools for light-driven silencing of targeted neurons Prog. Brain Res. 196, 49-61
8. Han, X. (2012) Optogenetics in the nonhuman primate Prog. Brain Res. 196, 215-233
9. Spudich, J. L., Yang, C. S., Jung, K. H., and Spudich, E. N. (2000) Retinylidene proteins: structures and functions from archaea to humans Annu. Rev. Cell Dev. Biol. 16, 365-392
10. Spudich, J. L. (2006) The multitalented microbial sensory rhodopsins Trends Microbiol. 14, 480-487
11. Sineshchekov, O. A., Govorunova, E. G., and Spudich, J. L. (2009) Photosensory functions of channelrhodopsins in native algal cells Photochem. Photobiol. 85, 556-563
12. Ihara, K., Umemura, T., Katagiri, I., Kitajima-Ihara, T., Sugiyama, Y., Kimura, Y., and Mukohata, Y. (1999) Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation J. Mol. Biol. 285, 163-174
13. Boyden, E. S. (2011) A history of optogenetics: the development of tools for controlling brain circuits with light F1000 Biology Reports 3, 11
14. 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
15. 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
16. 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
17. Berndt, A., Schoenenberger, P., Mattis, J., Tye, K. M., Deisseroth, K., Hegemann, P., and Oertner, T. G. (2011) High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels Proc. Natl. Acad. Sci. U.S.A. 108, 7595-7600
18. 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
19. Wang, H., Sugiyama, Y., Hikima, T., Sugano, E., Tomita, H., Takahashi, T., Ishizuka, T., and Yawo, H. (2009) Molecular determinants differentiating photocurrent properties of two channelrhodopsins from chlamydomonas J. Biol. Chem. 284, 5685-5696
20. Wen, L., Wang, H., Tanimoto, S., Egawa, R., Matsuzaka, Y., Mushiake, H., Ishizuka, T., and Yawo, H. (2010) Opto-current-clamp actuation of cortical neurons using a strategically designed channelrhodopsin PloS One 5, e12893
21. Gunaydin, L. A., Yizhar, O., Berndt, A., Sohal, V. S., Deisseroth, K., and Hegemann, P. (2010) Ultrafast optogenetic control Nat. Neurosci. 13, 387-392
22. Berndt, A., Yizhar, O., Gunaydin, L. A., Hegemann, P., and Deisseroth, K. (2009) Bi-stable neural state switches Nat. Neurosci. 12, 229-234
23. Bamann, C., Gueta, R., Kleinlogel, S., Nagel, G., and Bamberg, E. (2010) Structural guidance of the photocycle of channelrhodopsin-2 by an interhelical hydrogen bond Biochemistry 49, 267-278
24. Zhang, F., Prigge, M., Beyriere, F., Tsunoda, S. P., Mattis, J., Yizhar, O., Hegemann, P., and Deisseroth, K. (2008) Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri Nat. Neurosci. 11, 631-633
25. Govorunova, E. G., Spudich, E. N., Lane, C. E., Sineshchekov, O. A., and Spudich, J. L. (2011) New channelrhodopsin with a red-shifted spectrum and rapid kinetics from Mesostigma viride mBio 2, e00115-00111
26. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., Stehfest, K., Fudim, R., Ramakrishnan, C., Huguenard, J. R., Hegemann, P., and Deisseroth, K. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction Nature 477, 171-178
27. Kleinlogel, S., Feldbauer, K., Dempski, R. E., Fotis, H., Wood, P. G., Bamann, C., and Bamberg, E. (2011) Ultra light-sensitive and fast neuronal activation with the Ca(2)+-permeable channelrhodopsin CatCh Nat. Neurosci 14, 513-518
28. Han, X. and Boyden, E. S. (2007) Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution PloS One 2, e299
29. 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
30. Ma, D., Zerangue, N., Lin, Y. F., Collins, A., Yu, M., Jan, Y. N., and Jan, L. Y. (2001) Role of ER export signals in controlling surface potassium channel numbers Science (New York, N.Y.) 291, 316-319
31. Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., Goshen, I., Thompson, K. R., and Deisseroth, K. (2010) Molecular and cellular approaches for diversifying and extending optogenetics Cell 141, 154-165
32. Gradinaru, V., Thompson, K. R., and Deisseroth, K. (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications Brain Cell Biol. 36, 129-139
33. Zhao, S., Cunha, C., Zhang, F., Liu, Q., Gloss, B., Deisseroth, K., Augustine, G. J., and Feng, G. (2008) Improved expression of halorhodopsin for light-induced silencing of neuronal activity Brain Cell Biol. 36, 141-154
34. Bamberg, E., Tittor, J., and Oesterhelt, D. (1993) Light-driven proton or chloride pumping by halorhodopsin Proc. Natl. Acad. Sci. U.S.A. 90, 639-643
35. Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., and Boyden, E. S. (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps Nature 463, 98-102
36. Raimondo, J. V., Kay, L., Ellender, T. J., and Akerman, C. J. (2012) Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission Nat. Neurosci. [Epub ahead of print] 10.1038/nn.3143
37. Han, X., Chow, B. Y., Zhou, H., Klapoetke, N. C., Chuong, A., Rajimehr, R., Yang, A., Baratta, M. V., Winkle, J., Desimone, R., and Boyden, E. S. (2011) A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex Front. Syst. Neurosci. 5, 18
38. Duschl, A., Lanyi, J. K., and Zimanyi, L. (1990) Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis J. Biol. Chem. 265, 1261-1267
39. Zemelman, B. V., Lee, G. A., Ng, M., and Miesenbock, G. (2002) Selective photostimulation of genetically chARGed neurons Neuron 33, 15-22
40. Li, X., Gutierrez, D. V., Hanson, M. G., Han, J., Mark, M. D., Chiel, H., Hegemann, P., Landmesser, L. T., and Herlitze, S. (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin Proc. Natl. Acad. Sci. U.S.A. 102, 17816-17821
41. Ye, H., Daoud-El Baba, M., Peng, R. W., and Fussenegger, M. (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice Science (New York, N.Y.) 332, 1565-1568
42. Airan, R. D., Thompson, K. R., Fenno, L. E., Bernstein, H., and Deisseroth, K. (2009) Temporally precise in vivo control of intracellular signalling Nature 458, 1025-1029
43. Lima, S. Q. and Miesenbock, G. (2005) Remote control of behavior through genetically targeted photostimulation of neurons Cell 121, 141-152
44. 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
45. 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
46. Janovjak, H., Szobota, S., Wyart, C., Trauner, D., and Isacoff, E. Y. (2010) A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing Nat. Neurosci. 13, 1027-1032
47. Tsien, J. Z., Chen, D. F., Gerber, D., Tom, C., Mercer, E. H., Anderson, D. J., Mayford, M., Kandel, E. R., and Tonegawa, S. (1996) Subregion- and cell type-restricted gene knockout in mouse brain Cell 87, 1317-1326
48. Sauer, B. and Henderson, N. (1988) Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1 Proc. Natl. Acad. Sci. U.S.A. 85, 5166-5170
49. Madisen, L., Mao, T., Koch, H., Zhuo, J. M., Berenyi, A., Fujisawa, S., Hsu, Y. W., Garcia, A. J., 3rd, Gu, X., Zanella, S., Kidney, J., Gu, H., Mao, Y., Hooks, B. M., Boyden, E. S., Buzsaki, G., Ramirez, J. M., Jones, A. R., Svoboda, K., Han, X., Turner, E. E., and Zeng, H. (2012) A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing Nat. Neurosci. 15, 793-802
50. Waehler, R., Russell, S. J., and Curiel, D. T. (2007) Engineering targeted viral vectors for gene therapy Nat. Rev. Genet. 8, 573-587
51. Neve, R. L. and Carlezon, W. A., Jr., Eds. (2002) Gene delivery into the brain using viral vectors, Vol. 20, Nature Publishing Group: New York.
52. Luo, D. and Saltzman, W. M. (2000) Synthetic DNA delivery systems Nat. Biotechnol. 18, 33-37
53. Nathanson, J. L., Jappelli, R., Scheeff, E. D., Manning, G., Obata, K., Brenner, S., and Callaway, E. M. (2009) Short Promoters in Viral Vectors Drive Selective Expression in Mammalian Inhibitory Neurons, but do not Restrict Activity to Specific Inhibitory Cell-Types Front. Neural Circuits 3, 19
54. Han, X., Qian, X., Bernstein, J. G., Zhou, H. H., Franzesi, G. T., Stern, P., Bronson, R. T., Graybiel, A. M., Desimone, R., and Boyden, E. S. (2009) Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain Neuron 62, 191-198
55. 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
56. Cruikshank, S. J., Urabe, H., Nurmikko, A. V., and Connors, B. W. (2010) Pathway-Specific Feedforward Circuits between Thalamus and Neocortex Revealed by Selective Optical Stimulation of Axons Neuron 65, 230-245
57. Tye, K. M., Prakash, R., Kim, S. Y., Fenno, L. E., Grosenick, L., Zarabi, H., Thompson, K. R., Gradinaru, V., Ramakrishnan, C., and Deisseroth, K. (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety Nature 471, 358-362
58. Mazarakis, N. D., Azzouz, M., Rohll, J. B., Ellard, F. M., Wilkes, F. J., Olsen, A. L., Carter, E. E., Barber, R. D., Baban, D. F., Kingsman, S. M., Kingsman, A. J., O'Malley, K., and Mitrophanous, K. A. (2001) Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery Hum. Mol. Genet. 10, 2109-2121
59. Mobley, J. and Vo-Dinh, T. (2003) Optical properties of Tissue. In Biomedical Photonics Handbook, pp 1-72, CRC Press: Boca Raton, FL
60. Bernstein, J. G., Han, X., Henninger, M. A., Ko, E. Y., Qian, X., Franzesi, G. T., McConnell, J. P., Stern, P., Desimone, R., and Boyden, E. S. (2008) Prosthetic systems for therapeutic optical activation and silencing of genetically-targeted neurons Proc. Soc. Photo-Opt. Instrum. Eng. 6854, 68540H
61. 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
62. Bernstein, J. G., Garrity, P. A., and Boyden, E. S. (2012) Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits Curr. Opin. Neurobiol. 22, 61-71
63. Wells, J., Kao, C., Mariappan, K., Albea, J., Jansen, E. D., Konrad, P., and Mahadevan-Jansen, A. (2005) Optical stimulation of neural tissue in vivo Opt. Lett. 30, 504-506
64. Tufail, Y., Yoshihiro, A., Pati, S., Li, M. M., and Tyler, W. J. (2011) Ultrasonic neuromodulation by brain stimulation with transcranial ultrasound Nat. Protoc. 6, 1453-1470
65. Ayling, O. G., Harrison, T. C., Boyd, J. D., Goroshkov, A., and Murphy, T. H. (2009) Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice Nat. Methods 6, 219-224
66. Gratzel, M. (2001) Photoelectrochemical cells Nature 414, 338-344
67. Honda, K. (2004) Dawn of the evolution of photoelectrochemistry J. Photochem. Photobiol. 63-68
68. Zorzos, A. N., Dietrich, A., Talei Franzesi, G., Chow, B. Y., Han, X., Fonstad, C. G., and Boyden, E. S. (2009) Light-proof neural recording electrodes Soc. Neurosci. 388, GG107
69. Atasoy, D., Aponte, Y., Su, H. H., and Sternson, S. M. (2008) A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping J. Neurosci. 28, 7025-7030