Optical control of neuronal activity

Annual Review of Biophysics

Volumn 39, Issue 1, 2010, Pages 329-348

  Szobota, Stephanie ^a   Isacoff, Ehud Y ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Channelrhodopsin; Halorhodopsin; LiGluR; Optogenetics; Photostimulation; SPARK

Indexed keywords

ADENOSINE TRIPHOSPHATE; AZOBENZENE DERIVATIVE; CALCIUM; CAPSAICIN; CHANNELRHODOPSIN 1; CHANNELRHODOPSIN 2; GLUTAMATE RECEPTOR; GLUTAMIC ACID DERIVATIVE; GUANINE NUCLEOTIDE BINDING PROTEIN; ION CHANNEL; MELANOPSIN; NEUROTRANSMITTER; OPSIN; POTASSIUM CHANNEL; PURINERGIC P2X2 RECEPTOR; QUATERNARY AMMONIUM DERIVATIVE; RHODOPSIN 4; UNCLASSIFIED DRUG;

GENETIC ENGINEERING; ISOMERIZATION; LIGAND BINDING; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NERVE CONDUCTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTOSENSITIVITY; PHOTOSTIMULATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ANIMALS; NEURONS; OPTICS AND PHOTONICS; SIGNAL TRANSDUCTION;

EID: 77952940224     PISSN: 1936122X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.093008.131400     Document Type: Review

References (98)

1. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L 2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450(7168):420-424
2. Ahmed NA, Radwan NM, Ibrahim KM, Khedr ME, El Aziz MA, Khadrawy YA. 2008. Effect of three different intensities of infrared laser energy on the levels of amino acid neurotransmitters in the cortex and hippocampus of rat brain. Photomed. Laser Surg. 26(5):479-488
3. Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K 2009. Temporally precise in vivo control of intracellular signalling. Nature 458(7241):1025-1029
4. Alilain WJ, Li X, Horn KP, Dhingra R, Dick TE, et al. 2008. Light-induced rescue of breathing after spinal cord injury. J. Neurosci. 28(46):11862-11870
5. Allègre G, Avrillier S, Albe-Fessard D. 1994. Stimulation in the rat of a nerve fiber bundle by a short UV pulse from an excimer laser. Neurosci. Lett. 180(2):261-264
6. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, et al. 2007. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54(2):205-218
7. Arrenberg AB, Del Bene F, Baier H. 2009. Optical control of zebrafish behavior with halorhodopsin. Proc. Natl. Acad. Sci. USA 106:17968-17973
8. Bamann C, Kirsch T, Nagel G, Bamberg E. 2008. Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. J. Mol. Biol. 375(3):686-694
9. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH. 2004. Light-activated ion channels for remote control of neuronal firing. Nat. Neurosci. 7(12):1381-1386
10. Banghart MR, Mourot A, Fortin DL, Yao JZ, Kramer RH, Trauner D. 2009. Photochromic blockers of voltage-gated potassium channels. Angew. Chem. Int. Ed. Engl. 48(48):9097-9101
11. Bartels E, Wassermann NH, Erlanger BF. 1971. Photochromic activators of the acetylcholine receptor. Proc. Natl. Acad. Sci. USA 68(8):1820-1823
12. Berndt A, Yizhar O, Gunaydin LA, Hegemann P, Deisseroth K. 2009. Bi-stable neural state switches. Nat. Neurosci. 12(2):229-234
13. Bernstein JG, Han X, Henninger MA, Ko EY, Qian X, et al. 2008. Prosthetic systems for therapeutic optical activation and silencing of genetically-targeted neurons. Proc. Soc. Photo-Opt. Instrum. Eng. 6854:68540H
14. Berthold P, Tsunoda SP, Ernst OP, Mages W, Gradmann D, Hegemann P. 2008. Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization. Plant Cell 20(6):1665-1677
15. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, et al 2006. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50(1):23-33
16. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8(9):1263-1268
17. Callaway EM, Katz LC. 1993. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 90(16):7661-7665
18. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, et al 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247):663-667
19. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816-824
20. + channel and a molecular photoswitch. J. Neurophysiol. 96:2792-2796
21. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, et al 2009. Writing memories with light-addressable reinforcement circuitry. Cell 139:405-415
22. Clyne JD, Miesenböck G 2008. Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133(2):354-363
23. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, et al. 2010. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463(7277):98-102
24. Douglass AD, Kraves S, Deisseroth K, Schier AF, Engert F. 2008. Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr. Biol. 18(15):1133-1137
25. Downes GB, Gautam N. 1999. The G protein subunit gene families. Genomics 62(3):544-552
26. + channels to reactive oxygen species. Proc. Natl. Acad. Sci. USA 92(25):11796-11800
27. Duschl A, Lanyi JK, Zimányi L. 1990. Properties and photochemistry of a halorhodopsin from the haloalkalophile, Natronobacterium pharaonis. J. Biol. Chem. 265(3):1261-1267
28. Ebrey T, Koutalos Y. 2001. Vertebrate photoreceptors. Prog. Retin. Eye Res. 20(1):49-94
29. Ellis-Davies GC. 2007. Caged compounds: photorelease technology for control of cellular chemistry and physiology. Nat. Methods 4(8):619-628
30. Ernst OP, Sánchez Murcia PA, Daldrop P, Tsunoda SP, Kateriya S, Hegemann P. 2008. Photoactivation of channelrhodopsin. J. Biol. Chem. 283(3):1637-1643
31. Farber IC, Grinvald A 1983. Identification of presynaptic neurons by laser photostimulation. Science 222(4627):1025-1027
32. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E. 2009. Channelrhodopsin-2 is a leaky proton pump. Proc. Natl. Acad. Sci. USA 106(30):12317-12322
33. Fork RL 1971. Laser stimulation of nerve cells in Aplysia. Science 171(974):907-908
34. Fortin DL, Banghart MR, Dunn TW, Borges K, Wagenaar DA, et al. 2008. Photochemical control of endogenous ion channels and cellular excitability. Nat. Methods 5(4):331-338
35. Gorostiza P, Volgraf M, Numano R, Szobota S, Trauner D, Isacoff EY. 2007. Mechanisms of photo-switch conjugation and light activation of an ionotropic glutamate receptor. Proc. Natl. Acad. Sci. USA 104(26):10865-10870
36. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K 2009. Optical deconstruction of Parkinsonian neural circuitry. Science 324(5925):354-359
37. Gradinaru V, Thompson KR, Deisseroth K. 2008. eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol. 36(1-4):129-139
38. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, et al. 2007. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 27(52):14231-14238
39. Han X, Boyden ES. 2007. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PloS ONE 2(3):e299
40. Han X, Qian X, Bernstein JG, Zhou HH, Franzesi GT, et al. 2009. Millisecond-timescale optical control of neural dynamics in the nonhuman primate brain. Neuron 62(2):191-198
41. Haupts U, Tittor J, Oesterhelt D. 1999. Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu. Rev. Biophys. Biomol. Struct. 28:367-399
42. + channel signature sequence. Biophys. J. 66(4):1061-1067
43. + channel. Biophys. J. 65(5):2089-2096
44. Hillman P, Hochstein S, Minke B. 1983. Transduction in invertebrate photoreceptors: role of pigment bistability. Physiol. Rev. 63(2):668-772
45. Hirase H, Nikolenko V, Goldberg JH, Yuste R. 2002. Multiphoton stimulation of neurons. J. Neurobiol. 51(3):237-247
46. Izzo AD, Richter CP, Jansen ED, Walsh JT Jr. 2006. Laser stimulation of the auditory nerve. Lasers Surg. Med. 38(8):745-753
47. Kaplan JH, Forbush B, Hoffman JF. 1978. Caged-ATP, a photolabile source of ATP. Biophys. J. 21(3):A72
48. Khakh BS, North RA 2006. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442(7102):527-532
49. Kourie JI. 1998. Interaction of reactive oxygen species with ion transport mechanisms. Am. J. Physiol. 275(Pt. 1):C1-24
50. Lester HA, Chang HW 1977. Response of acetylcholine receptors to rapid photochemically produced increases in agonist concentration. Nature 266(5600):373-374
51. Lester HA, Nass MM, Krouse ME, Nerbonne JM, Wassermann NH, Erlanger BF. 1980. Electrophys-iological experiments with photoisomerizable cholinergic compounds: review and progress report. Ann. NY Acad. Sci. 346:475-490
52. Lester HA, Nerbonne JM. 1982. Physiological and pharmacological manipulations with light flashes. Annu. Rev. Biophys. Bioeng. 11:151-175
53. Li G, Oswald RE, Niu L 2003. Channel-opening kinetics of GluR6 kainate receptor. Biochemistry 42(42):12367-12375
54. LiX, Gutierrez DV, Hanson MG, Han J, Mark MD, et al. 2005. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc. Natl. Acad. Sci. USA 102(49):17816-17821
55. + channels. J. Biol. Chem. 280(25):23945-23959
56. Lima SQ, Hromádka T, Znamenskiy P, Zador AM. 2009. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS One 4(7):e6099
57. Lima SQ, Miesenböck G 2005. Remote control of behavior through genetically targeted photostimu-lation of neurons. Cell 121(1):141-152
58. Lin B, Koizumi A, Tanaka N, Panda S, Masland RH. 2008. Restoration of visual function in retinal degeneration mice by ectopic expression of melanopsin. Proc. Natl. Acad. Sci. USA 105(41):16009-16014
59. Lin JY, Lin MZ, Steinbach P, Tsien RY. 2009. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96(5):1803-1814
60. Liu Q, Hollopeter G, Jorgensen EM. 2009. Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc. Natl. Acad. Sci. USA 106(26):10823-10828
61. Lucas RJ. 2006. Chromophore regeneration: Melanopsin does its own thing. Proc. Natl. Acad. Sci. USA 103(27):10153-10154
62. Matthews RG, Hubbard R, Brown PK, Wald G. 1963. Tautomeric forms of metarhodopsin. J. Gen. Physiol. 47:215-240
63. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW 2005. Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433(7027):741-745
64. Mezey E, Tóth ZE, Cortright DN, Arzubi MK, Krause JE, et al. 2000. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl. Acad. Sci. USA 97(7):3655-3660
65. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15(24):2279-2284
66. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, et al. 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100(24):13940-13945
67. Nagele T, Hoche R, Zinth W, Wachtveitl J. 1997. Femtosecond photoisomerization of cis-azobenzene. Chem. Phys. Lett. 272(5-6):489-495
68. Numano R, Szobota S, Lau AY, Gorostiza P, Volgraf M, et al. 2009. Nanosculpting reversed wavelength sensitivity into a photoswitchable iGluR. Proc. Natl. Acad. Sci. USA 106(16):6814-6819
69. Petreanu L, Huber D, Sobczyk A, Svoboda K. 2007. Channelrhodopsin-2- assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10(5):663-668
70. Pfisterer C, Gruia A, Fischer S. 2009. The mechanism of photo-energy storage in the halorhodopsin chloride pump. J. Biol. Chem. 284(20):13562-13569
71. Pierce S, Giese AC. 1957. Photoreversal of ultraviolet injury to frog and crab nerves. J. Cell Physiol. 49(2):303-317
72. Qiu X, Kumbalasiri T, Carlson SM, Wong KY, Krishna V, et al 2005. Induction of photosensitivity by heterologous expression of melanopsin. Nature 433(7027):745-749
73. Reece PJ, Dholakia K, Thomas RC, Cottrell GA. 2008. Green laser light (532 nm) activates a chloride current in the C1 neuron of Helix aspersa. Neurosci. Lett. 433(3):265-269
74. Rickgauer JP, Tank DW. 2009. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. USA 106:15025-15030
75. Schroll C, Riemensperger T, Bucher D, Ehmer J, Völler T, et al. 2006. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16(17):1741-1747
76. Scott EK, Mason L, Arrenberg AB, Ziv L, Gosse NJ, et al. 2007. Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat. Methods 4:323-326
77. Sohal VS, Zhang F, Yizhar O, Deisseroth K 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459(7247):698-702
78. Spudich JL, Yang CS, Jung KH, Spudich EN. 2000. Retinylidene proteins: structures and functions from archaea to humans. Annu. Rev. Cell. Dev. Biol. 16:365-392
79. Swanson GT, Feldmeyer D, Kaneda M, Cull-Candy SG. 1996. Effect of RNA editing and subunit co-assembly single-channel properties of recombinant kainate receptors. J. Physiol. 492(Pt. 1):129-142
80. Szobota S, Gorostiza P, Del Bene F, Wyart C, Fortin DL, et al. 2007. Remote control of neuronal activity with a light-gated glutamate receptor. Neuron 54(4):535-545
81. Tønnesen J, Sørensen AT, Deisseroth K, Lundberg C, Kokaia M. 2009. Optogenetic control of epilep-tiform activity. Proc. Natl. Acad. Sci. USA 106(29):12162-12167
82. Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, et al 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324(5930):1080-1084
83. Váró G, Needleman R, Lanyi JK. 1995. Light-driven chloride ion transport by halorhodopsin from Natronobacterium pharaonis. 2. Chloride release and uptake, protein conformation change, and thermodynamics. Biochemistry 34(44):14500-14507
84. Volgraf M, Gorostiza P, Numano R, Kramer RH, Isacoff EY, Trauner D. 2006. Allosteric control of an ionotropic glutamate receptor with an optical switch. Nat. Chem. Biol. 2(1):47-52
85. Volgraf M, Gorostiza P, Szobota S, Helix MR, Isacoff EY, Trauner D. 2007. Reversibly caged glutamate: a photochromic agonist of ionotropic glutamate receptors. J. Am. Chem. Soc. 129(2):260-261
86. Wade PD, Taylor J, Siekevitz P. 1988. Mammalian cerebral cortical tissue responds to low-intensity visible light. Proc. Natl. Acad. Sci. USA 85(23):9322-9326
87. Wells J, Kao C, Konrad P, Milner T, Kim J, et al. 2007. Biophysical mechanisms of transient optical stimulation of peripheral nerve. Biophys. J. 93(7):2567-2580
88. Wells J, Kao C, Mariappan K, Albea J, Jansen ED, et al. 2005. Optical stimulation of neural tissue in vivo. Opt. Lett. 30(5):504-506
89. Wilcox M, Viola RW, Johnson KW, Billington AP, Carpenter BK, et al. 1990. Synthesis of photolabile precursors of amino acid neurotransmitters. J. Org. Chem. 55(5):1585-1589
90. Wyart C, Del Bene F, Warp E, Scott EK, Trauner D, et al 2009. Optogenetic dissection of a behavioral module in the vertebrate spinal cord. Nature 461(7262):407-410
91. Zemelman BV, Lee GA, NgM, Miesenböck G. 2002. Selective photostimulation ofgenetically chARGed neurons. Neuron 33(1):15-22
92. Zemelman BV, Nesnas N, Lee GA, Miesenböck G. 2003. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. USA 100(3):1352-1357
93. Zhang F, Prigge M, Beyrière F, Tsunoda SP, Mattis J, et al. 2008. Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat. Neurosci. 11(6):631-633
94. Zhang F, Wang LP, Boyden ES, Deisseroth K. 2006. Channelrhodopsin-2 and optical controlofexcitable cells. Nat. Methods 3(10):785-792
95. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, et al 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446(7136):633-639
96. Zhang Y, Ivanova E, Bi A, Pan ZH. 2009. Ectopic expression of multiple microbial rhodopsins restores ON and OFF light responses in retinas with photoreceptor degeneration. J. Neurosci. 29(29):9186-9196
97. Zhao S, Cunha C, Zhang F, Liu Q, Gloss B, et al. 2008. Improved expression of halorhodopsin for light-induced silencing of neuronal activity. Brain Cell Biol. 36(1-4):141-154
98. Gunaydin LA, Yizhar O, Berndt A, Sohal VS, Deisseroth K, Hegemann P. 2010. Ultrafast optogenetic control. Nat. Neurosci. 13(3):387-392