Recent developments in optical neuromodulation technologies

Molecular Neurobiology

Volumn 47, Issue 1, 2013, Pages 172-185

  Kos, Aron ^a   Loohuis, Nikkie F Olde ^a   Glennon, Jeffrey C ^a   Celikel, Tansu ^b   Martens, Gerard J M ^b   Tiesinga, Paul H ^b   Aschrafi, Armaz ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Bacteriorhodopsin; Behavior; Channel rhodopsin; Halorhodopsin; Neuronal networks

Indexed keywords

HALORHODOPSIN; OPSIN;

ANIMAL TISSUE; BRAIN FUNCTION; CONTROLLED STUDY; DECISION MAKING; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE CELL NETWORK; NERVE DEGENERATION; NEUROMODULATION; NEUROPSYCHIATRY; NEUROSCIENCE; NONHUMAN; OPTOGENETICS; PROCESS OPTIMIZATION; REVIEW;

EID: 84872497479     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8361-y     Document Type: Review

References (113)

1. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186-198
2. Matsuno-Yagi A, Mukohata Y (1977) Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. Biochem Biophys Res Commun 78:237-243
3. Nagel G et al (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395-2398. doi: 10.1126/science.1072068
4. Oesterhelt D, Stoeckenius W (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nat New Biol 233:149-152
5. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263-1268
6. Nagel G 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
7. Miller G (2006) Optogenetics. Shining new light on neural circuits. Science 314:1674-1676
8. Lee JH et al (2010) Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465:788-792
9. Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K (2009) Temporally precise in vivo control of intracellular signalling. Nature 458:1025-1029
10. Zemelman BV, Lee GA, Ng M, Miesenbock G (2002) Selective photostimulation of genetically chARGed neurons. Neuron 33:15-22
11. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186-193. doi: 10.1038/35093002
12. Burns ME, Baylor DA (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci 24:779-805. doi: 10.1146/annurev.neuro.24.1.779
13. Zemelman BV, Nesnas N, Lee GA, 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. doi: 10.1073/pnas.242738899
14. Lima SQ, Miesenbock G (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121:141-152
15. Kramer RH, Chambers JJ, Trauner D (2005) Photochemical tools for remote control of ion channels in excitable cells. Nat Chem Biol 1:360-365
16. Banghart M, Borges K, Isacoff E, Trauner D, Kramer RH (2004) Light-activated ion channels for remote control of neuronal firing. Nat Neurosci 7:1381-1386
17. Fortin DL et al (2008) Photochemical control of endogenous ion channels and cellular excitability. Nat Methods 5:331-338
18. Gorostiza P, Isacoff EY (2008) Optical switches for remote and noninvasive control of cell signaling. Science 322:395-399
19. 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 2:47-52
20. Janovjak H, Szobota S, Wyart C, Trauner D, Isacoff EY (2010) A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing. Nat Neurosci 13:1027-1032
21. Fernald RD (2006) Casting a genetic light on the evolution of eyes. Science 313:1914-1918
22. Yizhar O, Fenno L, Zhang F, Hegemann P, Diesseroth K (2011). Microbial opsins: a family of single-component tools for optical control of neural activity. Cold Spring Harb Protoc. doi: 10.1101/pdb.top102
23. Haupts U, Tittor J, Bamberg E, Oesterhelt D (1997) General concept for ion translocation by halobacterial retinal proteins: the isomerization/switch/ transfer (IST) model. Biochemistry 36:2-7. doi: 10.1021/bi962014g
24. Oesterhelt D, Stoeckenius W (1973) Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A 70:2853-2857
25. Racker E, Stoeckenius W (1974) Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. J Biol Chem 249:662-663
26. Beja O et al (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902-1906
27. Beja O, Spudich EN, Spudich JL, Leclerc M, DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature 411:786-789. doi: 10.1038/35081051
28. Sasaki J et al (1995) Conversion of bacteriorhodopsin into a chloride ion pump. Science 269:73-75
29. Zhang F et al (2008) Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat Neurosci 11:631-633
30. Kato HE et al (2012) Crystal structure of the channelrhodopsin light-gated cation channel. Nature 482:369-374. doi: 10.1038/nature10870
31. Grossman N, Nikolic K, Toumazou C, Degenaar P (2011) Modeling study of the light stimulation of a neuron cell with channelrhodopsin-2 mutants. IEEE Trans Biomed Eng 58:1742-1751. doi: 10.1109/TBME.2011.2114883
32. Plazzo AP et al (2012) Bioinformatic and mutational analysis of channelrhodopsin-2 protein cation-conducting pathway. J Biol Chem 287:4818-4825. doi: 10.1074/jbc.M111.326207
33. Pulver SR, Pashkovski SL, Hornstein NJ, Garrity PA, Griffith LC (2009) Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J Neurophysiol 101:3075-3088. doi: 10.1152/jn.00071.2009
34. Mancuso JJ, Kim J, Lee S, Tsuda S, Chow NB, Augustine GJ (2011) Optogenetic probing of functional brain circuitry. Exp Physiol 96:26-33. doi: 10.1113/expphysiol.2010.055731
35. Bamann C, Gueta R, Kleinlogel S, Nagel G, Bamberg E (2010) Structural guidance of the photocycle of channelrhodopsin-2 by an interhelical hydrogen bond. Biochemistry 49:267-278. doi: 10.1021/bi901634p
36. Li X et al (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
37. 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 15:2279-2284
38. Bi A et al (2006) Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23-33
39. Thyagarajan S, van Wyk M, Lehmann K, Lowel S, Feng G, Wassle H (2010) Visual function in mice with photoreceptor degeneration and transgenic expression of channelrhodopsin 2 in ganglion cells. J Neurosci 30:8745-8758
40. Zhang F et al (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446:633-639
41. Gradinaru V, Thompson KR, Deisseroth K (2008) eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol 36:129-139. doi: 10.1007/s11068-008-9027-6
42. Zhao S et al (2008) Improved expression of halorhodopsin for light-induced silencing of neuronal activity. Brain Cell Biol 36:141-154. doi: 10.1007/s11068-008-9034-7
43. Berndt A et al (2011) High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc Natl Acad Sci U S A 108:7595-7600
44. Kleinlogel S et al (2011) Ultra light-sensitive and fast neuronal activation with the Ca(2)+-permeable channelrhodopsin CatCh. Nat Neurosci 14:513-518
45. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K (2011) Optogenetics in neural systems. Neuron 71:9-34
46. Kleinlogel S et al (2011) A gene-fusion strategy for stoichiometric and co-localized expression of light-gated membrane proteins. Nat Methods 8:1083-1088. doi: 10.1038/nmeth.1766
47. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW (2005) Addition of human melanopsin renders mammalian cells photoresponsive. Nature 433:741-745
48. Kim JM, Hwa J, Garriga P, Reeves PJ, RajBhandary UL, Khorana HG (2005) Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops. Biochemistry 44:2284-2292. doi: 10.1021/bi048328i
49. Dittgen T et al (2004) Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc Natl Acad Sci U S A 101:18206-18211
50. Monahan PE, Samulski RJ (2000) Adeno-associated virus vectors for gene therapy: more pros than cons? Mol Med Today 6:433-440
51. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L (2007) Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450:420-424
52. Ciocchi S et al (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277-282
53. Haubensak W et al (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468:270-276
54. Kravitz AV et al (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622-626. doi: 10.1038/nature09159
55. Lobo MK et al (2010) Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330:385-390
56. Petreanu L, Mao T, Sternson SM, Svoboda K (2009) The subcellular organization of neocortical excitatory connections. Nature 457:1142-1145
57. Aravanis AM et al (2007) An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng 4:S143-S156
58. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324:354-359
59. Busskamp V et al (2010) Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329:413-417
60. Diester I et al (2011) An optogenetic toolbox designed for primates. Nat Neurosci 14:387-397
61. Han X et al (2011) A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front Syst Neurosci 5:18. doi: 10.3389/fnsys.2011.00018
62. Nathanson JL, Yanagawa Y, Obata K, Callaway EM (2009) Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of adeno-associated virus and lentivirus vectors. Neuroscience 161:441-450
63. Choi VW, McCarty DM, Samulski RJ (2005) AAV hybrid serotypes: improved vectors for gene delivery. Curr Gene Ther 5:299-310
64. Markakis EA et al (2010) Comparative transduction efficiency of AAV vector serotypes 1-6 in the substantia nigra and striatum of the primate brain. Mol Ther 18:588-593
65. Burger C et al (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10:302-317. doi: 10.1016/j.ymthe.2004.05.024
66. Gradinaru V et al (2010) Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141:154-165
67. Greenberg KP, Pham A, Werblin FS (2011) Differential targeting of optical neuromodulators to ganglion cell soma and dendrites allows dynamic control of center-surround antagonism. Neuron 69:713-720
68. Lewis TL Jr, Mao T, Svoboda K, Arnold DB (2009) Myosin-dependent targeting of transmembrane proteins to neuronal dendrites. Nat Neurosci 12:568-576
69. Lewis TL Jr, Mao T, Arnold DB (2011) A role for myosin VI in the localization of axonal proteins. PLoS Biol 9:e1001021. doi: 10.1371/journal. pbio.1001021
70. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683
71. Tye KM et al (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358-362
72. Brenner M, Kisseberth WC, Su Y, Besnard F, Messing A (1994) GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 14:1030-1037
73. Gourine AV et al (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329:571-575
74. LaLumiere RT (2011) A new technique for controlling the brain: optogenetics and its potential for use in research and the clinic. Brain Stimulation 4:1-6. doi: 10.1016/j.brs.2010.09.009
75. Kuhlman SJ, Huang ZJ (2008) High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLoS One 3:e2005. doi: 10.1371/journal.pone.0002005
76. Atasoy D, Aponte Y, Su HH, Sternson SM (2008) A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci 28:7025-7030
77. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698-702
78. Feng G et al (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51
79. Arenkiel BR et al (2007) In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54:205-218
80. Wang H et al (2007) High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci U S A 104:8143-8148
81. Adesnik H, Scanziani M (2010) Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464:1155-1160
82. Gradinaru V et al (2007) Targeting and readout strategies for fast optical neural control in vitro and in vivo. J Neurosci 27:14231-14238
83. Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2- assisted circuit mapping of long-range callosal projections. Nat Neurosci 10:663-668
84. Huber D et al (2008) Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451:61-64
85. Berndt A, Yizhar O, Gunaydin LA, Hegemann P, Deisseroth K (2009) Bi-stable neural state switches. Nat Neurosci 12:229-234
86. Carter ME et al (2010) Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci 13:1526-1533
87. Mahoney TR et al (2008) Intestinal signaling to GABAergic neurons regulates a rhythmic behavior in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105:16350-16355. doi: 10.1073/pnas.0803617105
88. Leifer AM, Fang-Yen C, Gershow M, Alkema MJ, Samuel AD (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat Methods 8:147-152. doi: 10.1038/nmeth.1554
89. Clyne JD, Miesenbock G (2008) Sex-specific control and tuning of the pattern generator for courtship song in Drosophila. Cell 133:354-363. doi: 10.1016/j.cell.2008.01.050
90. Claridge-Chang A et al (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405-415. doi: 10.1016/j.cell.2009.08.034
91. Zhu P et al (2009) Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the Tet system. Front Neural Circuits 3:21. doi: 10.3389/neuro.04.021.2009
92. Wyart C et al (2009) Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461:407-410. doi: 10.1038/nature08323
93. Arrenberg AB, Del Bene F, Baier H (2009) Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci U S A 106:17968-17973. doi: 10.1073/pnas.0906252106
94. Cardin JA et al (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667. doi: 10.1038/nature08002
95. Adamantidis AR et al (2011) Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J Neurosci 31:10829-10835. doi: 10.1523/JNEUROSCI.2246-11.2011
96. Tsai HC et al (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:1080-1084. doi: 10.1126/science.1168878
97. Stuber GD et al (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:377-380. doi: 10.1038/nature10194
98. Aponte Y, Atasoy D, Sternson SM (2011) AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat Neurosci 14:351-355. doi: 10.1038/nn.2739
99. Lin D et al (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221-226. doi: 10.1038/nature09736
100. Witten IB et al (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330:1677-1681. doi: 10.1126/science.1193771
101. Covington HE 3rd et al (2010) Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 30:16082-16090. doi: 10.1523/JNEUROSCI.1731-10.2010
102. Johansen JP et al (2010) Optical activation of lateral amygdala pyramidal cells instructs associative fear learning. Proc Natl Acad Sci U S A 107:12692-12697. doi: 10.1073/pnas.1002418107
103. Goshen I et al (2011) Dynamics of retrieval strategies for remote memories. Cell 147:678-689. doi: 10.1016/j.cell.2011.09.033
104. Tsunematsu T, Kilduff TS, Boyden ES, Takahashi S, Tominaga M, Yamanaka A (2011) Acute optogenetic silencing of orexin/hypocretin neurons induces slow-wave sleep in mice. J Neurosci 31:10529-10539. doi: 10.1523/JNEUROSCI.0784- 11.2011
105. Choi GB, Stettler DD, Kallman BR, Bhaskar ST, Fleischmann A, Axel R (2011) Driving opposing behaviors with ensembles of piriform neurons. Cell 146:1004-1015. doi: 10.1016/j.cell.2011.07.041
106. Pascoli V, Turiault M, Luscher C (2012) Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 481:71-75. doi: 10.1038/nature10709
107. Anikeeva P et al (2012) Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat Neurosci 15:163-170. doi: 10.1038/nn.2992
108. Arrenberg AB, Stainier DY, Baier H, Huisken J (2010) Optogenetic control of cardiac function. Science 330:971-974
109. Bruegmann T et al (2010) Optogenetic control of heart muscle in vitro and in vivo. Nat Methods 7:897-900
110. Stirman JN et al (2011) Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat Methods 8:153-158
111. Stroh A et al (2011) Tracking stem cell differentiation in the setting of automated optogenetic stimulation. Stem Cells 29:78-88. doi: 10.1002/stem.558
112. Tonnesen J et al (2011) Functional integration of grafted neural stem cell-derived dopaminergic neurons monitored by optogenetics in an in vitro Parkinson model. PLoS One 6:e17560. doi: 10.1371/journal.pone.0017560
113. Weick JP, Johnson MA, Skroch SP, Williams JC, Deisseroth K, Zhang SC (2010) Functional control of transplantable human ESC-derived neurons via optogenetic targeting. Stem Cells 28:2008-2016. doi: 10.1002/stem.514