In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2

Neuron

Volumn 54, Issue 2, 2007, Pages 205-218

  Arenkiel, Benjamin R ^a   Peca, Joao ^a,b   Davison, Ian G ^a   Feliciano, Catia ^a,c   Deisseroth, Karl ^d   Augustine, George J ^a   Ehlers, Michael D ^a   Feng, Guoping ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d Stanford University   (United States)

Author keywords

MOLNEURO; SYSNEURO

Indexed keywords

CHANNELRHODOPSIN 2; HYBRID PROTEIN; ION CHANNEL; UNCLASSIFIED DRUG;

ACCURACY; ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CELL ACTIVATION; CHLAMYDOMONAS REINHARDTII; GLOMERULUS; GREEN ALGA; ILLUMINATION; IN VIVO STUDY; LIGHT; MAMMAL; MITRAL CELL; MOUSE; NERVOUS SYSTEM; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PYRIFORM CORTEX; REPRODUCIBILITY; STIMULUS RESPONSE; TRANSGENIC MOUSE;

ANIMALS; CELL COUNT; CEREBRAL CORTEX; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; ION CHANNELS; LIGHT; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEURONS; OLFACTORY BULB; PHOTIC STIMULATION; PROMOTER REGIONS (GENETICS);

EID: 34147126914     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.03.005     Document Type: Article

References (64)

1. Allison A.C. The morphology of the olfactory system in vertebrates. Biol. Rev. 28 (1953) 195-244
2. Aungst J.L., Heyward P.M., Puche A.C., Karnup S.V., Hayar A., Szabo G., and Shipley M.T. Centre-surround inhibition among olfactory bulb glomeruli. Nature 426 (2003) 623-629
3. Balu R., Larimer P., and Strowbridge B.W. Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J. Neurophysiol. 92 (2004) 743-753
4. Belluscio L., and Katz L.C. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J. Neurosci. 21 (2001) 2113-2122
5. Bi A., Cui J., Ma Y., Olshevskaya E., Pu M., Dizhoor A., and Pan Z. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50 (2006) 23-33
6. Boyden E.S., Zhang F., Bamberg E., Nagel G., and Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8 (2005) 1263-1268
7. Buck L.B. Olfactory receptors and odor coding in mammals. Nutr. Rev. 62 (2004) S184-S188
8. Buonviso N., Revial M.F., and Jourdan F. The projections of mitral cells from small local regions of the olfactory bulb: an anterograde tracing study using PHA-L (Phaseolus vulgaris leucoagglutinin). Eur. J. Neurosci. 3 (1991) 493-500
9. Caroni P. Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J. Neurosci. Methods 71 (1997) 3-9
10. Chen B.E., Lendvai B., Nimchinsky E.A., Burbach B., Fox K., and Svoboda K. Imaging high-resolution structure of GFP-expressing neurons in neocortex in vivo. Learn. Mem. 7 (2000) 433-441
11. De Paola V., Holtmaat A., Knott G., Song S., Wilbrecht L., Caroni P., and Svoboda K. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49 (2006) 861-875
12. Feng G., Mellor R.H., Bernstein M., Keller-Peck C., Nguyen Q.T., Wallace M., Nerbonne J.M., Lichtman J.W., and Sanes J.R. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28 (2000) 41-51
13. Feng G., Lu J., and Gross J. Generation of transgenic mice. Methods Mol. Med. 9 (2004) 255-267
14. Flusberg B.A., Cocker E.D., Piyawattanametha W., Jung J.C., Cheung E.L., and Schnitzer M.J. Fiber-optic fluorescence imaging. Nat. Methods 2 (2005) 941-950
15. Flusberg B.A., Jung J.C., Cocker E.D., Anderson E.P., and Schnitzer M.J. In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. Opt. Lett. 30 (2005) 2272-2274
16. Franks K.M., and Isaacson J.S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49 (2006) 357-363
17. Gan W.B., Grutzendler J., Wong W.T., Wong R.O., and Lichtman J.W. Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 27 (2000) 219-225
18. Haberly L.B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26 (2001) 551-576
19. Hamada S., Senzaki K., Hamaguchi-Hamada K., Tabuchi K., Yamamoto H., Yamamoto T., Yoshikawa S., Okano H., and Okado N. Localization of 5-HT2A receptor in rat cerebral cortex and olfactory system revealed by immunohistochemistry using two antibodies raised in rabbit and chicken. Brain Res. Mol. Brain Res. 54 (1998) 199-211
20. Hardy A., Palouzier-Paulignan B., Duchamp A., Royet J.P., and Duchamp-Viret P. 5-Hydroxytryptamine action in the rat olfactory bulb: in vitro electrophysiological patch-clamp recordings of juxtaglomerular and mitral cells. Neuroscience 131 (2005) 717-731
21. Holtmaat A., Wilbrecht L., Knott G.W., Welker E., and Svoboda K. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441 (2006) 979-983
22. Illig K.R., and Haberly L.B. Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457 (2003) 361-373
23. Ishizuka T., Kakuda M., Araki R., and Yawo H. Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels. Neurosci. Res. 54 (2006) 85-94
24. Johnson D.M., Illig K.R., Behan M., and Haberly L.B. New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex functions like "association" cortex in other sensory systems. J. Neurosci. 20 (2000) 6974-6982
25. Kandel E.R., Schwartz J.H., and Jessell T.M. Principles of Neuroscience. Fourth Edition (2000), The McGraw-Hill Companies, Columbus, OH
26. Karpova A.Y., Tervo D.G., Gray N.W., and Svoboda K. Rapid and reversible inactivation of synaptic transmission in genetically targeted neurons. Neuron 48 (2005) 727-735
27. Kobbert C., Apps R., Bechmann I., Lanciego J.L., Mey J., and Thanos S. Current concepts in neuroanatomical tracing. Prog. Neurobiol. 62 (2000) 327-351
28. Kohwi M., Osumi N., Rubenstein J.L., and Alvarez-Buylla A. Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J. Neurosci. 25 (2005) 6997-7003
29. Lei H., Mooney R., and Katz L.C. Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J. Neurosci. 26 (2006) 12023-12032
30. Li X., Gutierrez M., Hansen G., Han J., Melanie M.D., Chiel H., Hegemann P., Landmesser L., and Herlitze S. Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. Proc. Natl. Acad. Sci. USA 102 (2005) 17816-17821
31. Liedtke W., Tobin D.M., Bargmann C.I., and Friedman J.M. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 100 Suppl 2 (2003) 14531-14536
32. Lima S.Q., and Miesenbock G. Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121 (2005) 141-152
33. Lin D.Y., Shea S.D., and Katz L.C. Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50 (2006) 937-949
34. Lledo P.M., Gheusi G., and Vincent J.D. Information processing in the mammalian olfactory system. Physiol. Rev. 85 (2005) 281-317
35. Luo M., and Katz L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32 (2001) 1165-1179
36. Maskos U., Kissa K., St Cloment C., and Brulet P. Retrograde trans-synaptic transfer of green fluorescent protein allows the genetic mapping of neuronal circuits in transgenic mice. Proc. Natl. Acad. Sci. USA 99 (2002) 10120-10125
37. McGann J.P., Pirez N., Gainey M.A., Muratore C., Elias A.S., and Wachowiak M. Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48 (2005) 1039-1053
38. McLean J.H., Darby-King A., and Paterno G.D. Localization of 5-HT2A receptor mRNA by in situ hybridization in the olfactory bulb of the postnatal rat. J. Comp. Neurol. 353 (1995) 371-378
39. Miesenbock G. Genetic methods for illuminating the function of neural circuits. Curr. Opin. Neurobiol. 14 (2004) 395-402
40. Mombaerts P. Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286 (1999) 707-711
41. Mombaerts P. Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol. 22 (2006) 713-737
42. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., and Axel R. Visualizing an olfactory sensory map. Cell 87 (1996) 675-686
43. Mori K., Takahashi Y.K., Igarashi K.M., and Yamaguchi M. Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol. Rev. 86 (2006) 409-433
44. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100 (2003) 13940-13945
45. Nagel G., Brauner M., Liewald J.F., Adeishvili N., Bamberg E., and Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15 (2005) 2279-2284
46. Nagel G., Szellas T., Kateriya S., Adeishvili N., Hegemann P., and Bamberg E. Channelrhodopsins: directly light-gated cation channels. Biochem. Soc. Trans. 33 (2005) 863-866
47. Ojima H., Mori K., and Kishi K. The trajectory of mitral cell axons in the rabbit olfactory cortex revealed by intracellular HRP injection. J. Comp. Neurol. 230 (1984) 77-87
48. Parrish-Aungst S., Shipley M.T., Erdelyi G., Szabo G., and Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 501 (2007) 825-836
49. Piyawattanametha W., Barretto R.P., Ko T.H., Flusberg B.A., Cocker E.D., Ra H., Lee D., Solgaard O., and Schnitzer M.J. Fast-scanning two-photon fluorescence imaging based on a microelectromechanical systems two- dimensional scanning mirror. Opt. Lett. 31 (2006) 2018-2020
50. Shepherd G.M. Synaptic Organization of the Brain. Fifth Edition (2004), Oxford University Press, New York
51. Shepherd G.M., Chen W.R., and Greer C.A. The Olfactory Bulb. In: Shepherd G.M. (Ed). Synaptic Organization of the Brain (2004), Oxford University Press, New York 165-216
52. Shoham S., O'Connor D.H., Sarkisov D.V., and Wang S.S. Rapid neurotransmitter uncaging in spatially defined patterns. Nat. Methods 2 (2005) 837-843
53. Song C.K., Enquist L.W., and Bartness T.J. New developments in tracing neural circuits with herpesviruses. Virus Res. 111 (2005) 235-249
54. Tabor R., Yaksi E., Weislogel J.M., and Friedrich R.W. Processing of odor mixtures in the zebrafish olfactory bulb. J. Neurosci. 24 (2004) 6611-6620
55. Urban N.N. Lateral inhibition in the olfactory bulb and in olfaction. Physiol. Behav. 77 (2002) 607-612
56. Urban N.N., and Sakmann B. Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J. Physiol. 542 (2002) 355-367
57. Wang H., Peca J., Matsusaki M., Matsusaki K., Noguchi J., Qui L., Wang D., Zhang F., Boyden E., Deisseroth K., et al. High-speed mapping of synaptic connectivity using photostimulation in channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. USA (2007) in press
58. Yokoi M., Mori K., and Nakanishi S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92 (1995) 3371-3375
59. Zemelman B.V., Lee G.A., Ng M., and Miesenbock G. Selective photostimulation of genetically ChARGed neurons. Neuron 33 (2002) 15-22
60. Zemelman B.V., Nesnas N., Lee G.A., and Miesenbock G. Photochemical gating of heterologous ion channels: remote control over genetically designated populations of neurons. Proc. Natl. Acad. Sci. USA 100 (2003) 1352-1357
61. Zhang Y., and Oertner T.G. Optical induction of synaptic plasticity using a light-sensitive channel. Nat. Methods 2 (2007) 139-141
62. Zou Z., and Buck L.B. Combinatorial effects of odorant mixes in olfactory cortex. Science 311 (2006) 1477-1481
63. Zou Z., Horowitz L.F., Montmayeur J.P., Snapper S., and Buck L.B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414 (2001) 173-179
64. Zou Z., Li F., and Buck L.B. Odor maps in the olfactory cortex. Proc. Natl. Acad. Sci. USA 102 (2005) 7724-7729