Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1529, 2009, Pages 2453-2467

  Homma, Ryota ^a   Baker, Bradley J ^a   Jin, Lei ^a   Garaschuk, Olga ^b   Konnerth, Arthur ^c   Cohen, Lawrence B ^a,d   Zecevic, Dejan ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d RedShirtImaging LLC   (United States)

Author keywords

Calcium sensitive dyes; Neural networks; One photon (wide field) microscopy; Two photon microscopy; Voltage sensitive dyes

Indexed keywords

BRAIN; DYE; FIELD METHOD; IMAGING METHOD; NERVOUS SYSTEM;

MAMMALIA;

EID: 69949090456     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0084     Document Type: Review

References (91)

1. Antic, S. 2003 Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. 550, 35-50. (doi:10.1113/jphysiol. 2002.033746) (Pubitemid 36869268)
2. Antic, S. & Zecevic, D. 1995 Optical signals from neurons with internally applied voltage-sensitive dyes. J. Neurosci. 15, 1392-1405.
3. Antic, S., Major, G. & Zecevic, D. 1999 Fast optical recording of membrane potential changes from dendrites of pyramidal neurons. J. Neurophysiol. 82, 1615-1621. (Pubitemid 29439723)
4. Antic, S., Wuskell, J. P., Loew, L. & Zecevic, D. 2000 Functional profile of the giant metacerebral neuron of Helix aspersa: temporal and spatial dynamics of electrical activity in situ. J. Physiol. 527, 55-69. (doi:10.1111/ J.1469-7793.2000.00055.x) (Pubitemid 30649584)
5. Ataka, K. & Pieribone, V. A. 2002 A genetically-targetable fluorescent probe of channel gating with rapid kinetics. Biophys. J. 82, 509-516. (doi:10.1016/S0006-3495 (02)75415-5) (Pubitemid 34289823)
6. Baird, G. S., Zacharias, D. A. & Tsien, R. Y. 1999 Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl Acad. Sci. USA 96, 11 241-11246. (doi:10.1073/pnas.96.20.11241)
7. Baker, B. J., Lee, H., Pieribone, V. A., Cohen, L. B., Isacoff, E. Y., Knopfel, T. & Kosmidis, E. K. 2007 Fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells. J. Neurosci. Methods 161, 32-38. (doi:10.1016/j.jneumeth.2006.10.005) (Pubitemid 46349245)
8. Berridge, M. J., Lipp, P. & Bootman, M. D. 2000 The versatility and universality of calcium signaling. Nat. Rev. Mol. Cell. Biol. 1, 11-21. (doi:10.1038/35036035)
9. Blasdel, G. G. & Salama, G. 1986 Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579-585. (doi:10.1038/321579a0) (Pubitemid 16042209)
10. Bonhoeffer, T. & Grinvald, A. 1993 The layout of isoorientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization. J. Neurosci. 13, 4157-4180. (Pubitemid 23299941)
11. Bouevitch, O., Lewis, A., Pinevsky, I., Wuskell, J. & Loew, L. 1993 Probing membrane potential with nonlinear optics. Biophys. J. 65, 672-679. (doi:10.1016/S0006-3495 (93)81126-3) (Pubitemid 23263879)
12. Braddick, H. J. J. 1960 Photoelectric photometry. Rep. Prog. Phys. 23, 154-175. (doi:10.1088/0034-4885/23/1/303)
13. Briggman, K. L. & Kristan, W. B. 2006 Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J. Neurosci. 26, 10925-10933. (doi:10.1523/ JNEUROSCI.3265-06.2006)
14. 2+ imaging. Pflugers Arch. 446, 766-773. (doi:10.1007/s00424-003- 1138-4)
15. Cacciatore, T. W., Brodfuehrer, P. D., Gonzalez, J. E., Jiang, T., Adams, S. R., Tsien, R. Y., Kristan Jr, W. B. & Kleinfeld, D. 1999 Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes. Neuron 23, 449-459. (doi:10.1016/S0896-6273(00)80799-0) (Pubitemid 29359917)
16. Canepari, M., Djurisic, M. & Zecevic, D. 2007 Dendritic signals from rat hippocampal CAl pyramidal neurons during coincident pre- and post-synaptic activity: a combined voltage- and calcium-imaging study. J. Physiol. 580, 463-484. (doi:10.1113/jphysiol.2006.125005) (Pubitemid 46564176)
17. Cohen, L. B. & Keynes, R. D. 1971 Changes in light scattering associated with the action potential in crab nerves. J. Physiol. 212, 259-275.
18. Cohen, L. B. & Lesher, S. 1986 Optical monitoring of membrane potential: methods of multisite optical measurement. Soc. Gen. Physiol. Ser. 40, 71-99.
19. Cohen, L. B. & Salzberg, B. M. 1978 Optical measurement of membrane potential. Rev. Physiol. Biochem. Pharmacol. 83, 35-88.
20. Cohen, L. B., Keynes, R. D. & Hille, B. 1968 Light scattering and birefringence changes during nerve activity. Nature 218, 438-441. (doi:10.1038/218438a0)
21. Davila, H. V., Salzberg, B. M., Cohen, L. B. & Waggoner, A. S. 1973 A large change in axon fluorescence that provides a promising method for measuring membrane potential. Nat. New Biol. 241, 159-160.
22. 2+ indicator protein. Eur. J. Neurosci. 22, 627-635. (doi:10.1111/j. 1460-9568.2005.04250.x)
23. Dimitrov, D., He, Y., Mutoh, H., Baker, B. J., Cohen, L., Akemann, W. & Knopfel, T. 2007 Engineering and characterization of an enhanced fluorescent protein voltage sensor. PLoS ONE 2, e440. (doi:10.1371/journal. pone.0000440)
24. Djurisic, M., Antic, S., Chen, W.-R. & Zecevic, D. 2004 Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones. J. Neurosci. 24, 6703-6714. (doi:10.1523/JNEUROSCI.0307-04.2004) (Pubitemid 38993890)
25. Djurisic, M., Popovic, M., Carnevale, N. & Zecevic, D. 2008 Functional structure of the mitral cell dendritic tuft in the rat olfactory bulb. J. Neurosci. 28, 4057-4068. (doi:10. 1523/JNEUROSCI.5296-07.2008)
26. Dombeck, D. A., Sacconi, L., Blanchard-Desce, M. & Webb, W. W. 2005 Optical recording of fast neuronal membrane potential transients in acute mammalian brain slices by second-harmonic generation microscopy. J. Neurophysiol. 94, 3628-3636. (doi:10.1152/jn.00416.2005) (Pubitemid 41504796)
27. Friedrich, R. W. & Korsching, S. I. 1997 Combinatorial, and chemotropic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18, 737-752. (doi:10.1016/S0896-6273(00)80314-l)
28. Fromherz, P., Dambacher, K. H., Ephardt, H., Lambacher, A., Müller, C. O., Neigl, R., Schaden, H., Schenk, O. & Vetter, T. 1991 Fluorescent dyes as probes of voltage transients in neuron membranes: progress report. Ber. Bunsenges. Phys. Chem. 95, 1333-1345.
29. Garaschuk, O., Milos, R. I. & Konnerth, A. 2006 Targeted bulk-loading of fluorescent indicators for two-photon brain imaging in vivo. Nat. Prot. 1, 380-386. (doi:10. 1038/nprot.2006.58)
30. Garaschuk, O., Griesbeck, O. & Konnerth, A. 2007 Troponin C-based biosensors: a new family of genetically encoded indicators for in vivo calcium imaging in the nervous system. Cell Calcium 42, 351-361. (doi:10. 1016/j.ceca.2007.02.011) (Pubitemid 47264000)
31. Gonzalez, J. E. & Tsien, R. Y. 1995 Voltage sensing by fluorescence energy transfer in single cells. Biophys. J. 69, 1272-1280. (doi:10.1016/S0006- 3495(95)80029-9)
32. Grinvald, A., Hildesheim, R., Farber, I. C. & Anglister, L. 1982 Improved fluorescent probes for the measurement of rapid changes in membrane potential. Biophys. J. 39, 301-308. (doi:10.1016/S0006-3495(82)84520-7) (Pubitemid 13240779)
33. Grinvald, A., Lieke, E., Frostig, R. D., Gilbert, C. D. & Wiesel, T. N. 1986 Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361-364. (doi:l0.1038/324361a0) (Pubitemid 17180109)
34. Grinvald, A., Frostig, R. D., Lieke, E. & Hildesheim, R. 1988 Optical imaging of neuronal activity. Physiol. Rev. 68, 1285-1366.
35. Gross, E., Bedlack, R. S. & Loew, L. M. 1994 Dualwavelength ratiometric fluorescence measurements of the membrane dipole potential. Biophys. J. 67, 208-216. (doi:10.1016/S0006-3495(94)80471-0) (Pubitemid 24197886)
36. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
37. Gupta, R. K., Salzberg, B. M., Grinvald, A., Cohen, L. B., Kamino, K., Lesher, S., Boyle, M. B., Waggoner, A. S. & Wang, C. H. 1981 Improvements in optical methods for measuring rapid changes in membrane potential. J. Membr. Biol. 58, 123-137. (doi:10.1007/BF01870975) (Pubitemid 11148778)
38. Hamer, F. M. 1964 The cyanine dyes and related compounds. New York, NY: Wiley.
39. 2+ indicator proteins in transgenic mice under TET control. PLoS Biol. 2, 763-775. (doi:10.1371/journal.pbio.0020163)
40. Heim, N. & Griesbeck, O. 2004 Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J. Biol. Chem. 279, 14 280-14 286. (doi:10.1074/jbc.M312751200) (Pubitemid 38468968)
41. Heim, N., Garaschuk, O., Friedrich, M. W., Mank, M., Milos, R. I., Kovalchuk, Y., Konnerth, A. & Griesbeck, O. 2007 Improved calcium imaging in transgenic mice expressing a troponin-C based biosensor. Nat. Methods 4, 127-129. (doi:10.1038/nmeth1009) (Pubitemid 46454679)
42. Helmchen, F. & Denk, W. 2005 Deep tissue two-photon microscopy. Nat. Methods 2, 932-940. (doi:10.1038/ nmeth818)
43. 2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70, 1069-1081. (doi:10.1016/S0006-3495(96)79653-4)
44. Homma, R., Baker, B., Jin, L., Garaschuk, O., Konnerth, A., Cohen, L. B., Bleau, C. X. & Zecevic, D. 2009 Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. In Dynamic imaging: towards quantitative understanding of brain function. (ed. F. Hyder). Methods Mol. Biol. 489, pp. 43-79.
45. Inoue, S. 1986 Video microscopy, p. 128. New York, NY: Plenum Press.
46. Kerr, J. N., Greenberg, D. & Helmchen, F. 2005 Imaging input and output of neocortical networks in vivo. Proc. Natl Acad Sci. USA 102, 14 063-14 068. (doi:10.1073/ pnas.0506029102) (Pubitemid 41377703)
47. Kleinfeld, D. & Delaney, K. R. 1996 Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes. J. Comp. Neurol 375, 89-108. (doi:l0.1002/(SICI) 1096-9861 (19961104)375:1<89::AID-CNE6>3.0.CO;2-K) (Pubitemid 26378146)
48. Li, J., Mack, J. A., Souren, M., Yaksi, E., Higashijima, S., Mione, M., Fetcho, J. R. & Friedrich, R. W. 2005 Early development of functional spatial maps in the zebraflsh olfactory bulb. J. Neurosci. 25, 5784-5795. (doi:10. 1523/JNEUROSCI.0922-05.2005) (Pubitemid 40847891)
49. Loew, L. M. 1993 Confbcal microscopy of Potentiometric fluorescent dyes. Methods Cell Biol. 38, 195-209. (doi:10.1016/S0091-679X(08)61003-l)
50. Loew, L. M., Cohen, L. B., Salzberg, B. M., Obaid, A. L. & Bezanilla, F. 1985 Charge-shift probes of membrane potential. Characterization of aminostyrylpyridinium dyes on the squid giant axon. Biophys. J. 47, 71-77. (doi: 10.1016/S0006-3495(85)83878-9)
51. Loew, L. M., Cohen, L. B., Dix, J., Fluhler, E. N., Montana, V., Salama, G. & Wu, J. Y. 1992 A napthyl analog of the aminostyryl pyridinium class of Potentiometrie membrane dyes shows consistent sensitivity in a variety of tissue, cell, and model membrane preparations. J. Membr. Biol. 130, 1-10. (doi:10.1007/BF00233734)
52. Malmstadt, H. V., Enke, C. G., Crouch, S. R. & Harlick, G. 1974 Electronic measurements for scientists. Menlo Park, CA: Benjamin.
53. Mank, M., Reiff, D. F., Heim, N., Friedrich, M. W., Borst, A. & Griesbeck, O. 2006 A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys. J. 90, 1790-1796. (doi:10.1529/biophysj.105. 073536)
54. Millard, A. C., Jin, L., Wuskell, J. P., Boudreau, D. M., Lewis, A. & Loew, L. M. 2005 Wavelength- and timedependence of Potentiometric nonlinear optical signals from styryl dyes. J. Membr. Biol. 208, 103-111. (doi: 10. 1007/s00232-005-0823-y)
55. Miyawaki, A. 2005 Innovations in the imaging of brain functions using fluorescent proteins. Neuron 48, 189-199. (doi:10.1016/j.neuron.2005.10.003) (Pubitemid 41476353)
56. 2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887. (doi: 10.1038/42264)
57. Momose-Sato, Y., Sato, K., Sakai, T., Hirota, A., Matsutani, K. & Kamino, K. 1995 Evaluation of optimal voltagesensitive dyes for optical measurement of embryonic neural activity. J. Membr. Biol. 144, 167-176. (doi:10. 1007/BF00232802)
58. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K. & Okamura, Y. 2005 Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243. (doi:10.1038/nature03650) (Pubitemid 40943089)
59. Nagai, T., Sawano, A., Park, E. S. & Miyawaki, A. 2001 Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc. Natl Acad. Sci. USA 98, 3197-3202. (doi: 10.1073/pnas.051636098) (Pubitemid 32220822)
60. 2+ by circularly permuted yellow fluorescent proteins. Proc. Natl Acad. Sci. USA 101, 10 554-10 559. (doi:10.1073/pnas.0400417101)
61. 2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19, 137-141. (doi: 10.1038/84397)
62. Nakashima, M., Yamada, S., Shiono, S., Maeda, M. & Satoh, F. 1992 448-detector optical recording system: development and application to Aplysia gill-withdrawal reflex. IEEE Trans. Biomed. Eng. 39, 26-36. (doi:10. 1109/10.108124)
63. Neher, E. & Augustine, G. J. 1992 Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. 450, 273-301.
64. Niell, C. M. & Smith, S. J. 2005 Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941-951. (doi:10.1016/j. neuron.2005.01.047)
65. Nimmerjahn, A., Kirchhoff, F., Kerr, J. N. D. & Helmchen, F. 2004 Sulfbrhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1, 31-37. (doi:10.1038/nmeth706)
66. Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P. & Reid, R. C. 2005 Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597-603. (doi:10.1038/nature03274)
67. 2+ imaging of dendritic spines. Anal. Chem. 77, 5861-5869. (doi:10.1021/ac0506837)
68. Onimaru, H. & Homma, I. 2005 Optical imaging of respiratory neuron activity from the dorsal view of the lower brainstem. Clin. Exp. Pharmacol. Physiol. 32, 297-301. (doi:10.1111/j.l440-1681.2005.04187.x) (Pubitemid 40586065)
69. Orbach, H. S., Cohen, L. B. & Grinvald, A. 1985 Optical mapping of electrical activity in rat somatosensory and visual cortex. J. Neurosci. 5, 1886-1895. (Pubitemid 15234444)
70. Palmer, L. M. & Stuart, G. J. 2006 Site of action potential initiation in layer 5 pyramidal neurons. J. Neurosci. 26, 1854-1863. (doi: 10.1523/JNEUROSCI.4812-05.2006)
71. Reiff, D. F., Ihring, A., Guerrero, G., Isacoff, E. Y., Joesch, M., Nakai, J. & Borst, A. 2005 In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25, 4766-4778. (doi:10.1523/JNEUROSCI. 4900-04.2005) (Pubitemid 40664125)
72. Rohr, S. & Salzberg, B. M. 1994 Multiple site optical recording of transmembrane voltage in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale. Biophys. J. 67, 1301-1315. (doi:10.1016/S0006-3495(94)80602-2) (Pubitemid 24272984)
73. Ross, W. N., Salzberg, B. M., Cohen, L. B. & Davila, H. V. 1974 A large change in dye absorption during the action potential. Biophys. J. 14, 983-986. (doi:10.1016/S0006-3495(74)85963-1)
74. Salzberg, B. M., Grinvald, A., Cohen, L. B., Davila, H. V. & Ross, W. N. 1977 Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons. J. Neurophysiol. 40, 1281-1291. (Pubitemid 8233139)
75. Siegel, M. S. & Isacoff, E. Y. 1997 A genetically encoded optical probe of membrane voltage. Neuron 19, 735-741. (doi:10.1016/S0896-6273(00)80955- l)
76. Sjostrom, P. J., Rancz, E. A., Roth, A. & Hausser, M. 2008 Dendritic excitability and synaptic plasticity. Physiol. Rev. 88, 769-840. (doi:10.1152/physrev.00016.2007)
77. Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. 2003 In vivo two-photon calcium imaging of neuronal networks. Proc. Natl Acad. Sci. USA 100, 7319-7324. (doi:10.1073/pnas.l232232100) (Pubitemid 36706436)
78. Stuart, G. J. & Sakmann, B. 1994 Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72. (doi:10.1038/367069a0) (Pubitemid 24038533)
79. Sullivan, M. R., Nimmerjahn, A., Sarkisov, D. V., Helmchen, F. & Wang, S. S. 2005 In vivo calcium imaging of circuit activity in cerebellar cortex. J. Neurophysiol. 94, 1636-1644. (doi:10.1152/jn.01013.2004) (Pubitemid 41061393)
80. Teisseyre, T. Z., Millard, A. C., Yan, P., Wuskell, J. P., Wei, M. D., Lewis, A. & Loew, L. M. 2007 Nonlinear optical Potentiometric dyes optimized for imaging with 1064-nm light. J. Biomed. Opt. 12, 044001. (doi:10.1117/1. 2772276) (Pubitemid 350066407)
81. Tsau, Y., Wenner, P., O'Donovan, M. J., Cohen, L. B., Loew, L. M. & Wuskell, J. P. 1996 Dye screening and signal-to-noise ratio for retrogradely transported voltagesensitive dyes. J. Neurosci. Methods 70, 121-129. (doi:10.1016/S0165-0270(96)00109-4) (Pubitemid 27016211)
82. Tsien, R. Y. 1981 A non-disruptive technique for loading calcium buffers and indicators into cells. Nature 290, 527-528. (doi:10.1038/290527a0)
83. Tsien, R. W. & Tsien, R. Y. 1990 Calcium channels, stores, and oscillations. Annu. Rev. Cell Biol. 6, 715-760. (doi:10.1146/annurev.cb.06. 110190.003435)
84. Tsutsui, H., Karasawa, S., Okamura, Y. & Miyawaki, A. 2008 Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 8, 683-685. (doi:0.1038/nmeth.l235)
85. Verkhratsky, A. 2005 Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol. Rev. 85, 201-279. (doi:10.1152/physrev.00004. 2004) (Pubitemid 40173995)
86. Wachowiak, M. & Cohen, L. B. 2001 Representation of odorants by receptor neuron input to the mouse olfactory bulb. Neuron 32, 723-735. (doi:10.1016/S0896-6273(01)00506-2) (Pubitemid 33145204)
87. Wachowiak, M. & Cohen, L. B. 2003 Correspondence between odorant-evoked patterns of receptor neuron input and intrinsic optical signals in the mouse olfactory bulb. J. Neurophysiol. 89, 1623-1639. (doi:10.1152/jn. 00747.2002) (Pubitemid 36324004)
88. Waggoner, A. S. & Grinvald, A. 1977 Mechanisms of rapid optical changes of potential-sensitive dyes. Ann. NY. Acad. Sci. 303, 217-241. (Pubitemid 8272078)
89. Zecevic, D. 1996 Multiple spike-initiation zones in single neurons revealed by voltage-sensitive dyes. Nature 381, 322-325. (doi: 10.1038/381322a0) (Pubitemid 26156088)
90. Zhang, J., Campbell, R. E., Ting, A. Y. & Tsien, R. Y. 2002 Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3, 906-918. (doi:10.1038/nrm976) (Pubitemid 35477369)
91. Zochowski, M., Wachowiak, D. M., Falk, C. X., Cohen, L. B., Lam, Y-W, Antic, S. & Zecevic, D. 2000 Imaging membrane potential with voltage-sensitive dyes. Biol. Bull. 198, 1-21. (doi:10.2307/1542798) (Pubitemid 30119045)