Submillisecond optical reporting of membrane potential in situ using a neuronal tracer dye

Journal of Neuroscience

Volumn 29, Issue 29, 2009, Pages 9197-9209

  Bradley, Jonathan ^a   Luo, Ray ^b   Otis, Thomas S ^a,b   DiGregorio, David A ^a  

^a CNRS   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIO; DIPICRYLAMINE; FLUORESCENT DYE; TRACER; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ARTICLE; BRAIN SLICE; CELL STRAIN HEK293; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC POTENTIAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; ILLUMINATION; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NON INVASIVE PROCEDURE; OPTICS; PRIORITY JOURNAL; PURKINJE CELL; SENSOR; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; CELL LINE; CEREBELLUM; CYTOLOGICAL TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HIPPOCAMPUS; HUMANS; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEURONS; PATCH-CLAMP TECHNIQUES; PICRATES; PURKINJE CELLS; TIME FACTORS;

EID: 67651155949     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1240-09.2009     Document Type: Article

References (64)

1. Antic SD (2003) Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J Physiol 550:35-50.
2. Axelrod D (1979) Carbocyanine dye orientation in red cell membrane studied by microscopic fluorescence polarization. Biophys J 26:557-573.
3. Baker BJ, Kosmidis EK, Vucinic D, Falk CX, Cohen LB, Djurisic M, Zecevic D (2005) Imaging brain activity with voltage-and calcium-sensitive dyes. Cell Mol Neurobiol 25:245-282.
4. Baker BJ, Lee H, Pieribone VA, Cohen LB, Isacoff EY, Knopfel T, Kosmidis EK (2007) Three fluorescent protein voltage sensors exhibit low plasma membrane expression in mammalian cells. J Neurosci Methods 161:32-38.
5. Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451-465.
6. Blunck R, Chanda B, Bezanilla F (2005) Nano to micro-fluorescence measurements of electric fields in molecules and genetically specified neurons. J Membr Biol 208:91-102.
7. Chanda B, Asamoah OK, Blunck R, Roux B, Bezanilla F (2005a) Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement. Nature 436:852-856.
8. Chanda B, Blunck R, Faria LC, Schweizer FE, Mody I, Bezanilla F (2005b) A hybrid approach to measuring electrical activity in genetically specified neurons. Nat Neurosci 8:1619-1626.
9. Cohen LB, Salzberg BM, Davila HV, Ross WN, Landowne D, Waggoner AS, Wang CH (1974) Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol 19:1-36.
10. Cohen LB, Salzberg BM (1978) Optical measurement of membrane potential. Rev Physiol Biochem Pharmacol 83:35-88.
11. Cohen LB, Salzberg BM, Grinvald A (1978) Optical methods for monitoring neuron activity. Annu Rev Neurosci 1:171-182.
12. Dailey ME, Buchanan J, Bergles DE, Smith SJ (1994) Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J Neurosci 14:1060-1078.
13. Davie JT, Clark BA, Häusser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28:7599-7609.
14. DiFranco M, Capote J, Quiñonez M, Vergara JL (2007) Voltage-dependent dynamic FRET signals from the transverse tubules in mammalian skeletal muscle fibers. J Gen Physiol 130:581-600.
15. DiGregorio DA, Peskoff A, Vergara JL (1999) Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J Neurosci 19:7846-7859.
16. Djurisic M, Antic S, Chen WR, Zecevic D (2004) Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones. J Neurosci 24:6703-6714.
17. Dombeck DA, Blanchard-Desce M, Webb W (2004) Optical recording of action potentials with second-harmonic generation microscopy. J Neurosci 24:999-1003.
18. Dombeck DA, Sacconi L, Blanchard-Desce M, Webb WW (2005) Optical recording of fast neuronal membrane potential transients in acute mammalian brain slices by second-harmonic generation microscopy. J Neurophysiol 94:3628-3636.
19. Duemani Reddy G, Kelleher K, Fink R, Saggau P (2008) Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity. Nat Neurosci 11:713-720.
20. Eccles JC, Llinás R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 182:268-296.
21. Escobar AL, Monck JR, Fernandez JM, Vergara JL (1994) Localization of the site of Ca2 release at the level of a single sarcomere in skeletal muscle fibres. Nature 367:739-741.
22. A receptor γ2 subunit mutations linked to human epileptic syndromes differentially affect phasic and tonic inhibition. J Neurosci 27:14108-14116.
23. Fernández JM, Taylor RE, Bezanilla F (1983) Induced capacitance in the squid giant axon. Lipophilic ion displacement currents. J Gen Physiol 82:331-346.
24. Fisher JA, Barchi JR, Welle CG, Kim GH, Kosterin P, Obaid AL, Yodh AG, Contreras D, Salzberg BM (2008) Two-photon excitation of potentiometric probes enables optical recording of action potentials from Mammalian nerve terminals in situ. J Neurophysiol 99:1545-1553.
25. Fromherz P, Hübener G, Kuhn B, Hinner MJ (2008) ANNINE-6plus, a voltage-sensitive dye with good solubility, strong membrane binding and high sensitivity. Eur Biophys J 37:509-514.
26. Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW (2000) Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 27:219-225.
27. González JE, Tsien RY (1995) Voltage sensing by fluorescence resonance energy transfer in single cells. Biophys J 69:1272-1280.
28. González JE, Tsien RY (1997) Improved indicators of cell membrane potential that use fluorescence resonance energy transfer. Chem Biol 4:269-277.
29. Grinvald A, Hildesheim R (2004) VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci 5:874-885.
30. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
31. Honig MG, Hume RI (1986) Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J Cell Biol 103:171-187.
32. Honig MG, Hume RI (1989) Carbocyanine dyes. Novel markers for labelling neurons. Trends Neurosci 12:336-338.
33. Khaliq ZM, Raman IM (2005) Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci 25:454-463.
34. Kole MH, Stuart GJ (2008) Is action potential threshold lowest in the axon? Nat Neurosci 11:1253-1255.
35. Kuhn B, Fromherz P, Denk W (2004) High sensitivity of Stark-shift voltagesensing dyes by one-or two-photon excitation near the red spectral edge. Biophys J 87:631-639.
36. Lichtman JW, Fraser SE (2001) The neuronal naturalist: watching neurons in their native habitat. Nat Neurosci 4 [Suppl]:1215-1220.
37. Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171-195.
38. Lu CC, Kabakov A, Markin VS, Mager S, Frazier GA, Hilgemann DW (1995) Membrane transport mechanisms probed by capacitance measurements with megahertz voltage clamp. Proc Natl Acad Sci U S A 92:11220-11224.
39. Luo L, Callaway EM, Svoboda K (2008) Genetic dissection of neural circuits. Neuron 57:634-660.
40. Majewska A, Yiu G, Yuste R (2000) A custom-made two-photon microscope and deconvolution system. Pflugers Arch 441:398-408.
41. Morgan JL, Wong RO (2008) Ballistic labeling with fluorescent dyes and indicators. Curr Protoc Neurosci 43:2.11.1-2.11.10.
42. Nielsen TA, DiGregorio DA, Silver RA (2004) Modulation of glutamate mobility reveals the mechanism underlying slow-rising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft. Neuron 42:757-771.
43. Nuriya M, Jiang J, Nemet B, Eisenthal KB, Yuste R (2006) Imaging membrane potential in dendritic spines. Proc Natl Acad Sci U S A 103:786-790.
44. Obaid AL, Koyano T, Lindstrom J, Sakai T, Salzberg BM (1999) Spatiotemporal patterns of activity in an intact mammalian network with single-cell resolution: optical studies of nicotinic activity in an enteric plexus. J Neurosci 19:3073-3093.
45. Obaid AL, Loew LM, Wuskell JP, Salzberg BM (2004) Novel naphthylstyrylpyridium potentiometric dyes offer advantages for neural network analysis. J Neurosci Methods 134:179-190.
46. Oberhauser AF, Fernandez JM (1995) Hydrophobic ions amplify the capacitive currents used to measure exocytotic fusion. Biophys J 69:451-459.
47. O'Brien JA, Lummis SC (2006) Diolistic labeling of neuronal cultures and intact tissue using a hand-held gene gun. Nat Protoc 1:1517-1521.
48. Otsu Y, Bormuth V, Wong J, Mathieu B, Dugué GP, Feltz A, Dieudonné S (2008) Optical monitoring of neuronal activity at high frame rate with a digital random-access multiphoton (RAMP) microscope. J Neurosci Methods 173:259-270.
49. Palmer LM, Stuart GJ (2006) Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26:1854-1863.
50. Parsons TD, Salzberg BM, Obaid AL, Raccuia-Behling F, Kleinfeld D (1991) Long-term optical recording of patterns of electrical activity in ensembles of cultured Aplysia neurons. J Neurophysiol 66:316-333.
51. Petersen CC, Grinvald A, Sakmann B (2003) Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J Neurosci 23:1298-1309.
52. Ratzliff AH, Howard AL, Santhakumar V, Osapay I, Soltesz I (2004) Rapid deletion of mossy cells does not result in a hyperexcitable dentate gyrus: implications for epileptogenesis. J Neurosci 24:2259-2269.
53. Rohr S, Salzberg BM (1994) Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale. Biophys J 67:1301-1315.
54. Salzberg BM, Davila HV, Cohen LB (1973) Optical recording of impulses in individual neurones of an invertebrate central nervous system. Nature 246:508-509.
55. Salzberg BM, Obaid AL, Bezanilla F (1993) Microsecond response of a voltage-sensitive merocyanine dye: fast voltage-clamp measurements on squid giant axon. Jpn J Physiol 43 [Suppl 1]:S37-S41.
56. Sjulson L, Miesenböck G (2007) Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda) 22:47-55.
57. Sjulson L, Miesenböck G (2008) Rational optimization and imaging in vivo of a genetically encoded optical voltage reporter. J Neurosci 28:5582-5593.
58. Stuart G, Häusser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
59. Taraska JW, Zagotta WN (2007) Cyclic nucleotide-regulated ion channels: spotlight on symmetry. Structure 15:1023-1024.
60. Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008) Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 5:683-685.
61. Wu CC, Russell RM, Nguyen RT, Karten HJ (2003) Tracing developing pathways in the brain: a comparison of carbocyanine dyes and cholera toxin b subunit. Neuroscience 117:831-845.
62. Zhang Y, Chou JH, Bradley J, Bargmann CI, Zinn K (1997) The Caenorhabditis elegans seven-transmembrane protein ODR-10 functions as an odorant receptor in mammalian cells. Proc Natl Acad Sci U S A 94:12162-12167.
63. Zhou WL, Yan P, Wuskell JP, Loew LM, Antic SD (2007) Intracellular long-wavelength voltage-sensitive dyes for studying the dynamics of action potentials in axons and thin dendrites. J Neurosci Methods 164:225-239.
64. Zhou WL, Yan P, Wuskell JP, Loew LM, Antic SD (2008) Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons. Eur J Neurosci 27:923-936.