Two-photon excitation of potentiometric probes enables optical recording of action potentials from mammalian nerve terminals in situ

Journal of Neurophysiology

Volumn 99, Issue 3, 2008, Pages 1545-1553

  Fisher, Jonathan A N ^a,d   Barchi, Jonathan R ^b   Welle, Cristin G ^c   Kim, Gi Ho ^c   Kosterin, Paul ^c   Obaid, Ana Lía ^c   Yodh, Arjun G ^a   Contreras, Diego ^c   Salzberg, Brian M ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN; ELECTRIC ACTIVITY; ELECTRODE; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE; MAMMAL; MOUSE; NERVE ENDING; NERVE POTENTIAL; NEUROHYPOPHYSIS; NONHUMAN; POTENTIOMETRY; PRIORITY JOURNAL;

ACTION POTENTIALS; ANIMALS; FEMALE; FLUORESCENCE; FLUORESCENT DYES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PITUITARY GLAND, INTERMEDIATE; PRESYNAPTIC TERMINALS; PYRIDINIUM COMPOUNDS; SPECTROMETRY, FLUORESCENCE;

EID: 40949136074     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00929.2007     Document Type: Article

References (44)

1. Ang CW, Carlson GC, Coulter DA. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J Neurosci 25: 9567-9580, 2005.
2. Antic S, Zecevic D. Optical signals from neurons with internally applied voltage-sensitive dyes. J Neurosci 15: 1392-1405, 1995.
3. Bedlack RS Jr, Wei M, Loew LM. Localized membrane depolarizations and localized calcium influx during electric field-guided neurite growth. Neuron 9: 393-403, 1992.
4. Campagnola PJ, Wei MD, Lewis A, Loew LM. High-resolution nonlinear optical imaging of live cells by second harmonic generation. Biophys J 77: 3341-3349, 1999.
5. Civillico EF, Contreras D. Integration of evoked responses in supragranular cortex studied with optical recordings in vivo. J Neurophysiol 96: 336-351, 2006.
6. Cohen LB, Salzberg BM. Optical measurement of membrane potential. Rev Physiol Biochem Pharmacol 83: 35-88, 1978.
7. Collins JR. Change in the infra-red absorption spectrum of water with temperature. Physiol Rev 26: 771-779, 1925.
8. Contreras D, Llinás R. Voltage-sensitive dye imaging of neocortical spatiotemporal dynamics to afferent activation frequency. J Neurosci 21: 9403-9413, 2001.
9. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R. A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54: 105-120, 2007.
10. Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 248: 73-76, 1990.
11. Djurisic M, Antic S, Chen WR, Zecevic D. Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones. J Neurosci 24: 6703-6714, 2004.
12. Douglas WW. How do neurones secrete peptides? Exocytosis and its consequences, including "synaptic vesicle" formation, in the hypothalamo-neurohypophyseal system. Prog Brain Res 39: 21-39, 1973.
13. Fisher JAN. Linear and Non-Linear Fluorescence Imaging of Neuronal Activity (PhD thesis). Department of Physics and Astronomy, University of Pennsylvania, Philadelphia, PA, 2007.
14. Fisher JAN, Civillico EF, Contreras D, Yodh AG. in vivo fluorescence microscopy of neuronal activity in three dimensions by use of voltage-sensitive dyes. Opt Lett 29: 71-73, 2004.
15. Fisher JAN, Salzberg BM, Yodh AG. Near infrared two-photon excitation cross-sections of voltage-sensitive dyes. J Neurosci Methods 148: 94-102, 2005.
16. Gainer H, Wolfe SA Jr, Obaid AL, Salzberg BM. Action potentials and frequency-dependent secretion in the mouse neurohypophysis. Neuroendocrinology 43: 557-563, 1986.
17. Grinvald A, Lieke EE, Frostig RD, Hildesheim R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci 14: 2545-2568, 1994.
18. Grinvald A, Salzberg BM, Lev-Ram V, Hildesheim R. Optical recording of synaptic potentials from processes of single neurons using intracellular potentiometric dyes. Biophys J 51: 643-651, 1987.
19. Heer F, Hafizovic S, Ugniwenko T, Frey U, Franks W, Perriard E, Perriard JC, Blau A, Ziegler C, Hierlemann A. Single-chip microelectronic system to interface with living cells. Biosens Bioelectron 22: 2546-2553, 2007.
20. Hellwarth R, Christensen P. Nonlinear optical microscope examination of structures in polycrystalline ZnSe. Opt Commun 12: 318-322, 1974.
21. Jackson MB, Konnerth A, Augustine GJ. Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci USA 88: 380-384, 1991.
22. Kuhn B, Fromherz P, Denk W. High sensitivity of Stark-shift voltage-sensing dyes by one- or two-photon excitation near the red spectral edge. Biophys J 87: 631-639, 2004.
23. Kurtz R, Fricke M, Kalb J, Tinnefeld P, Sauer M. Application of multiline two-photon microscopy to functional in vivo imaging. J Neurosci Methods 151: 276-286, 2006.
24. Millard AC, Jin L, Wuskell JP, Boudreau DM, Lewis A, Loew LM. Wavelength- and time-dependence of potentiometric non-linear optical signals from styryl dyes. J Membr Biol 208: 103-111, 2005.
25. Moreaux L, Pons T, Dambrin V, Blanchard-Desce M, Mertz J. Electrooptic response of second-harmonic generation membrane potential sensors. Opt Lett 28: 625-627, 2003.
26. Muschol M, Kosterin P, Ichikawa M, Salzberg BM. Activity-dependent depression of excitability and calcium transients in the neurohypophysis suggests a model of "stuttering conduction". J Neurosci 23: 11352-11362, 2003.
27. Nordmann JJ. Ultrastructural morphometry of the rat neurohypophysis. J Anat 123: 213-218, 1977.
28. Nuriya M, Jiang J, Nemet B, Eisenthal KB, Yuste R. Imaging membrane potential in dendritic spines. Proc Natl Acad Sci USA 103: 786-790, 2006.
29. Obaid AL, Koyano T, Lindstrom J, Sakai T, Salzberg BM. 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, 1999.
30. Obaid AL, Loew LM, Wuskell JP, Salzberg BM. Novel naphthyl styrylpyridinium potentiometric dyes offer advantages for neural network analysis. J Neurosci Methods 134: 179-190, 2004.
31. Obaid AL, Nelson ME, Lindstrom J, Salzberg BM. Optical studies of nicotinic acetylcholine receptor subtypes in the guinea-pig enteric nervous system. J Exp Biol 208: 2981-3001, 2005.
32. Patolsky F, Timko BP, Yu G, Fang Y, Greytak AB, Zheng G, Lieber CM. Detection, stimulation, and inhibition of neuronal signals with high-density nanowire transistor arrays. Science 313: 1100-1104, 2006.
33. Petersen CC, Grinvald A, Sakmann B. 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, 2003.
34. Pons T, Mertz J. Membrane potential detection with second-harmonic generation and two-photon excited fluorescence: a theoretical comparison. Opt Commun 258: 203-209, 2006.
35. Richards B, Wolf E. Electromagnetic diffraction in optical systems II. Structure of the image field in an aplanatic system. Proc R Soc London A 253: 358-379, 1959.
36. Ross WN, Reichardt LF. Species-specific effects on the optical signals of voltage-sensitive dyes. J Membr Biol 48: 343-356, 1979.
37. Sacconi L, Dombeck DA, Webb WW. Overcoming photodamage in second-harmonic generation microscopy: real-time optical recording of neuronal action potentials. Proc Natl Acad Sci USA 103: 3124-3129, 2006.
38. Salzberg BM. Optical recording of electrical activity in neurons using molecular probes. In: Current Methods in Cellular Neurobiology, edited by Barker J, McKelvy J. New York: John Wiley, 1983, p. 139-187.
39. Salzberg BM, Obaid AL, Bezanilla F. Microsecond response of a voltage-sensitive merocyanine dye: fast voltage-clamp measurements on squid giant axon. Jpn J Physiol 43: S37-S41, 1993.
40. Salzberg BM, Obaid AL, Gainer H. Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis. J Gen Physiol 86: 395-411, 1985.
41. Sheppard CJR, Kompfner R, Gannaway J, Walsh D. The scanning harmonic optical microscope. IEEE J Quant Electron QE13: 100D, 1977.
42. Sims PJ, Waggoner AS, Wang CH, Hoffman JF. Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13: 3315-3330, 1974.
43. Sjulson L, Miesenboeck G. Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda) 22: 47-55, 2007.
44. Zipfel WR, Williams RM, Webb WW. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 21: 1369-1377, 2003.