Abstract
To evaluate the suitability of a variety of fast voltage-sensitive dyes for optical recording of rapid transmembrane potential activity in the embryonic nervous system, we screened over twenty dyes, including several newly synthesized probes, in three different embryonic neural preparations: cervical vagus nerve bundle, nodose ganglion, and brainstem from 7-day old chick embryos. Measurements of voltage-related optical signals were made using a multiple-site optical recordingsystem. Signal size, signal-to-noise ratio, photobleaching, and phototoxicity were examined. Several promising new merocyanine-rhodanine dyes for embryonic nervous systems were found.
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Albowitz, B., Kuhnt, U., Ehrenreich, L. 1990. Optical recording of epileptiform voltage changes in the neocortical slice. Exp. Brain Res. 81:241–256
Cohen, L.B., Lesher, S. 1986. Optical monitoring of membrane potential: methods of multisite optical measurement. In: Optical Methods in Cell Physiology. P. De Weer and B.M. Salzberg editors. pp. 71–99. John Wiley, New York
Cohen, L.B., Salzberg, B.M. 1978. Optical measurement of membrane potential. Rev. Physiol. Biochem. Pharmacol. 83:35–88
Cohen, L.B., Salzberg, B.M., Davila, H.V., Ross, W.N., Landowne, D., Waggoner, A.S., Wang, C.H. 1974. Changes in axon fluorescence during activity: Molecular probes of membrane potential. J. Membrane Biol. 19:1–36
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. Nature 241:159–160
Falk, C.X., Wu, J-Y., Cohen, L.B., Tang, A.C. 1993. Nonuniform expression of habituation in the activity of distinct classes of neurons in the Aplysia abdominal ganglion. J. Neurosci. 13:4072–4081
Fujii, S., Hirota, A., Kamino, K. 1981. Action potential synchrony in embryonic precontractile chick heart: Optical monitoring with potentiometric dyes. J. Physiol. 319:529–541
Grinvald, A. 1985. Real-time optical mapping of neuronal activity: from single growth cones to the intact mammalian brain. Annu. Rev. Neurosci. 8:263–305
Grinvald, A., Hildesheim, R., Farber, I.C., Anglister, J. 1982. Improved fluorescent probes for the measurement of rapid changes in membrane potential. Biophys. J. 39:301–308
Grinvald, A., Hildesheim, R., Gupta, R., Cohen, L.B. 1980. Better fluorescent probes for optical measurement of changes in membrane potential. Biol. Bull. 159:484
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. Membrane Biol. 58:123–137
Hirota, A., Komuro, H., Sakai, T., Momose-Sato, Y., Katoh, Y., Matsutani, K., Kamino, K. 1992. Voltage-sensitive dyes for monitoring membrane potential activity in embryonic nervous systems. Jpn. J. Physiol. 42 (Suppl.):S124
Kamino, K. 1990. Optical studies of early developing cardiac and neural activity using voltage-sensitive dyes. Jpn. J. Physiol. 40:443–461
Kamino, K. 1991. Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol. Rev. 71:53–91
Kamino, K., Hirota, A., Fujii, S. 1981. Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature 290:595–597
Kamino, K., Hirota, A., Komuro, H. 1989a. Optical indications of electrical activity and excitation-contraction coupling in the early embryonic heart. Adv. Biophys. 25:45–93
Kamino, K., Katoh, Y., Komuro, H., Sato, K. 1989b. Multiple-site optical monitoring of neural activity evoked by vagus nerve stimulation in the embryonic chick brain stem. J. Physiol. 409:263–283
Kamino, K., Komuro, H., Sakai, T., Sato, K. 1990. Optical assessment of spatially ordered patterns of neural response to vagal stimulation in the early embryonic chick brainstem. Neurosci. Res. 8:255–271
Kingston, R.H. 1978. Detection of Optical and Infrared Radiation. Springer-Verlag, New York
Komuro, H., Momose-Sato, Y., Sakai, T., Hirota, A., Kamino, K. 1993. Optical monitoring of early appearance of spontaneous membrane potential changes in the embryonic chick medulla oblongata using a voltage-sensitive dye. Neuroscience 52:55–62
Komuro, H., Sakai, T., Hirota, A., Kamino, K. 1986. Conduction pattern of excitation in the amphibian atrium assessed by multiple-site optical recording of action potentials. Jpn. J. Physiol. 36:123–137
Komuro, H., Sakai, T., Momose-Sato, Y., Hirota, A., Kamino, K. 1991. Optical detection of postsynaptic potentials evoked by vagal stimulation in the early embryonic chick brain stem slice. J. Physiol. 442:631–648
Konnerth, A., Obaid, A.L., Salzberg, B.M. 1987. Optical recording of electrical activity from parallel fibres and other cell types in skate cerebellar slices in vitro. J. Physiol. 393:681–702
Loew, L.M. 1988. How to choose a potentiometric membrane probe. In: Spectroscopic Membrane Probes, Vol. 2. L.M. Loew, editor, pp. 139–151. CRC, Boca Raton, Florida
Loew, L.M., Cohen, L.B., Dix, J., Fluhler, E.N., Montana, V., Salama, G., Wu, J-Y. 1992. A naphthyl analog of the aminostyryl pyridinum class of potentiometric membrane dyes shows consistent sensitivity in a variety of tissue, cell, and model membrane preparations. J. Membrane Biol. 130:1–10
Loew, L.M., Cohen, L.B., Salzberg, B.M., Obaid, A.L., Bezanilla, F. 1985. Charge-shift probes of membrane potential. Characterization of amino-styrylpyridinium dyes on the squid giant axon. Biophys. J. 47:71–77
Momose-Sato, Y., Sakai, T., Komuro, H., Hirota, A., Kamino, K. 1991. Optical mapping of the early development of the response pattern to vagal stimulation in embryonic chick brain stem. J. Physiol. 442:649–668
Obaid, A.L., Flores, R., Salzberg, B.M. 1989. Calcium channels that are required for secretion from intact nerve terminals of vertebrates are sensitive to ω-conotoxin and relatively insensitive to dihydropyridines. J. Gen. Physiol. 93:715–729
Obaid, A.L., Orkand, R.K., Gainer, H., Salzberg, B.M. 1985. Active calcium responses recorded optically from nerve terminals of the frog neurohypophysis. J. Gen. Physiol. 85:481–489
Parsons, T.D., Kleinfeld, D., Raccuia-Behling, F., Salzberg, B.M. 1989. Optical recording of the electrical activity of synaptically interacting Aplysia neurons in culture using potentiometric probes. Biophys. J. 56:213–221
Parsons, T.D., Salzberg, B.M., Obaid, A.L., 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
Ross, W.N., Reichardt, L.F. 1979. Species-specific effects on the optical signals of voltage-sensitive dyes. J. Membrane Biol. 48:343–356
Ross, W.N., Salzberg, B.M., Cohen, L.B., Grinvald, A., Davila, H.V., Waggoner, A.S., Wang, C.H. 1977. Changes in absorption, fluorescence, dichroism, and birefringence in stained giant axons: optical measurement of membrane potential. J. Membrane Biol. 33:141–183
Sakai, T., Hirota, A., Komuro, H., Fujii, S., Kamino, K. 1985. Optical recording of membrane potential responses from early embryonic chick ganglia using voltage-sensitive dyes. Develop. Brain Res. 17:39–51
Sakai, T., Momose-Sato, Y., Hirota, A., Sato, K., Kamino, K. 1993. Optical mapping of conduction patterns of excitation in the rat atrium using a voltage-sensitive dye. Jpn. J. Physiol. 43(Suppl. 2):S85
Salzberg, B.M. 1983. Optical recording of electrical activity in neurons using molecular probes. In: Current Methods in Cellular Neurobiology, Vol. 3, Electrophysiological Techniques. J.L. Barker and F. McKelvy, editors, pp. 139–187. John Wiley, New York
Salzberg, B.M., Davila, H.V., Cohen, L.B. 1973. Optical recording of impulses in individual neurones of an invertebrate central nervous system. Nature 246:508–509
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
Salzberg, B.M., Obaid, A.L., Senseman, D.M., Gainer, H. 1983. Optical recording of action potentials from vertebrate nerve terminals using potentiometric probes provides evidence for sodium and calcium components. Nature 306:36–40
Sato, K., Momose-Sato, Y., Sakai, T., Hirota, A., Komuro, H., Kamino, K. 1993. Optical assessment of spatial patterning of strengthduration relationship for vagal responses in the early embryonic chick brainstem. Jpn. J. Physiol. 43:521–539
Sawanobori, T., Hirota, A., Fujii, S., Kamino, K. 1981. Optical recording of conducted action potential in heart muscle using a voltagesensitive dye. Jpn. J. Physiol. 31:369–380
Senseman, D.M., Salzberg, B.M. 1980. Electrical activity in an exocrine gland: optical recording with a potentiometric dye. Science 208:1269–1271
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We thank Larry Cohen and Brian Salzberg for critical reading of the manuscript and for helpful suggestions and comments. We are grateful to Dr. Shigeo Yasui of Nippon Kankoh-Shikiso Kenkyusho for his cooperation in synthesizing new dyes. Supported in part by Grants from MESC of Japan, the Mitsubishi Foundation, the Uehara Memorial Life Science Foundation and Mochida Memorial Medical and Pharmaceutical Foundation.
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Momose-Sato, Y., Sato, K., Sakai, T. et al. Evaluation of optimal voltage-sensitive dyes for optical monitoring of embryonic neural activity. J. Membarin Biol. 144, 167–176 (1995). https://doi.org/10.1007/BF00232802
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DOI: https://doi.org/10.1007/BF00232802