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Voltage-sensitive dyes for monitoring multineuronal activity in the intact central nervous system

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Abstract

Optical monitoring of activity provides new kinds of information about brain function. Two examples are discussed in this article. First, the spike activity of many individual neurons in small ganglia can be determined. Second, the spatio-temporal characteristics of coherent activity in the brain can be directly measured. This article discusses both general characteristics of optical measurements (sources of noise) as well as more methodological aspects related to voltage-sensitive dye measurements from the nervous system. 1998 © Chapman & Hall

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References

  • Albowitz, B. & Kuhnt, U. (1993) Spread of epileptiform potentials in the neocortical slice: recordings with voltage-sensitive dyes. Brain Res. 631, 329–33.

    Google Scholar 

  • Antic, S. & Zecevic, D. (1995) Optical signals from neurons with internally applied voltage-sensitive dyes. J. Neurosci. 15, 1392–405.

    Google Scholar 

  • Ben-oren, I., Peleg, G., Lewis, A., Minke, B. & Loew, L. (1996) Infrared nonlinear optical measurements of membrane potential in photoreceptor cells. Biophys. J. 71, 1616–20.

    Google Scholar 

  • Blasdel, G.G. & Salama, G. (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321, 579–85.

    Google Scholar 

  • Bouevitch, O., Lewis, A. Pinevsky, I., Wuskell, J. & Loew, L. (1993) Probing membrane potential with nonlinear optics. Biophys. J. 65, 672–9.

    Google Scholar 

  • Boyle, M.B. & Cohen, L.B. (1980) Birefringence signals that monitor membrane potential in cell bodies of molluscan neurons. Fed. Proc. 39, 2130.

    Google Scholar 

  • Braddick, H. J. J. (1960) Photoelectric photometry. Rep. Prog. Phys. 23, 154–75.

    Google Scholar 

  • Bullen, A., Patel, S.S. & Saggau, P. (1997) High-speed, random-access fluorescence microscopy: I. High resolution optical recording with voltage-sensitive dyes and ion indicators. Biophys. J. 73, 477–91.

    Google Scholar 

  • Cash, D. & Carew, T. J. (1989) A quantitative analysis of the development of the central nervous system in juvenile Aplysia californica. J. Neurobiol. 20, 25–47.

    Google Scholar 

  • Cinelli, A.R. & Salzberg, B.M. (1992) Dendritic origin of late events in optical recordings from salamander olfactory bulb. J. Neurophysiol. 68, 786–806.

    Google Scholar 

  • Cinelli, A.R., Neff, S.R. & Kauer, J.S. (1995) Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. I. Characterization of the recording system. J. Neurophysiol. 73, 2017–32.

    Google Scholar 

  • Coggeshall, R.E. (1967) A light and electron microscope study of the abdominal ganglion of Aplysia californica. J. Neurophysiol. 30, 1263–87.

    Google Scholar 

  • Cohen, L.B. & Lesher, S. (1986) Optical monitoring of membrane potential: methods of multisite optical measurement. Soc. Gen. Physiol. Ser. 40, 71–99.

    Google Scholar 

  • Cohen, L.B. & Salzberg, B.M. (1978) Optical measurement of membrane potential Rev. Physiol. Biochem. Pharmacol. 83, 35–88.

    Google Scholar 

  • Delaney, K.R., Gelperin, A., Fee, M.S., Flores, J.A., Gervais, R., Tank, D.W. & Kleinfeld, D. (1994) Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc. Nat. Acad. Sci. USA 91, 669–73.

    Google Scholar 

  • Dainty, J.C. (1984) Laser Speckle and Related Phenomena. New York: Springer-Verlag.

    Google Scholar 

  • 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 New Biol. 241, 159–60.

    Google Scholar 

  • Denk, W. Piston, D.W. & Webb, W. (1995) Two-photon molecular excitation in laser-scanning microscopy. In Handbook of Biological Confocal Microscopy (edited by Pawley, J.W.) pp. 445–58. New York: Plenum Press.

    Google Scholar 

  • Ehrenberg, B. & Berezin, Y. (1984) Surface potential on purple membranes and its sidedness studied by resonance Raman dye probe. Biophys. J. 45, 663–70.

    Google Scholar 

  • Eilers, J., Callawaert, G., Armstrong, C. & Konnerth, A. (1995) Calcium signaling in a narrow somatic submembrane shell during synaptic activity in cerebellar Purkinje neurons. Proc. Natl. Acad. Sci. USA, 92, 10272–6.

    Google Scholar 

  • Falk, C.X., Wu JY, Cohen, L.B. & Tang, C. (1993) Non-uniform expression of habituation in the activity of distinct classes of neurons in the Aplysia abdominal ganglion. J. Neurosci. 13, 4072–81.

    Google Scholar 

  • Fromherz, P., Dambacher, K.H., Ephardt, H., Lambacher, A., Muller, 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, 1333–45.

    Google Scholar 

  • Gonzalez, J.E. & Tsien, R.Y. (1995) Voltage sensing by fluorescence energy transfer in single cells. Biophy. J. 69, 1272–80.

    Google Scholar 

  • Grinvald, A. & Farber, I.C. (1981) Optical recording of calcium action potentials from growth cones of Optical monitoring of multineuron activity 185 cultured neurons with a laser microbeam. Science 212, 1164–7.

    Google Scholar 

  • Grinvald, A., Ross, W.N. & Farber, I. (1981) Simultaneous optical measurements of electrical activity from multiple sites on processes of cultured neurons. Proc. Natl. Acad. Sci. USA 78, 3245–9.

    Google Scholar 

  • Grinvald, A., Hildesheim, R., Farber, I.C. & Anglister, L. (1982a) Improved fluorescent probes for the measurement of rapid changes in membrane potential. Biophys. J. 39, 301–8.

    Google Scholar 

  • Grinvald, A., Manker, A. & Segal, M. (1982b) Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J. Physiol. 333, 269–91.

    Google Scholar 

  • 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, 361–4.

    Google Scholar 

  • Grinvald, A., Frostig, R.D., Lieke, E. & Hildesheim, R. (1988) Optical imaging of neuronal activity. Physiol. Rev. 68, 1285–366.

    Google Scholar 

  • Grinvald, A., Lieke, E.E., Frostig, R.D. & Hildesheim, R. (1994) Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14, 2545–68.

    Google Scholar 

  • Gross, E., Bedlack, R.S. & Loew, L.M. (1994) Dual-wavelength ratiometric fluorescence measurements of the membrane dipole potential. Biophys. J. 67, 208–16.

    Google Scholar 

  • 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, 123–37.

    Google Scholar 

  • Hamer, F.M. (1964) The Cyanine Dyes and Related Compounds. New York: Wiley.

    Google Scholar 

  • Hickie, C., Wenner, P., O'Donovan, M., Tsau, Y., Fang, J. & Cohen, L.B. (1996) Optical monitoring of activity from individual and identified populations of neurons retrogradely labeled with voltage-sensitive dyes. Abs. Soc. Neurosci. 22, 321.

    Google Scholar 

  • Hirota, A., Sato, K., Momose-sato, Y., Sakai, T. & Kamino, K. (1995) A new simultaneous 1020-site optical recording system for monitoring neural activity using voltage-sensitive dyes. J. Neurosci. Methods 56, 187–94.

    Google Scholar 

  • Ichikawa, M., Iijima, T. & Matsumoto, G. (1992) Simultaneous 16,384-site Optical Recording of Neural Activities in the Brain. New York: Oxford University Press.

    Google Scholar 

  • Iijima, T., Ichikawa, M. & Matsumoto, G. (1989) Optical monitoring of LTP and related phenomena. Abstracts Soc. Neurosci. 15, 398.

    Google Scholar 

  • Iijima, T., Ichikawa, M. & Matsumoto, G. (1992) Synaptic activation of rat adrenal medulla examined with a large photodiode array in combination with a voltage-sensitive dye. Neuroscience 51, 211–19.

    Google Scholar 

  • Kauer, J.S. (1988) Real-time imaging of evoked activity in local circuits of the salamander olfactory bulb. Nature 331, 166–8.

    Google Scholar 

  • Kazan, B. & Knoll, M. (1968) Electronic Image Storage. New York: Academic Press.

    Google Scholar 

  • 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.

    Google Scholar 

  • Kupfermann, I., Pinsker, H., Castellucci, V. & Kandel, E.R. (1971) Central and peripheral control of gill movements in Aplysia. Science 174, 1252–6.

    Google Scholar 

  • Lasser-ross, N., Miyakawa, H., Lev-ram, V., Young, S.R. & Ross, W.N. (1991) High time resolution fluorescence imaging with a CCD camera. J. Neurosci. Methods 36, 253–61.

    Google Scholar 

  • Loew, L.M. (1993) Confocal microscopy of potentiometric fluorescent dyes. Methods Cell Biol. 38, 195–209.

    Google Scholar 

  • 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, 71–7.

    Google Scholar 

  • London, J.A., Zecevic, D. & Cohen, L.B. (1987) Simultaneous optical recording of activity from many neurons during feeding in Navanax. J. Neurosci. 7, 649–61.

    Google Scholar 

  • Malmstadt, H.V., Enke, C.G., Crouch, S.R. & Harlick, G. (1974) Electronic Measurements for Scientists. Menlo Park, CA: Benjamin.

    Google Scholar 

  • Momose-sato, Y., Sato, K., Sakai, T., Hirota, A., Matsutani, K. & Kamino, K. (1995) Evaluation of optimal voltage-sensitive dyes for optical measurement of embryonic neural activity. J. Membr. Biol. 144, 167–76.

    Google Scholar 

  • Morton, D.W., Chiel, H.J., Cohen, L.B. & Wu, J.Y. (1991) Optical methods can be utilized to map the location and activity of putative motor neurons and interneurons during rhythmic patterns of activity in the buccal ganglion of Aplysia. Brain Res. 564, 45–55.

    Google Scholar 

  • Nakashima, M., Yamada, S., Shiono, S., Maeda, M. & Sato, F. (1992) 448-detector optical recording system: development and application to Aplysia gill-withdrawal reflex. IEEE Trans. Biomed. Eng. 39, 26–36.

    Google Scholar 

  • Nirenberg, S. & Cepko, C. (1993) Targeted ablation of diverse cell classes in the nervous system in vivo. J. Neurosci. 13, 3238–51.

    Google Scholar 

  • Orbach, H.S & Cohen, L.B. (1983) Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system. J. Neurosci. 3, 2251–62.

    Google Scholar 

  • Orbach, H. S., Cohen, L.B. & Grinvald, A. (1985) Optical mapping of electrical activity in rat somatosensory and visual cortex. J. Neurosci. 5, 1886–895.

    Google Scholar 

  • Petran, M. & Hadravsky, M. (1966) Czechoslovakian patent 7720.

  • Poe, G.R., Rector, D.M. & Harper, R.M. (1994) Hippocampal refected optical patterns during sleep and waking states in the freely behaving cat. J. Neurosci. 14, 2933–42.

    Google Scholar 

  • Prechtl, J.C. (1994) Visual motion induces synchronous oscillations in turtle visual cortex. Proc. Natl. Acad. Sci. USA 91, 12467–71.

    Google Scholar 

  • Prechtl, J.C., Cohen, L.B., Peseran, B., Mitra, P.P. & Kleinfeld, D. (1997) Visual stimuli induce waves of electrical activity in turtle cortex. Proc. Natl. Acad. Sci. USA 94, 7621–26.

    Google Scholar 

  • Ratzlaff, E.H. & Grinvald, A. (1991) A tandem-lens epifluorescence microscope: hundred-fold brightness advantage for wide-field imaging. J. Neurosci. Methods 36, 127–37.

    Google Scholar 

  • Ross, W.N. & Reichardt, L.F. (1979) Species-specific effects on the optical signals of voltage-sensitive dyes. J. Membr. Biol. 48, 343–56.

    Google Scholar 

  • 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, 983–6.

    Google Scholar 

  • Sakai, T., Hirota, A., Komuro, H., Fuj ii, S. & Kamino, K. (1985) Optical recording of membrane potential responses from early embryonic chick ganglia using voltage-sensitive dyes. Brain Res. 349, 39–51.

    Google Scholar 

  • Salama, G. (1988) Voltage-sensitive dyes and imaging techniques reveal new patterns of electrical activity in heart and cortex. SPIE Proc. 94, 75–86.

    Google Scholar 

  • Salzberg, B.M. (1983) Optical recording of electrical activity in neurons using molecular probes. In Current Methods in Cellular Neurobiology (edited by Barker, J.L. and Mckelvy, J.F.) pp. 139–87. New York: Wiley.

    Google Scholar 

  • Salzberg, B.M., Davila, H.V. & Cohen, L.B. (1973) Optical recording of impulses in individual neurons of an invertebrate central nervous system. Nature 246, 508–9.

    Google Scholar 

  • 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, 1281–91.

    Google Scholar 

  • Sharnoff, M., Henry, R.W. & Belleza, D.M.J. (1978a) Holographic visualization of the nerve impulse. Biophys. J. 21, 109A.

    Google Scholar 

  • Sharnoff, M., Romer, N. J., Cohen, L.B., Salzberg, B.M., Boyle, M.B. & Lesher, S. (1978b) Differential holography of squid giant axons during excitation and rest (abstract). Biol. Bull. 155, 465–6.

    Google Scholar 

  • Shaw, R. (1979) Photographic detectors. Appl. Optics Optical Eng. 7, 121–54.

    Google Scholar 

  • Sherebrin, M.H. (1972) Changes in infrared spectrum of nerve during excitation. Nature 235, 122–4.

    Google Scholar 

  • Sherebrin, M.H., Macclement, B.A.E. & Franko, A.J. (1972) Electric-field induced shifts in the infrared spectrum of conducting nerve axons. Biophys. J. 12, 977–89.

    Google Scholar 

  • Shrager, P., Chiu, S.Y., Ritchie, J.M., Zecevic, D. & Cohen, L.B. (1987) Optical measurement of propagation in normal and demyelinated frog nerve. Biophys. J. 51, 351–5.

    Google Scholar 

  • Siegel, M.S. & Isacoff, E.Y. (1997) A genetically encoded optical probe of membrane voltage. Neuron 19, 735–41.

    Google Scholar 

  • Tank, D. & Ahmed, Z. (1985) Multiple-site monitoring of activity in cultured neurons. Biophys. J. 47, 476A.

    Google Scholar 

  • Tsau, Y., Wu, J.Y., Hopp, H.P., Cohen, L.B., Schiminovich, D. & Falk, C.X. (1994) Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis. J. Neurosci. 14, 4167–84.

    Google Scholar 

  • 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 voltage-sensitive dyes. J. Neurosci. Methods 70, 121–9.

    Google Scholar 

  • Waggoner, A.S. (1979) Dye indicators of membrane potential. Annu. Rev. Biophys. Bioeng. 8, 47–68.

    Google Scholar 

  • Waggoner, A.S. & Grinvald, A. (1977) Mechanisms of rapid optical changes of potential sensitive dyes. Ann. NY. Acad. Sci. 303, 217–41.

    Google Scholar 

  • Wenner, P., Tsau, Y., Cohen, L.B., O'Donovan, M.J. & Dan, Y. (1996) Voltage sensitive dye recording using retrogradely transported dye in the chicken spinal cord: staining and signal characteristics. J. Neurosci. Methods 70, 111–20.

    Google Scholar 

  • Wu, J.Y. & Cohen, L.B. (1993) Fast multisite optical measurements of membrane potential. In Fluorescent and Luminescent Probes for Biological Activity (edited by Mason, W.T.), p. 389–404. London: Academic Press.

    Google Scholar 

  • Wu, J.Y., Cohen, L.B. & Falk, C.X. (1994a) Neuronal activity during different behaviours suggests a distributed neuronal organization in the Aplysia abdominal ganglion. Science 263, 820–3.

    Google Scholar 

  • Wu, J.Y., Tsau, T., Hopp, H.P., Cohen, L.B., Tang, A.C. & Falk, C.X. (1994b) Consistency in nervous systems: trial-to-trial and animal-to-animal variations in the response to repeated application of a sensory stimulus in Aplysia. J. Neurosci. 14, 1366–84.

    Google Scholar 

  • Yuste, R. & Denk, W. (1995) Dendritic spines as basic functional units of neuronal integration. Nature 375, 682–4.

    Google Scholar 

  • Zecevic, D., Wu, J.Y., Cohen, L.B., London, J.A., Hopp, H.P. & Falk, C.X. (1989) Hundreds of neurons in the Aplysia abdominal ganglion are active during the gill-withdrawal reflex. J. Neurosci. 9, 3681–9.

    Google Scholar 

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Wu, JY., Lam, YW., Falk, C.X. et al. Voltage-sensitive dyes for monitoring multineuronal activity in the intact central nervous system. Histochem J 30, 169–187 (1998). https://doi.org/10.1023/A:1003295319615

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