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Imaging activity of neuronal populations with new long-wavelength voltage-sensitive dyes

  • Brain Cell Technology
  • Published:
Brain Cell Biology

Abstract

We have assessed the utility of five new long-wavelength fluorescent voltage-sensitive dyes (VSD) for imaging the activity of populations of neurons in mouse brain slices. Although all the five were capable of detecting activity resulting from activation of the Schaffer collateral-CA1 pyramidal cell synapse, they differed significantly in their properties, most notably in the signal-to-noise ratio of the changes in dye fluorescence associated with neuronal activity. Two of these dyes, Di-2-ANBDQPQ and Di-1-APEFEQPQ, should prove particularly useful for imaging activity in brain tissue and for combining VSD imaging with the control of neuronal activity via light-activated proteins such as channelrhodopsin-2 and halorhodopsin.

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References

  • Antic S, Major G, and Zecevic D. (1999). Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons. J. Neurophysiol. 82, 1615–1621

    PubMed  CAS  Google Scholar 

  • Antic S, Wuskell JP, Loew L, and 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

    Article  PubMed  CAS  Google Scholar 

  • Baker B, Mutoh H, Dimitrov D, Akemann W, Perron A, Iwamoto Y, Jin L, Cohen L, Isacoff E, Pieribone V, Hughes T, and Knöpfel T. (2008). Genetically encoded fluorescent sensors of membrane potential. Brain Cell Biol. 36, 53–67

    Article  PubMed  CAS  Google Scholar 

  • Berglund K, Schleich W, Krieger P, Loo L, Wang D, Cant N, Feng G, Augustine G, and Kuner T. (2006). Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon. Brain Cell Biol. 35, 207–228

    Article  PubMed  CAS  Google Scholar 

  • Canepari M, Djurisic M, and Zecevic D. (2007). Dendritic signals from rat hippocampal CA1 pyramidal neurons during coincident pre- and post-synaptic activity: a combined voltage- and calcium-imaging study. J. Physiol. 580, 463–484

    Article  PubMed  CAS  Google Scholar 

  • Chang PY, Taylor PE, and Jackson MB. (2007). Voltage imaging reveals the CA1 region at the CA2 border as a focus for epileptiform discharges and long-term potentiation in hippocampal slices. J. Neurophysiol. 98, 1309–1322

    Article  PubMed  Google Scholar 

  • Chen G, Hanson CL, Dunbar RL, and Ebner TJ. (1999). Novel form of spreading acidification and depression in the cerebellar cortex demonstrated by neutral red optical imaging. J Neurophysiol. 81, 1992–1998

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Cohen LB, Salzberg BM, and Davila HV. (1974). Changes in axon fluorescence during activity: molecular probes of membrane potential. J. Membr. Biol. 19, 1–36

    Article  PubMed  CAS  Google Scholar 

  • Cossart R, Ikegaya Y, and Yuste R. (2005) Calcium imaging of cortical networks dynamics. Cell Calcium 37, 451–457

    Article  PubMed  CAS  Google Scholar 

  • Djurisic M, Zochowski M, Wachowiak M, Falk CX, Cohen LB, and Zecevic D.(2003). Optical monitoring of neural activity using voltage-sensitive dyes. Methods Enzymology. 361, 423–451

    Article  PubMed  CAS  Google Scholar 

  • Fast VG. (2005). Simultaneous optical imaging of membrane potential and intracellular calcium. J.Electrocardiol. 38, 107–112

    Article  PubMed  Google Scholar 

  • Gao W, Dunbar RL, Chen G, Reinert KC, Oberdick J, and Ebner TJ. (2003). Optical imaging of long-term depression in the mouse cerebellar cortex in vivo. J Neurosci. 23, 1859–1866

    PubMed  CAS  Google Scholar 

  • Glover JC, Sato K, and Sato YM. (2008). Using voltage-sensitive dye recording to image the functional development of neuronal circuits in vertebrate embryos. Dev. Neurobiol. 68, 804–816

    Article  PubMed  Google Scholar 

  • Grinvald A, Manker A, and Segal M. (1982). Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J. Physiol. 333, 269–291

    PubMed  CAS  Google Scholar 

  • Gupta RK, Salzberg BM, and Grinvald A. (1981). Improvements in optical methods for measuring rapid changes in membrane potential. J. Membr. Biol. 58, 123–137

    Article  PubMed  CAS  Google Scholar 

  • Hirota A, Sato K, Momose-Sato Y, Sakai T, and Kamino K. (1995). A new simultaneous 1020-site optical recording system for monitoring neural activity using voltage-sensitive dyes. J. Neurosci. Methods. 56, 187–194

    Article  PubMed  CAS  Google Scholar 

  • Homma R, Baker BJ, Jin L, Garaschuk O, Konnerth A, Cohen LB, Bleau CX, Canepari M, Djurisic M, and Zecevic D. (2009). Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Methods Mol. Biol 489, 43–79

    Article  PubMed  CAS  Google Scholar 

  • Isomura Y, Sugimoto M, Fujiwara-Tsukamoto Y, Yamamoto-Muraki S, Yamada J, and Fukuda A. (2003). Synaptically activated Cl- accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J. Neurophysiol. 90, 2752–2756

    Article  PubMed  CAS  Google Scholar 

  • Jonas P, Bischofberger J, Fricker D, and Miles R. (2004). Interneuron diversity series: Fast in, fast out - temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci. 27, 30–40

    Article  PubMed  CAS  Google Scholar 

  • Loew LM, Campagnola P, Lewis A, Wuskell JP. (200) Confocal and nonlinear optical imaging of potentiometric dyes. Methods Cell Biol. 70, 429–452

    Article  PubMed  CAS  Google Scholar 

  • Loew LM, Cohen LB, Salzberg BM, Obaid AL, and Bezanilla F. (1985). Charge-shift probes of membrane potential. Characterization of aminostyrylpyridinium dyes on the squid giant axon. Biophys. J. 47, 71–77

    Article  PubMed  CAS  Google Scholar 

  • Loew LM, Scully S, Simpson L, Waggoner AS. (1979). Evidence for a charge-shift electrochromic mechanism in a probe of membrane potential. Nature 281, 497–499

    Article  PubMed  CAS  Google Scholar 

  • Loew LM, Simpson L. (1981) Charge shift probes of membrane potential. A probable electrochromic mechanism for ASP probes on a hemispherical lipid bilayer. Biophysical Journal 34, 353–365

    Article  PubMed  CAS  Google Scholar 

  • Maeda H, Ohno T, Sakurai M. (2007). Optical and electrophysiological recordings of corticospinal synaptic activity and its developmental change in in vitro rat slice co-cultures. Neurosci. 150, 829–840

    Article  PubMed  CAS  Google Scholar 

  • Milojkovic BA, Wuskell JP, Loew LM, and Antic SD. (2005). Initiation of sodium spikelets in basal dendrites of neocortical pyramidal neurons. J. Membr. Biol. 208, 155–169

    Article  PubMed  CAS  Google Scholar 

  • Nakamura M, Sekino Y, and Manabe T. (2007). GABAergic interneurons facilitate mossy fiber excitability in the developing hippocampus. J. Neurosci. 27, 1365–1373

    Article  PubMed  CAS  Google Scholar 

  • Nuriya M, Jiang J, Nemet B, Eisenthal KB, and Yuste R. (2006). Imaging membrane potential in dendritic spines. Proc. Natl. Acad. Sci. USA. 103, 786–790

    Article  PubMed  CAS  Google Scholar 

  • Palmer LM, and Stuart GJ. (2006). Site of action potential initiation in Layer 5 pyramidal neurons. J. Neurosci. 26, 1854–1863

    Article  PubMed  CAS  Google Scholar 

  • Reinert KC, Gao W, Chen G, and Ebner TJ. (2007). Flavoprotein autofluorescence imaging in the cerebellar cortex in vivo. J. Neurosci. 85, 3221–3232

    Article  CAS  Google Scholar 

  • Rochefort NL, Jia H, and Konnerth A. (2008). Calcium imaging in the living brain: prospects for molecular medicine. Trends Mol. Med. 14, 389–399

    Article  PubMed  CAS  Google Scholar 

  • Sekino Y, Obata K, Tanifuji M, Mizuno M, and Murayama J. (1997). Delayed signal propagation via CA2 in rat hippocampal slices revealed by optical recording. J. Neurophysiol. 78, 1662–1668

    PubMed  CAS  Google Scholar 

  • Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, and Grinvald A. (1999). Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24, 791–802

    Article  PubMed  CAS  Google Scholar 

  • Sinha SR, and Saggau P. (1999). Simultaneous optical recording of membrane potential and intracellular calcium from brain slices. Methods 18, 204–214

    Article  PubMed  CAS  Google Scholar 

  • Sjostrom PJ, Rancz EA, Roth A, and Hausser M. (2008). Dendritic excitability and synaptic plasticity. Physiol. Rev. 88, 769–840

    Article  PubMed  CAS  Google Scholar 

  • Spors H, and Grinvald A. (2002) Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301–315

    Article  PubMed  CAS  Google Scholar 

  • Tominaga T, Tominaga Y, Yamada H, Matsumoto G, and Ichikawa M. (2000). Quantification of optical signals with electrophysiological signals in neural activities of Di-4-ANEPPS stained rat hippocampal slices. J. Neurosci. Methods 102, 11–23

    Article  PubMed  CAS  Google Scholar 

  • Tominaga T, Tominaga Y, and Ichikawa M. (2002). Optical imaging of long-lasting depolarization on burst stimulation in area CA1 of rat hippocampal slices. J. Neurophysiol. 88, 1523–1532

    PubMed  Google Scholar 

  • Tsutsui H, Karasawa S, Okamura Y, and Miyawaki A. (2008). Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat. Methods 5, 683–685

    Article  PubMed  CAS  Google Scholar 

  • Wu JY, Lam YW, Falk CX, Cohen LB, Fang J, Loew L, Prechtl JC, Kleinfeld D, and Tsau Y. (1998). Voltage-sensitive dyes for monitoring multineuronal activity in the intact central nervous system. Histochem. J. 30, 169–187

    Article  PubMed  CAS  Google Scholar 

  • Wuskell JP, Boudreau D, Wei M-d, Jin L, Engl R, Chebolu R, Bullen A, Hoffacker KD, Kerimo J, Cohen LB, Zochowski MR, and Loew LM. (2006). Synthesis, spectra, delivery and potentiometric responses of new styryl dyes with extended spectral ranges. J. Neurosci. Methods 151, 200–215

    Article  PubMed  Google Scholar 

  • Zhang F, Aravanis A, Adamantidis A, de Lecea L, and Deisseroth K. (2007). Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 8, 577–581

    Article  PubMed  CAS  Google Scholar 

  • Zhou W-L, Yan P, Wuskell JP, Loew LM, and 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

    Article  PubMed  CAS  Google Scholar 

  • Zhou WL, Yan P, Wuskell JP, Loew LM, and Antic SD. (2008). Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons. Eur. J. Neurosci. 27, 923–936

    Article  PubMed  Google Scholar 

  • Zochowski M, Wachowiak M, Falk C, Cohen L, Lam Y, Antic S, and Zecevic D. (2000). Imaging membrane potential with voltage-sensitive dyes. Biol. Bull. 198, 1–21

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by funds from the Duke-NUS Graduate Medical School, and NIMH grant to G. Augustine, as well as NIH Grant EB001963 to L. Loew, and a Grant-in-Aid for Scientific Research on Priority Areas from MEXT of Japan (20021010) to Y. Sekino.

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Correspondence to Yuko Sekino.

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Kee, M.Z.L., Wuskell, J.P., Loew, L.M. et al. Imaging activity of neuronal populations with new long-wavelength voltage-sensitive dyes. Brain Cell Bio 36, 157–172 (2008). https://doi.org/10.1007/s11068-009-9039-x

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  • DOI: https://doi.org/10.1007/s11068-009-9039-x

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