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J Neurophysiol (January 2, 2008). doi:10.1152/jn.00929.2007
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Submitted on August 17, 2007
Accepted on January 2, 2008

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

Jonathan A. N. Fisher1, Jonathan R. Barchi2, Cristin G. Welle3, Gi-Ho Kim4, Paul Kosterin5, Ana Lia Obaid6, Arjun G. Yodh7, Diego Contreras3, and Brian M. Salzberg3*

1 Physics and Astronomy, University of Pennsylvania School of Arts and Sciences, Philadelphia, Pennsylvania, United States
2 Bioengineering, University of Pennsylvania School of Engineering and Applied Science, Philadelphia, Pennsylvania, United States
3 Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States
4 Neuroscience, Philadelphia, Pennsylvania, United States; Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States
5 Philadelphia, Pennsylvania, United States; Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States; Neuroscience, Philadelphia, Pennsylvania, United States
6 University of Pennsylvania School of Medicine; Neuroscience, Philadelphia, Pennsylvania, United States
7 Physics and Astronomy, University of Pennsylvania School of Arts and Sciences, Philadelphia, Pennsylvania, United States; Philadelphia, Pennsylvania, United States

* To whom correspondence should be addressed. E-mail: bmsalzbe{at}mail.med.upenn.edu.

We report the first optical recordings of action potentials, in single trials, from one or a few (~1-2 μm) mammalian nerve terminals in an intact in vitro preparation, the mouse neurohypophysis. The measurements utilized two-photon excitation along the "blue" edge of the two-photon absorption spectrum of di-3-ANEPPDHQ (a fluorescent voltage-sensitive naphthylstyryl-pyridinium dye), and epifluorescence detection, a configuration that is critical for non-invasive recording of electrical activity from intact brains. Single-trial recordings of action potentials exhibited signal-to-noise ratios of ~5:1 and fractional fluorescence changes of up to ~10%. This method, by virtue of its optical sectioning capability, deep tissue penetration, and efficient epifluorescence detection, offers clear advantages over linear, as well as other non-linear optical techniques used to monitor voltage changes in localized neuronal regions, and provides an alternative to invasive electrode arrays for studying neuronal systems in vivo.




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