Abstract

We describe an optical technique for label-free detection of the action potential in cultured mammalian neurons. Induced morphological changes due to action potential propagation in neurons are optically interrogated with a phase sensitive interferometric technique. Optical recordings composed of signal pulses mirror the electrical spike train activity of individual neurons in a network. The optical pulses are transient nanoscale oscillatory changes in the optical path length of varying peak magnitude and temporal width. Exogenous application of glutamate to cortical neuronal cultures produced coincident increase in the electrical and optical activity; both were blocked by application of a Na-channel blocker, Tetrodotoxin. The observed transient change in optical path length in a single optical pulse is primarily due to physical fluctuations of the neuronal cell membrane mediated by a yet unknown electromechanical transduction phenomenon. Our analysis suggests a traveling surface wave in the neuronal cell membrane is responsible for the measured optical signal pulses.

© 2017 Optical Society of America

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Corrections

25 July 2017: A typographical correction was made to author listing.

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2017 (1)

2016 (4)

E. Sassaroli and N. Vykhodtseva, “Acoustic neuromodulation from a basic science prospective,” J. Ther. Ultrasound 4(1), 17 (2016).
[Crossref] [PubMed]

R. Budvytyte, A. Gonzalez-Perezl, L. D. Mosgaard, E. Villagran-Vargas, A. D. Jackson, and T. Heimburg, “Solitary electromechanical pulses in lobster neurons,” Biophys. J. 110(3), 150a (2016).
[Crossref]

S. Inagaki and T. Nagai, “Current progress in genetically encoded voltage indicators for neural activity recording,” Curr. Opin. Chem. Biol. 33, 95–100 (2016).
[Crossref] [PubMed]

A. H. Badreddine, T. Jordan, and I. J. Bigio, “Real-time imaging of action potentials in nerves using changes in birefringence,” Biomed. Opt. Express 7(5), 1966–1973 (2016).
[Crossref] [PubMed]

2015 (4)

S. Berlin, E. C. Carroll, Z. L. Newman, H. O. Okada, C. M. Quinn, B. Kallman, N. C. Rockwell, S. S. Martin, J. C. Lagarias, and E. Y. Isacoff, “Photoactivatable genetically encoded calcium indicators for targeted neuronal imaging,” Nat. Methods 12(9), 852–858 (2015).
[Crossref] [PubMed]

F. St-Pierre, M. Chavarha, and M. Z. Lin, “Designs and sensing mechanisms of genetically encoded fluorescent voltage indicators,” Curr. Opin. Chem. Biol. 27, 31–38 (2015).
[Crossref] [PubMed]

A. El Hady and B. B. Machta, “Mechanical surface waves accompany action potential propagation,” Nat. Commun. 6, 6697 (2015).
[Crossref] [PubMed]

Y. J. Yeh, A. J. Black, D. Landowne, and T. Akkin, “Optical coherence tomography for cross-sectional imaging of neural activity,” Neurophotonics 2(3), 035001 (2015).
[Crossref] [PubMed]

2014 (3)

S. Shrivastava and M. F. Schneider, “Evidence for two-dimensional solitary sound waves in a lipid controlled interface and its implications for biological signalling,” J. R. Soc. Interface 11(97), 20140098 (2014).
[Crossref] [PubMed]

D. R. Hochbaum, Y. Zhao, S. L. Farhi, N. Klapoetke, C. A. Werley, V. Kapoor, P. Zou, J. M. Kralj, D. Maclaurin, N. Smedemark-Margulies, J. L. Saulnier, G. L. Boulting, C. Straub, Y. K. Cho, M. Melkonian, G. K. S. Wong, D. J. Harrison, V. N. Murthy, B. L. Sabatini, E. S. Boyden, R. E. Campbell, and A. E. Cohen, “All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins,” Nat. Methods 11(8), 825–833 (2014).
[Crossref] [PubMed]

J. K. Mueller and W. J. Tyler, “A quantitative overview of biophysical forces impinging on neural function,” Phys. Biol. 11(5), 051001 (2014).
[Crossref] [PubMed]

2013 (2)

M. E. Spira and A. Hai, “Multi-electrode array technologies for neuroscience and cardiology,” Nat. Nanotechnol. 8(2), 83–94 (2013).
[Crossref] [PubMed]

G. Cao, J. Platisa, V. A. Pieribone, D. Raccuglia, M. Kunst, and M. N. Nitabach, “Genetically targeted optical electrophysiology in intact neural circuits,” Cell 154(4), 904–913 (2013).
[Crossref] [PubMed]

2012 (6)

C. Grienberger and A. Konnerth, “Imaging calcium in neurons,” Neuron 73(5), 862–885 (2012).
[Crossref] [PubMed]

L. Tian, S. A. Hires, and L. L. Looger, “Imaging neuronal activity with genetically encoded calcium indicators,” Cold Spring Harb. Protoc. 2012(6), 647–656 (2012).
[Crossref] [PubMed]

S. Reichinnek, A. von Kameke, A. M. Hagenston, E. Freitag, F. C. Roth, H. Bading, M. T. Hasan, A. Draguhn, and M. Both, “Reliable optical detection of coherent neuronal activity in fast oscillating networks in vitro,” Neuroimage 60(1), 139–152 (2012).
[Crossref] [PubMed]

L. Jin, Z. Han, J. Platisa, J. R. A. Wooltorton, L. B. Cohen, and V. A. Pieribone, “Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe,” Neuron 75(5), 779–785 (2012).
[Crossref] [PubMed]

J. Griesbauer, S. Bössinger, A. Wixforth, and M. F. Schneider, “Propagation of 2d pressure pulses in lipid monolayers and its possible implications for biology,” Phys. Rev. Lett. 108(19), 198103 (2012).
[Crossref] [PubMed]

S. Oh, C. Fang-Yen, W. Choi, Z. Yaqoob, D. Fu, Y. Park, R. R. Dassari, and M. S. Feld, “Label-free imaging of membrane potential using membrane electromotility,” Biophys. J. 103(1), 11–18 (2012).
[Crossref] [PubMed]

2011 (2)

D. S. Peterka, H. Takahashi, and R. Yuste, “Imaging voltage in neurons,” Neuron 69(1), 9–21 (2011).
[Crossref] [PubMed]

J. M. Kralj, A. D. Douglass, D. R. Hochbaum, D. Maclaurin, and A. E. Cohen, “Optical recording of action potentials in mammalian neurons using a microbial rhodopsin,” Nat. Methods 9(1), 90–95 (2011).
[Crossref] [PubMed]

2009 (6)

B. W. Graf, T. S. Ralston, H. J. Ko, and S. A. Boppart, “Detecting intrinsic scattering changes correlated to neuron action potentials using optical coherence imaging,” Opt. Express 17(16), 13447–13457 (2009).
[Crossref] [PubMed]

J. Bradley, R. Luo, T. S. Otis, and D. A. DiGregorio, “Submillisecond optical reporting of membrane potential in situ using a neuronal tracer dye,” J. Neurosci. 29(29), 9197–9209 (2009).
[Crossref] [PubMed]

M. Scanziani and M. Häusser, “Electrophysiology in the age of light,” Nature 461(7266), 930–939 (2009).
[Crossref] [PubMed]

D. S. Bassett and E. T. Bullmore, “Human brain networks in health and disease,” Curr. Opin. Neurol. 22(4), 340–347 (2009).
[Crossref] [PubMed]

T. Akkin, D. Landowne, and A. Sivaprakasam, “Optical coherence tomography phase measurement of transient changes in squid giant axons during activity,” J. Membr. Biol. 231(1), 35–46 (2009).
[Crossref] [PubMed]

S. S. L. Andersen, A. D. Jackson, and T. Heimburg, “Towards a thermodynamic theory of nerve pulse propagation,” Prog. Neurobiol. 88(2), 104–113 (2009).
[Crossref] [PubMed]

2008 (2)

J. Dunlop, M. Bowlby, R. Peri, D. Vasilyev, and R. Arias, “High-throughput electrophysiology: An emerging paradigm for ion-channel screening and physiology,” Nat. Rev. Drug Discov. 7(4), 358–368 (2008).
[Crossref] [PubMed]

J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
[Crossref] [PubMed]

2007 (5)

T. Heimburg and A. D. Jackson, “On the action potential as a propagating density pulse and the role of anesthetics,” Biophys. Rev. Lett. 2(01), 57–78 (2007).
[Crossref]

T. Akkin, C. Joo, and J. F. de Boer, “Depth-resolved measurement of transient structural changes during action potential propagation,” Biophys. J. 93(4), 1347–1353 (2007).
[Crossref] [PubMed]

G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[Crossref] [PubMed]

A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145(3), 887–899 (2007).
[Crossref] [PubMed]

C. Fang-Yen and M. S. Feld, “Intrinsic optical signals in neural tissues: Measurements, mechanisms, and applications,” Acs Sym. Ser. 963, 219–235 (2007).
[Crossref]

2005 (6)

M. A. Choma, A. K. Ellerbee, C. Yang, T. L. Creazzo, and J. A. Izatt, “Spectral-domain phase microscopy,” Opt. Lett. 30(10), 1162–1164 (2005).
[Crossref] [PubMed]

C. Joo, T. Akkin, B. Cense, B. H. Park, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging,” Opt. Lett. 30(16), 2131–2133 (2005).
[Crossref] [PubMed]

E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
[Crossref] [PubMed]

X. Li, W. Zhou, M. Liu, and Q. Luo, “Synchronized spontaneous spikes on multi-electrode array show development of cultured neuronal network,” Conf. Proc. IEEE Eng. Med. Biol. Soc. 2, 2134–2137 (2005).
[PubMed]

R. Q. Quiroga, L. Reddy, G. Kreiman, C. Koch, and I. Fried, “Invariant visual representation by single neurons in the human brain,” Nature 435(7045), 1102–1107 (2005).
[Crossref] [PubMed]

A. K. Engel, C. K. E. Moll, I. Fried, and G. A. Ojemann, “Invasive recordings from the human brain: Clinical insights and beyond,” Nat. Rev. Neurosci. 6(1), 35–47 (2005).
[Crossref] [PubMed]

2004 (3)

2003 (3)

C. Wolff, B. Fuks, and P. Chatelain, “Comparative study of membrane potential-sensitive fluorescent probes and their use in ion channel screening assays,” J. Biomol. Screen. 8(5), 533–543 (2003).
[Crossref] [PubMed]

C. Lossin, T. H. Rhodes, R. R. Desai, C. G. Vanoye, D. Wang, S. Carniciu, O. Devinsky, and A. L. George., “Epilepsy-associated dysfunction in the voltage-gated neuronal sodium channel scn1a,” J. Neurosci. 23(36), 11289–11295 (2003).
[PubMed]

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1990 (1)

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1980 (2)

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1978 (1)

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1973 (1)

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1970 (1)

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I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophys. J. 57(3), 633–635 (1990).
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L. Jin, Z. Han, J. Platisa, J. R. A. Wooltorton, L. B. Cohen, and V. A. Pieribone, “Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe,” Neuron 75(5), 779–785 (2012).
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D. Gross, W. S. Williams, and J. A. Connor, “Theory of electromechanical effects in nerve,” Cell. Mol. Neurobiol. 3(2), 89–111 (1983).
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Dassari, R. R.

S. Oh, C. Fang-Yen, W. Choi, Z. Yaqoob, D. Fu, Y. Park, R. R. Dassari, and M. S. Feld, “Label-free imaging of membrane potential using membrane electromotility,” Biophys. J. 103(1), 11–18 (2012).
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T. Akkin, C. Joo, and J. F. de Boer, “Depth-resolved measurement of transient structural changes during action potential propagation,” Biophys. J. 93(4), 1347–1353 (2007).
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E. S. Boyden, F. Zhang, E. Bamberg, G. Nagel, and K. Deisseroth, “Millisecond-timescale, genetically targeted optical control of neural activity,” Nat. Neurosci. 8(9), 1263–1268 (2005).
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C. Lossin, T. H. Rhodes, R. R. Desai, C. G. Vanoye, D. Wang, S. Carniciu, O. Devinsky, and A. L. George., “Epilepsy-associated dysfunction in the voltage-gated neuronal sodium channel scn1a,” J. Neurosci. 23(36), 11289–11295 (2003).
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C. Lossin, T. H. Rhodes, R. R. Desai, C. G. Vanoye, D. Wang, S. Carniciu, O. Devinsky, and A. L. George., “Epilepsy-associated dysfunction in the voltage-gated neuronal sodium channel scn1a,” J. Neurosci. 23(36), 11289–11295 (2003).
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J. Bradley, R. Luo, T. S. Otis, and D. A. DiGregorio, “Submillisecond optical reporting of membrane potential in situ using a neuronal tracer dye,” J. Neurosci. 29(29), 9197–9209 (2009).
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J. M. Kralj, A. D. Douglass, D. R. Hochbaum, D. Maclaurin, and A. E. Cohen, “Optical recording of action potentials in mammalian neurons using a microbial rhodopsin,” Nat. Methods 9(1), 90–95 (2011).
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S. Reichinnek, A. von Kameke, A. M. Hagenston, E. Freitag, F. C. Roth, H. Bading, M. T. Hasan, A. Draguhn, and M. Both, “Reliable optical detection of coherent neuronal activity in fast oscillating networks in vitro,” Neuroimage 60(1), 139–152 (2012).
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J. Dunlop, M. Bowlby, R. Peri, D. Vasilyev, and R. Arias, “High-throughput electrophysiology: An emerging paradigm for ion-channel screening and physiology,” Nat. Rev. Drug Discov. 7(4), 358–368 (2008).
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S. Oh, C. Fang-Yen, W. Choi, Z. Yaqoob, D. Fu, Y. Park, R. R. Dassari, and M. S. Feld, “Label-free imaging of membrane potential using membrane electromotility,” Biophys. J. 103(1), 11–18 (2012).
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S. Oh, C. Fang-Yen, W. Choi, Z. Yaqoob, D. Fu, Y. Park, R. R. Dassari, and M. S. Feld, “Label-free imaging of membrane potential using membrane electromotility,” Biophys. J. 103(1), 11–18 (2012).
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S. Reichinnek, A. von Kameke, A. M. Hagenston, E. Freitag, F. C. Roth, H. Bading, M. T. Hasan, A. Draguhn, and M. Both, “Reliable optical detection of coherent neuronal activity in fast oscillating networks in vitro,” Neuroimage 60(1), 139–152 (2012).
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Figures (6)

Fig. 1
Fig. 1

Optical setup for detecting neuronal activity using low coherence phase sensitive interferometry. (A) Schematic diagram of the interferometric instrument which consists of a broadband source (center wavelength at 860nm, bandwidth of 63 nm), fiber coupler, high-speed spectrometer, and computer with data acquisition system. (B) Output port of the fiber coupler is attached to the side port of an inverted microscope that transmits and focusses light on the s (C) Illustration of neuronal cell culture device in a sandwich configuration consisting of two glass slides that are separated by a fixed gap (~80 μm) with neurons attached to the bottom glass slide, and (D) Light reflecting from the bottom (glass-cell) and the top (cell-media) interfaces of the two glass slides of the neuronal cell culture device couple back into the interferometer and mix to form spectral interference fringe signal.

Fig. 2
Fig. 2

Representative optical signals recorded from individual neurons in a network. (A) Fluorescence immuno-stained (primary β-III-tubulin antibody- Alexa Fluor 488) image of networked rat cortical neurons used in our experiments. (B) & (C) Temporal change in OPD under different experimental conditions (no cell, cell without any stimulation, cell with Glutamate stimulation, cell with TTX inhibition) showing a non-periodic train of optical signal oscillation from unstimulated and stimulated neurons which die out when inhibited with TTX. Calculated OPD sensitivity (standard deviation of optical trace in (Fig. 2(B))) was 30 pm. (D) Isolated burst of individual optical pulses that have wave packet like signal pulse characteristics and their corresponding envelopes show variation in temporal pulse width.

Fig. 3
Fig. 3

Patch clamp recording of action potential firing from single neurons. (A) Pre-and post-glutamate stimulation voltage recording (current clamp) of randomly generated action potential spikes in networked neurons. (B) Inhibition of electrical activity with addition of TTX. Recordings in (A) and (B) are from two separate experiments.

Fig. 4
Fig. 4

Analysis of extracted features from individual optical pulse (Fig. 2) (N = 5 neurons). (A) Optical signals are rectified, followed by envelope detection of each pulse. (B) Firing rate of unstimulated vs stimulated/inhibited neurons, (p<0.05 for -Glu vs + Glu and -Glu vs + TTX). (C)-(D) scatter plots of envelope width, envelope peak under no stimulation, Glutamate stimulation, and TTX inhibition conditions, respectively.

Fig. 5
Fig. 5

(A) Illustration of plausible mechanistic origin of optical signal pulse (right panel) due to transient oscillation of neural cell membrane (middle panel) which is triggered by propagating action potential (B) Time-frequency analysis (continuous wavelet transform) of optical pulse train, and (C) Frequency characterization of membrane oscillation from individual optical pulse.

Fig. 6
Fig. 6

Optical pulses of varying temporal characteristics (A) Raw (blue) and filtered (low pass-orange) 60 sec extract of optical recording from a signal neuron showing a train of randomly spaced optical pulse. (i-iv) Zoomed section of select windows from optical recordings (A) showing single or multicyclic oscillation of the detected optical pulses. The temporal variation of the selected oscillatory pulses is evident (scale-bar = 50 ms).

Equations (3)

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S o ( k , t ) = α S i ( k ) { R 1 + R 2 + 2 R 1   R 2   | μ ( k ) | cos [ ϕ ( k , t ) ] }
ϕ ( z , t ) | z = d = 4 π λ c p ( z , t ) = tan 1 { I m   S 0 ( z , t ) R e   S 0 ( z , t ) }
Δ p ( d , t n ) = λ c 4 π Δ ϕ ( d , t n ) = λ c 4 π [ ϕ ( d , t n ) ϕ ( d , t 0 ) ]

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