Optical Stimulation Enables Paced Electrophysiological Studies in Embryonic Hearts

Overview

Journal Biomed Opt Express

Specialty Radiology

Date 2014 Apr 25

PMID 24761284

Citations 14

Authors

Yves T Wang

Shi Gu

Pei Ma

Michiko Watanabe

Andrew M Rollins

Michael W Jenkins

Affiliations

Soon will be listed here.

Abstract

Cardiac electrophysiology plays a critical role in the development and function of the heart. Studies of early embryonic electrical activity have lacked a viable point stimulation technique to pace in vitro samples. Here, optical pacing by high-precision infrared stimulation is used to pace excised embryonic hearts, allowing electrophysiological parameters to be quantified during pacing at varying rates with optical mapping. Combined optical pacing and optical mapping enables electrophysiological studies in embryos under more physiological conditions and at varying heart rates, allowing detection of abnormal conduction and comparisons between normal and pathological electrical activity during development in various models.

Citing Articles

Prenatal ethanol exposure impairs the conduction delay at the atrioventricular junction in the looping heart.

Ling S, Jenkins M, Watanabe M, Ford S, Rollins A Am J Physiol Heart Circ Physiol. 2021; 321(2):H294-H305.

PMID: 34142884 PMC: 8526336. DOI: 10.1152/ajpheart.00107.2021.

Fiberoptic array for multiple channel infrared neural stimulation of the brain.

Chernov M, Friedman R, Roe A Neurophotonics. 2021; 8(2):025005.

PMID: 33898637 PMC: 8062107. DOI: 10.1117/1.NPh.8.2.025005.

Optical Electrophysiology in the Developing Heart.

Thomas K, Goudy J, Henley T, Bressan M J Cardiovasc Dev Dis. 2018; 5(2).

PMID: 29751595 PMC: 6023508. DOI: 10.3390/jcdd5020028.

Probing the Electrophysiology of the Developing Heart.

Watanabe M, Rollins A, Polo-Parada L, Ma P, Gu S, Jenkins M J Cardiovasc Dev Dis. 2018; 3(1).

PMID: 29367561 PMC: 5715694. DOI: 10.3390/jcdd3010010.

An infrared optical pacing system for screening cardiac electrophysiology in human cardiomyocytes.

McPheeters M, Wang Y, Werdich A, Jenkins M, Laurita K PLoS One. 2017; 12(8):e0183761.

PMID: 28837652 PMC: 5570338. DOI: 10.1371/journal.pone.0183761.

References

Bruegmann T, Malan D, Hesse M, Beiert T, Fuegemann C, Fleischmann B . Optogenetic control of heart muscle in vitro and in vivo. Nat Methods. 2010; 7(11):897-900. DOI: 10.1038/nmeth.1512. View

Hamburger V, HAMILTON H . A series of normal stages in the development of the chick embryo. J Morphol. 2014; 88(1):49-92. View

Levy S, Pouget B, Clementy J, Bemurat M, BRICAUD H . Pacing-induced alternate Wenckebach periods: incidence and clinical significance. Pacing Clin Electrophysiol. 1979; 2(6):614-23. DOI: 10.1111/j.1540-8159.1979.tb04281.x. View

Wells J, Kao C, Konrad P, Milner T, Kim J, Mahadevan-Jansen A . Biophysical mechanisms of transient optical stimulation of peripheral nerve. Biophys J. 2007; 93(7):2567-80. PMC: 1965456. DOI: 10.1529/biophysj.107.104786. View

Rajguru S, Richter C, Matic A, Holstein G, Highstein S, Dittami G . Infrared photostimulation of the crista ampullaris. J Physiol. 2011; 589(Pt 6):1283-94. PMC: 3082092. DOI: 10.1113/jphysiol.2010.198333. View

Boyden E, Zhang F, Bamberg E, Nagel G, Deisseroth K . Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005; 8(9):1263-8. DOI: 10.1038/nn1525. View

Sedmera D, Reckova M, Rosengarten C, Torres M, Gourdie R, Thompson R . Optical mapping of electrical activation in the developing heart. Microsc Microanal. 2005; 11(3):209-15. DOI: 10.1017/S1431927605050452. View

Izzo A, Walsh Jr J, Ralph H, Webb J, Bendett M, Wells J . Laser stimulation of auditory neurons: effect of shorter pulse duration and penetration depth. Biophys J. 2008; 94(8):3159-66. PMC: 2275688. DOI: 10.1529/biophysj.107.117150. View

Kou L, Labrie D, Chylek P . Refractive indices of water and ice in the 0.65- to 2.5-µm spectral range. Appl Opt. 2010; 32(19):3531-40. DOI: 10.1364/AO.32.003531. View

10.

Weidmann S . Electrical constants of trabecular muscle from mammalian heart. J Physiol. 1970; 210(4):1041-54. PMC: 1395623. DOI: 10.1113/jphysiol.1970.sp009256. View

11.

Cayce J, Friedman R, Chen G, Jansen E, Mahadevan-Jansen A, Roe A . Infrared neural stimulation of primary visual cortex in non-human primates. Neuroimage. 2013; 84:181-90. PMC: 4120263. DOI: 10.1016/j.neuroimage.2013.08.040. View

12.

Radisic M, Park H, Shing H, Consi T, Schoen F, Langer R . Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A. 2004; 101(52):18129-34. PMC: 539727. DOI: 10.1073/pnas.0407817101. View

13.

Wells J, Kao C, Jansen E, Konrad P, Mahadevan-Jansen A . Application of infrared light for in vivo neural stimulation. J Biomed Opt. 2006; 10(6):064003. DOI: 10.1117/1.2121772. View

14.

Matic A, Robinson A, Young H, Badofsky B, Rajguru S, Stock S . Behavioral and electrophysiological responses evoked by chronic infrared neural stimulation of the cochlea. PLoS One. 2013; 8(3):e58189. PMC: 3591411. DOI: 10.1371/journal.pone.0058189. View

15.

Akar F, Roth B, Rosenbaum D . Optical measurement of cell-to-cell coupling in intact heart using subthreshold electrical stimulation. Am J Physiol Heart Circ Physiol. 2001; 281(2):H533-42. DOI: 10.1152/ajpheart.2001.281.2.H533. View

16.

Weidmann S . The electrical constants of Purkinje fibres. J Physiol. 1952; 118(3):348-60. PMC: 1392495. DOI: 10.1113/jphysiol.1952.sp004799. View

17.

Peterson E, Tyler D . Motor neuron activation in peripheral nerves using infrared neural stimulation. J Neural Eng. 2013; 11(1):016001. PMC: 3952042. DOI: 10.1088/1741-2560/11/1/016001. View

18.

Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P . Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A. 2003; 100(24):13940-5. PMC: 283525. DOI: 10.1073/pnas.1936192100. View

19.

Efimov I, Nikolski V, Salama G . Optical imaging of the heart. Circ Res. 2004; 95(1):21-33. DOI: 10.1161/01.RES.0000130529.18016.35. View

20.

Werdich A, Brzezinski A, Jeyaraj D, Sabeh M, Ficker E, Wan X . The zebrafish as a novel animal model to study the molecular mechanisms of mechano-electrical feedback in the heart. Prog Biophys Mol Biol. 2012; 110(2-3):154-65. PMC: 3663588. DOI: 10.1016/j.pbiomolbio.2012.07.006. View