Abstract

Optical mapping (OM) of electrical activity using voltage-sensitive fluorescent dyes is a powerful tool for the investigation of embryonic cardiac electrophysiology. However, because conventional OM integrates the signal in depth and projects it to a two-dimensional plane, information acquired is incomplete and dependent upon the orientation of the sample. This complicates interpretation of data, especially when comparing one heart to another. To overcome this limitation, we present volumetric OM using light-sheet microscopy, which enables high-speed capture of optically sectioned slices. Voltage-sensitive fluorescence images from multiple planes across entire early embryonic quail hearts were acquired, and complete, orientation-independent, four-dimensional maps of transmembrane potential are demonstrated. Volumetric OM data were collected while using optical pacing to control the heart rate, paving the way for physiological measurements and precise manipulation of the heartbeat in the future.

© 2016 Optical Society of America

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2016 (1)

M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
[Crossref]

2015 (1)

2014 (6)

Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
[Crossref] [PubMed]

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2014).
[Crossref] [PubMed]

P. Ma, Y. T. Wang, S. Gu, M. Watanabe, M. W. Jenkins, and A. M. Rollins, “Three-dimensional correction of conduction velocity in the embryonic heart using integrated optical mapping and optical coherence tomography,” J. Biomed. Opt. 19(7), 076004 (2014).
[Crossref] [PubMed]

J. H. Hou, J. M. Kralj, A. D. Douglass, F. Engert, and A. E. Cohen, “Simultaneous mapping of membrane voltage and calcium in zebrafish heart in vivo reveals chamber-specific developmental transitions in ionic currents,” Front. Physiol. 5, 344 (2014).
[Crossref] [PubMed]

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12(1), 23–26 (2014).
[Crossref] [PubMed]

2013 (3)

2012 (1)

T. J. Herron, P. Lee, and J. Jalife, “Optical Imaging of Voltage and Calcium in Cardiac Cells & Tissues,” Circ. Res. 110(4), 609–623 (2012).
[Crossref] [PubMed]

2010 (3)

D. Panáková, A. A. Werdich, and C. A. Macrae, “Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca2+ channel,” Nature 466(7308), 874–878 (2010).
[Crossref] [PubMed]

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (1)

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

2007 (2)

F. Qu, C. M. Ripplinger, V. P. Nikolski, C. Grimm, and I. R. Efimov, “Three-dimensional panoramic imaging of cardiac arrhythmias in rabbit heart,” J. Biomed. Opt. 12(4), 044019 (2007).
[Crossref] [PubMed]

T. Mikawa and R. Hurtado, “Development of the cardiac conduction system,” Semin. Cell Dev. Biol. 18(1), 90–100 (2007).
[Crossref] [PubMed]

2006 (1)

A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie, “Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles,” Am. J. Physiol. Heart Circ. Physiol. 292(3), H1291–H1300 (2006).
[Crossref] [PubMed]

2005 (1)

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

2004 (6)

I. R. Efimov, V. P. Nikolski, and G. Salama, “Optical Imaging of the Heart,” Circ. Res. 95(1), 21–33 (2004).
[Crossref] [PubMed]

D. W. Benson, “Genetics of atrioventricular conduction disease in humans,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 934–939 (2004).
[Crossref] [PubMed]

J. Kolega, “Phototoxicity and photoinactivation of blebbistatin in UV and visible light,” Biochem. Biophys. Res. Commun. 320(3), 1020–1025 (2004).
[Crossref] [PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
[Crossref] [PubMed]

2001 (1)

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

2000 (1)

S. Kirchhoff, J. S. Kim, A. Hagendorff, E. Thönnissen, O. Krüger, W. H. Lamers, and K. Willecke, “Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice,” Circ. Res. 87(5), 399–405 (2000).
[Crossref] [PubMed]

1994 (1)

S. Rohr and B. M. Salzberg, “Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale,” Biophys. J. 67(3), 1301–1315 (1994).
[Crossref] [PubMed]

1992 (1)

V. Hamburger and H. L. Hamilton, “A series of normal stages in the development of the chick embryo. 1951,” Dev. Dyn. 195(4), 231–272 (1992).
[Crossref] [PubMed]

1983 (1)

V. Elharrar and B. Surawicz, “Cycle length effect on restitution of action potential duration in dog cardiac fibers,” Am. J. Physiol. 244(6), H782–H792 (1983).
[PubMed]

Ahrens, M. B.

P. J. Keller, M. B. Ahrens, and J. Freeman, “Light-sheet imaging for systems neuroscience,” Nat. Methods 12(1), 27–29 (2014).
[Crossref] [PubMed]

Bembenek, J. N.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Benson, D. W.

D. W. Benson, “Genetics of atrioventricular conduction disease in humans,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 934–939 (2004).
[Crossref] [PubMed]

Betzig, E.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Bigelow, M. R.

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Böhme, R.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Brand-Arzamendi, K.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Bressan, M.

M. Bressan, G. Liu, and T. Mikawa, “Early Mesodermal Cues Assign Avian Cardiac Pacemaker Fate Potential in a Tertiary Heart Field,” Science 340(6133), 744–748 (2013).
[Crossref] [PubMed]

Bussen, M.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Chen, B.-C.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Cheng, Y.

Chi, N. C.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Chiel, H. J.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Chuck, E. T.

E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
[Crossref] [PubMed]

Cohen, A. E.

J. H. Hou, J. M. Kralj, A. D. Douglass, F. Engert, and A. E. Cohen, “Simultaneous mapping of membrane voltage and calcium in zebrafish heart in vivo reveals chamber-specific developmental transitions in ionic currents,” Front. Physiol. 5, 344 (2014).
[Crossref] [PubMed]

Creazzo, T. L.

E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
[Crossref] [PubMed]

Davidson, M. W.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Dealmeida, A.

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Del Bene, F.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Ding, C.

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S. Gu, Y. T. Wang, P. Ma, A. A. Werdich, A. M. Rollins, and M. W. Jenkins, “Mapping conduction velocity of early embryonic hearts with a robust fitting algorithm,” Biomed. Opt. Express 6(6), 2138–2157 (2015).
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Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
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P. Ma, Y. T. Wang, S. Gu, M. Watanabe, M. W. Jenkins, and A. M. Rollins, “Three-dimensional correction of conduction velocity in the embryonic heart using integrated optical mapping and optical coherence tomography,” J. Biomed. Opt. 19(7), 076004 (2014).
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M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
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S. Gu, Y. T. Wang, P. Ma, A. A. Werdich, A. M. Rollins, and M. W. Jenkins, “Mapping conduction velocity of early embryonic hearts with a robust fitting algorithm,” Biomed. Opt. Express 6(6), 2138–2157 (2015).
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Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
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J. H. Hou, J. M. Kralj, A. D. Douglass, F. Engert, and A. E. Cohen, “Simultaneous mapping of membrane voltage and calcium in zebrafish heart in vivo reveals chamber-specific developmental transitions in ionic currents,” Front. Physiol. 5, 344 (2014).
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S. Kirchhoff, J. S. Kim, A. Hagendorff, E. Thönnissen, O. Krüger, W. H. Lamers, and K. Willecke, “Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice,” Circ. Res. 87(5), 399–405 (2000).
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S. Kirchhoff, J. S. Kim, A. Hagendorff, E. Thönnissen, O. Krüger, W. H. Lamers, and K. Willecke, “Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice,” Circ. Res. 87(5), 399–405 (2000).
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T. J. Herron, P. Lee, and J. Jalife, “Optical Imaging of Voltage and Calcium in Cardiac Cells & Tissues,” Circ. Res. 110(4), 609–623 (2012).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
[Crossref]

S. Gu, Y. T. Wang, P. Ma, A. A. Werdich, A. M. Rollins, and M. W. Jenkins, “Mapping conduction velocity of early embryonic hearts with a robust fitting algorithm,” Biomed. Opt. Express 6(6), 2138–2157 (2015).
[Crossref] [PubMed]

Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
[Crossref] [PubMed]

P. Ma, Y. T. Wang, S. Gu, M. Watanabe, M. W. Jenkins, and A. M. Rollins, “Three-dimensional correction of conduction velocity in the embryonic heart using integrated optical mapping and optical coherence tomography,” J. Biomed. Opt. 19(7), 076004 (2014).
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E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
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M. Bressan, G. Liu, and T. Mikawa, “Early Mesodermal Cues Assign Avian Cardiac Pacemaker Fate Potential in a Tertiary Heart Field,” Science 340(6133), 744–748 (2013).
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T. Mikawa and R. Hurtado, “Development of the cardiac conduction system,” Semin. Cell Dev. Biol. 18(1), 90–100 (2007).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Mitchell, D. M.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Morley, G. E.

E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
[Crossref] [PubMed]

Mullins, R. D.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Nikolski, V. P.

F. Qu, C. M. Ripplinger, V. P. Nikolski, C. Grimm, and I. R. Efimov, “Three-dimensional panoramic imaging of cardiac arrhythmias in rabbit heart,” J. Biomed. Opt. 12(4), 044019 (2007).
[Crossref] [PubMed]

I. R. Efimov, V. P. Nikolski, and G. Salama, “Optical Imaging of the Heart,” Circ. Res. 95(1), 21–33 (2004).
[Crossref] [PubMed]

Olgin, J. E.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Panáková, D.

D. Panáková, A. A. Werdich, and C. A. Macrae, “Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca2+ channel,” Nature 466(7308), 874–878 (2010).
[Crossref] [PubMed]

Polo-Parada, L.

M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
[Crossref]

Qu, F.

F. Qu, C. M. Ripplinger, V. P. Nikolski, C. Grimm, and I. R. Efimov, “Three-dimensional panoramic imaging of cardiac arrhythmias in rabbit heart,” J. Biomed. Opt. 12(4), 044019 (2007).
[Crossref] [PubMed]

Reckova, M.

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Reymann, A. C.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Ripplinger, C. M.

F. Qu, C. M. Ripplinger, V. P. Nikolski, C. Grimm, and I. R. Efimov, “Three-dimensional panoramic imaging of cardiac arrhythmias in rabbit heart,” J. Biomed. Opt. 12(4), 044019 (2007).
[Crossref] [PubMed]

Ritter, A. T.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Rohr, S.

S. Rohr and B. M. Salzberg, “Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale,” Biophys. J. 67(3), 1301–1315 (1994).
[Crossref] [PubMed]

Rollins, A. M.

M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
[Crossref]

S. Gu, Y. T. Wang, P. Ma, A. A. Werdich, A. M. Rollins, and M. W. Jenkins, “Mapping conduction velocity of early embryonic hearts with a robust fitting algorithm,” Biomed. Opt. Express 6(6), 2138–2157 (2015).
[Crossref] [PubMed]

Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
[Crossref] [PubMed]

P. Ma, Y. T. Wang, S. Gu, M. Watanabe, M. W. Jenkins, and A. M. Rollins, “Three-dimensional correction of conduction velocity in the embryonic heart using integrated optical mapping and optical coherence tomography,” J. Biomed. Opt. 19(7), 076004 (2014).
[Crossref] [PubMed]

M. W. Jenkins, Y. T. Wang, Y. Q. Doughman, M. Watanabe, Y. Cheng, and A. M. Rollins, “Optical pacing of the adult rabbit heart,” Biomed. Opt. Express 4(9), 1626–1635 (2013).
[Crossref] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

M. Gargesha, M. W. Jenkins, D. L. Wilson, and A. M. Rollins, “High temporal resolution OCT using image-based retrospective gating,” Opt. Express 17(13), 10786–10799 (2009).
[Crossref] [PubMed]

Romero, D. P.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Rosenbaum, D. S.

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

Rosengarten, C.

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

Saffitz, J. E.

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

Salama, G.

I. R. Efimov, V. P. Nikolski, and G. Salama, “Optical Imaging of the Heart,” Circ. Res. 95(1), 21–33 (2004).
[Crossref] [PubMed]

Salzberg, B. M.

S. Rohr and B. M. Salzberg, “Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale,” Biophys. J. 67(3), 1301–1315 (1994).
[Crossref] [PubMed]

Schmid, B.

Schmidt, A. D.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Schuessler, R. B.

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

Sedmera, D.

A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie, “Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles,” Am. J. Physiol. Heart Circ. Physiol. 292(3), H1291–H1300 (2006).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Seydoux, G.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Shao, L.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Shaw, R. M.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Stadt, H.

A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie, “Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles,” Am. J. Physiol. Heart Circ. Physiol. 292(3), H1291–H1300 (2006).
[Crossref] [PubMed]

Stainier, D. Y. R.

N. C. Chi, M. Bussen, K. Brand-Arzamendi, C. Ding, J. E. Olgin, R. M. Shaw, G. R. Martin, and D. Y. R. Stainier, “Cardiac conduction is required to preserve cardiac chamber morphology,” Proc. Natl. Acad. Sci. U.S.A. 107(33), 14662–14667 (2010).
[Crossref] [PubMed]

Stanley, C. P.

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Stelzer, E. H.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Stelzer, E. H. K.

E. H. K. Stelzer, “Light-sheet fluorescence microscopy for quantitative biology,” Nat. Methods 12(1), 23–26 (2014).
[Crossref] [PubMed]

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

Surawicz, B.

V. Elharrar and B. Surawicz, “Cycle length effect on restitution of action potential duration in dog cardiac fibers,” Am. J. Physiol. 244(6), H782–H792 (1983).
[PubMed]

Swoger, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Thompson, R. P.

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

Thönnissen, E.

S. Kirchhoff, J. S. Kim, A. Hagendorff, E. Thönnissen, O. Krüger, W. H. Lamers, and K. Willecke, “Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice,” Circ. Res. 87(5), 399–405 (2000).
[Crossref] [PubMed]

Torres, M. I.

D. Sedmera, M. Reckova, C. Rosengarten, M. I. Torres, R. G. Gourdie, and R. P. Thompson, “Optical Mapping of Electrical Activation in the Developing Heart,” Microsc. Microanal. 11(3), 209–215 (2005).
[Crossref] [PubMed]

Tulu, U. S.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Voigt, F. F.

Wang, J. T.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Wang, K.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Wang, Y. T.

Watanabe, M.

M. Watanabe, A. M. Rollins, L. Polo-Parada, P. Ma, S. Gu, and M. W. Jenkins, “Probing the Electrophysiology of the Developing Heart,” Journal of Cardiovascular Development and Disease 3(1), 10 (2016).
[Crossref]

P. Ma, Y. T. Wang, S. Gu, M. Watanabe, M. W. Jenkins, and A. M. Rollins, “Three-dimensional correction of conduction velocity in the embryonic heart using integrated optical mapping and optical coherence tomography,” J. Biomed. Opt. 19(7), 076004 (2014).
[Crossref] [PubMed]

Y. T. Wang, S. Gu, P. Ma, M. Watanabe, A. M. Rollins, and M. W. Jenkins, “Optical stimulation enables paced electrophysiological studies in embryonic hearts,” Biomed. Opt. Express 5(4), 1000–1013 (2014).
[Crossref] [PubMed]

M. W. Jenkins, Y. T. Wang, Y. Q. Doughman, M. Watanabe, Y. Cheng, and A. M. Rollins, “Optical pacing of the adult rabbit heart,” Biomed. Opt. Express 4(9), 1626–1635 (2013).
[Crossref] [PubMed]

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Wen, X.

A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie, “Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles,” Am. J. Physiol. Heart Circ. Physiol. 292(3), H1291–H1300 (2006).
[Crossref] [PubMed]

Werdich, A. A.

S. Gu, Y. T. Wang, P. Ma, A. A. Werdich, A. M. Rollins, and M. W. Jenkins, “Mapping conduction velocity of early embryonic hearts with a robust fitting algorithm,” Biomed. Opt. Express 6(6), 2138–2157 (2015).
[Crossref] [PubMed]

D. Panáková, A. A. Werdich, and C. A. Macrae, “Wnt11 patterns a myocardial electrical gradient through regulation of the L-type Ca2+ channel,” Nature 466(7308), 874–878 (2010).
[Crossref] [PubMed]

Willecke, K.

S. Kirchhoff, J. S. Kim, A. Hagendorff, E. Thönnissen, O. Krüger, W. H. Lamers, and K. Willecke, “Abnormal cardiac conduction and morphogenesis in connexin40 and connexin43 double-deficient mice,” Circ. Res. 87(5), 399–405 (2000).
[Crossref] [PubMed]

Wilson, D. L.

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. K. Stelzer, “Reconstruction of Zebrafish Early Embryonic Development by Scanned Light Sheet Microscopy,” Science 322(5904), 1065–1069 (2008).
[Crossref] [PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. Stelzer, “Optical sectioning deep inside live embryos by selective plane illumination microscopy,” Science 305(5686), 1007–1009 (2004).
[Crossref] [PubMed]

Wu, X. S.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A. C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref] [PubMed]

Yamada, K. A.

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

Am. J. Physiol. (1)

V. Elharrar and B. Surawicz, “Cycle length effect on restitution of action potential duration in dog cardiac fibers,” Am. J. Physiol. 244(6), H782–H792 (1983).
[PubMed]

Am. J. Physiol. Heart Circ. Physiol. (1)

A. Gurjarpadhye, K. W. Hewett, C. Justus, X. Wen, H. Stadt, M. L. Kirby, D. Sedmera, and R. G. Gourdie, “Cardiac neural crest ablation inhibits compaction and electrical function of conduction system bundles,” Am. J. Physiol. Heart Circ. Physiol. 292(3), H1291–H1300 (2006).
[Crossref] [PubMed]

Anat. Rec. A Discov. Mol. Cell. Evol. Biol. (3)

D. W. Benson, “Genetics of atrioventricular conduction disease in humans,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 934–939 (2004).
[Crossref] [PubMed]

D. Sedmera, M. Reckova, M. R. Bigelow, A. Dealmeida, C. P. Stanley, T. Mikawa, R. G. Gourdie, and R. P. Thompson, “Developmental transitions in electrical activation patterns in chick embryonic heart,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 1001–1009 (2004).
[Crossref] [PubMed]

E. T. Chuck, K. Meyers, D. France, T. L. Creazzo, and G. E. Morley, “Transitions in ventricular activation revealed by two-dimensional optical mapping,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 280A(2), 990–1000 (2004).
[Crossref] [PubMed]

Biochem. Biophys. Res. Commun. (1)

J. Kolega, “Phototoxicity and photoinactivation of blebbistatin in UV and visible light,” Biochem. Biophys. Res. Commun. 320(3), 1020–1025 (2004).
[Crossref] [PubMed]

Biomed. Opt. Express (3)

Biophys. J. (1)

S. Rohr and B. M. Salzberg, “Multiple site optical recording of transmembrane voltage (MSORTV) in patterned growth heart cell cultures: assessing electrical behavior, with microsecond resolution, on a cellular and subcellular scale,” Biophys. J. 67(3), 1301–1315 (1994).
[Crossref] [PubMed]

Cardiovasc. Res. (1)

B. C. Eloff, D. L. Lerner, K. A. Yamada, R. B. Schuessler, J. E. Saffitz, and D. S. Rosenbaum, “High resolution optical mapping reveals conduction slowing in connexin43 deficient mice,” Cardiovasc. Res. 51(4), 681–690 (2001).
[Crossref] [PubMed]

Circ. Res. (3)

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Supplementary Material (3)

NameDescription
» Visualization 1: MP4 (191 KB)      Multiplanar reformatting of 4D transmembrane potential datasets. The colored activation wave is overlaid on the grayscale heart tube.
» Visualization 2: MP4 (575 KB)      Volume rendering of 4D transmembrane potentials of a looping stage embryonic heart.
» Visualization 3: MP4 (261 KB)      3D activation map of a looping stage embryonic heart.

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Figures (4)

Fig. 1
Fig. 1

System setup diagram. Galvo: galvanometer mirror. OP: optical pacing.

Fig. 2
Fig. 2

Panel A is a fluorescence image of an embryonic heart with voltage-sensitive dye staining. Yellow diamonds b, c and d are pixels whose traces are plotted in panels B, C and D respectively. Intensity values were normalized. myo: myocardium; endo: endocardium.

Fig. 3
Fig. 3

Multiplanar reformatting of 4D transmembrane potential data sets. The colored activation wave is overlaid on the grayscale heart tube. A, E, I, M are 3D transmembrane potential volumes at 0.28s, 0.38s, 0.48s and 0.58s respectively and the locations of the three orthogonal planes are indicated. B, F, J and N are xy-planes at corresponding time points. C, G, K and O are xz-planes at corresponding time points. D, H, L and P are yz-planes at corresponding time points. Colormap represents relative fluorescence intensity (normalized). The colormap is shown at the right bottom corner of panel M. AVJ: atrioventricular junction; OFT: outflow tract.

Fig. 4
Fig. 4

3D activation map of an HH stage 14 embryonic heart. AVJ: atrioventricular junction; V: ventricle; OFT: outflow tract. The region missing colormap in the atrium was the region affected by pacing artifact and it was removed from analysis.

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