Abstract

We describe a new experimental approach to investigate touch sensation in the model organism C. elegans using light field deconvolution microscopy. By combining fast volumetric image acquisition with controlled indentation of the organism using a high sensitivity force transducer, we are able to simultaneously measure activity in multiple touch receptor neurons expressing the calcium ion indicator GCaMP6s. By varying the applied mechanical stimulus we show how this method can be used to quantify touch sensitivity in C. elegans. We describe some of the challenges of performing light field calcium imaging in moving samples and demonstrate that they can be overcome by simple data processing.

© 2016 Optical Society of America

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  5. A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
    [Crossref] [PubMed]
  6. A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
    [Crossref] [PubMed]
  7. S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2015 (4)

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
[Crossref] [PubMed]

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
[Crossref] [PubMed]

Y. Chen, S. Bharill, E. Y. Isacoff, and M. Chalfie, “Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 112(37), 11690–11695 (2015).
[Crossref] [PubMed]

2014 (3)

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

N. Cohen, S. Yang, A. Andalman, M. Broxton, L. Grosenick, K. Deisseroth, M. Horowitz, and M. Levoy, “Enhancing the performance of the light field microscope using wavefront coding,” Opt. Express 22(20), 24817–24839 (2014).
[Crossref] [PubMed]

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

2013 (4)

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

M. Broxton, L. Grosenick, S. Yang, N. Cohen, A. Andalman, K. Deisseroth, and M. Levoy, “Wave optics theory and 3-D deconvolution for the light field microscope,” Opt. Express 21(21), 25418–25439 (2013).
[Crossref] [PubMed]

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

2012 (2)

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

2010 (2)

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

E. A. Lumpkin, K. L. Marshall, and A. M. Nelson, “The cell biology of touch,” J. Cell Biol. 191(2), 237–248 (2010).
[Crossref] [PubMed]

2009 (2)

M. Chalfie, “Neurosensory mechanotransduction,” Nat. Rev. Mol. Cell Biol. 10(1), 44–52 (2009).
[Crossref] [PubMed]

M. Levoy, Z. Zhang, and I. McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Microsc. 235(2), 144–162 (2009).
[Crossref] [PubMed]

2007 (1)

S.-J. Park, M. B. Goodman, and B. L. Pruitt, “Analysis of nematode mechanics by piezoresistive displacement clamp,” Proc. Natl. Acad. Sci. U.S.A. 104(44), 17376–17381 (2007).
[Crossref] [PubMed]

2006 (1)

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
[Crossref]

2005 (2)

R. O’Hagan, M. Chalfie, and M. B. Goodman, “The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals,” Nat. Neurosci. 8(1), 43–50 (2005).
[Crossref] [PubMed]

R. Ng, “Fourier slice photography,” ACM Trans. Graph. 24(3), 735–744 (2005).
[Crossref]

2003 (1)

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

2002 (1)

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

1995 (1)

M. Huang, G. Gu, E. L. Ferguson, and M. Chalfie, “A stomatin-like protein necessary for mechanosensation in C. elegans,” Nature 378(6554), 292–295 (1995).
[Crossref] [PubMed]

1991 (1)

M. Driscoll and M. Chalfie, “The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration,” Nature 349(6310), 588–593 (1991).
[Crossref] [PubMed]

1981 (1)

M. Chalfie and J. Sulston, “Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans,” Dev. Biol. 82(2), 358–370 (1981).
[Crossref] [PubMed]

Abrahamsson, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Adams, A.

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
[Crossref]

Agard, D. A.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Ahrens, M. B.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

Andalman, A.

Baba, Y.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Baohan, A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Bargmann, C. I.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Bharill, S.

Y. Chen, S. Bharill, E. Y. Isacoff, and M. Chalfie, “Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 112(37), 11690–11695 (2015).
[Crossref] [PubMed]

Bianchi, L.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Biswas, A.

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
[Crossref] [PubMed]

Boyden, E. S.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Broxton, M.

Chalfie, M.

Y. Chen, S. Bharill, E. Y. Isacoff, and M. Chalfie, “Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 112(37), 11690–11695 (2015).
[Crossref] [PubMed]

M. Chalfie, “Neurosensory mechanotransduction,” Nat. Rev. Mol. Cell Biol. 10(1), 44–52 (2009).
[Crossref] [PubMed]

R. O’Hagan, M. Chalfie, and M. B. Goodman, “The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals,” Nat. Neurosci. 8(1), 43–50 (2005).
[Crossref] [PubMed]

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

M. Huang, G. Gu, E. L. Ferguson, and M. Chalfie, “A stomatin-like protein necessary for mechanosensation in C. elegans,” Nature 378(6554), 292–295 (1995).
[Crossref] [PubMed]

M. Driscoll and M. Chalfie, “The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration,” Nature 349(6310), 588–593 (1991).
[Crossref] [PubMed]

M. Chalfie and J. Sulston, “Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans,” Dev. Biol. 82(2), 358–370 (1981).
[Crossref] [PubMed]

Chelur, D. S.

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

Chen, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Chen, L.

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

Chen, T.-W.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Chen, Y.

Y. Chen, S. Bharill, E. Y. Isacoff, and M. Chalfie, “Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 112(37), 11690–11695 (2015).
[Crossref] [PubMed]

Cohen, N.

Dahan, M.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Darzacq, X.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Deisseroth, K.

Driscoll, M.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

M. Driscoll and M. Chalfie, “The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration,” Nature 349(6310), 588–593 (1991).
[Crossref] [PubMed]

Dugast Darzacq, C.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Ernstrom, G. G.

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

Ferguson, E. L.

M. Huang, G. Gu, E. L. Ferguson, and M. Chalfie, “A stomatin-like protein necessary for mechanosensation in C. elegans,” Nature 378(6554), 292–295 (1995).
[Crossref] [PubMed]

Footer, M.

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
[Crossref]

Frøkjaer-Jensen, C.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Gerling, G. J.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Gerstbrein, B.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Goodman, M. B.

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

S.-J. Park, M. B. Goodman, and B. L. Pruitt, “Analysis of nematode mechanics by piezoresistive displacement clamp,” Proc. Natl. Acad. Sci. U.S.A. 104(44), 17376–17381 (2007).
[Crossref] [PubMed]

R. O’Hagan, M. Chalfie, and M. B. Goodman, “The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals,” Nat. Neurosci. 8(1), 43–50 (2005).
[Crossref] [PubMed]

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

Grewe, B. F.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Grosenick, L.

Gu, G.

M. Huang, G. Gu, E. L. Ferguson, and M. Chalfie, “A stomatin-like protein necessary for mechanosensation in C. elegans,” Nature 378(6554), 292–295 (1995).
[Crossref] [PubMed]

Gustafsson, M. G. L.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Hajj, B.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Hanrahan, P.

M. Levoy and P. Hanrahan, “Light field rendering,” in Proceedings of the 23rd annual conference on Computer graphics and interactive techniques, (ACM, 1996), pp. 31–42.

Helmchen, F.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Hoffmann, M.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Horowitz, M.

Huang, M.

M. Huang, G. Gu, E. L. Ferguson, and M. Chalfie, “A stomatin-like protein necessary for mechanosensation in C. elegans,” Nature 378(6554), 292–295 (1995).
[Crossref] [PubMed]

Isacoff, E. Y.

Y. Chen, S. Bharill, E. Y. Isacoff, and M. Chalfie, “Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans,” Proc. Natl. Acad. Sci. U.S.A. 112(37), 11690–11695 (2015).
[Crossref] [PubMed]

Jayaraman, V.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Jenkins, B. A.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Kampa, B. M.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Kasper, H.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Kato, S.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Katsov, A. Y.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Keller, P. J.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

Kerr, R.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Kerr, R. A.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Kim, D. S.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Kumar, S.

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
[Crossref] [PubMed]

Langer, D.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Lesniak, D. R.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Levoy, M.

N. Cohen, S. Yang, A. Andalman, M. Broxton, L. Grosenick, K. Deisseroth, M. Horowitz, and M. Levoy, “Enhancing the performance of the light field microscope using wavefront coding,” Opt. Express 22(20), 24817–24839 (2014).
[Crossref] [PubMed]

M. Broxton, L. Grosenick, S. Yang, N. Cohen, A. Andalman, K. Deisseroth, and M. Levoy, “Wave optics theory and 3-D deconvolution for the light field microscope,” Opt. Express 21(21), 25418–25439 (2013).
[Crossref] [PubMed]

M. Levoy, Z. Zhang, and I. McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Microsc. 235(2), 144–162 (2009).
[Crossref] [PubMed]

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
[Crossref]

M. Levoy and P. Hanrahan, “Light field rendering,” in Proceedings of the 23rd annual conference on Computer graphics and interactive techniques, (ACM, 1996), pp. 31–42.

Li, J. M.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

Liu, G.

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
[Crossref] [PubMed]

Looger, L. L.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Lumpkin, E. A.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

E. A. Lumpkin, K. L. Marshall, and A. M. Nelson, “The cell biology of touch,” J. Cell Biol. 191(2), 237–248 (2010).
[Crossref] [PubMed]

Manivannan, M.

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
[Crossref] [PubMed]

Marshall, K. L.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

E. A. Lumpkin, K. L. Marshall, and A. M. Nelson, “The cell biology of touch,” J. Cell Biol. 191(2), 237–248 (2010).
[Crossref] [PubMed]

Mazzochette, E. A.

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

McDowall, I.

M. Levoy, Z. Zhang, and I. McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Microsc. 235(2), 144–162 (2009).
[Crossref] [PubMed]

Mizuguchi, G.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Mueller, F.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Nelson, A. M.

E. A. Lumpkin, K. L. Marshall, and A. M. Nelson, “The cell biology of touch,” J. Cell Biol. 191(2), 237–248 (2010).
[Crossref] [PubMed]

Ng, R.

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
[Crossref]

R. Ng, “Fourier slice photography,” ACM Trans. Graph. 24(3), 735–744 (2005).
[Crossref]

O’ Hagan, R.

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

O’Hagan, R.

R. O’Hagan, M. Chalfie, and M. B. Goodman, “The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals,” Nat. Neurosci. 8(1), 43–50 (2005).
[Crossref] [PubMed]

Orger, M. B.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Pak, N.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Park, S.-J.

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

S.-J. Park, M. B. Goodman, and B. L. Pruitt, “Analysis of nematode mechanics by piezoresistive displacement clamp,” Proc. Natl. Acad. Sci. U.S.A. 104(44), 17376–17381 (2007).
[Crossref] [PubMed]

Petzold, B. C.

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

Prevedel, R.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Pruitt, B. L.

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

S.-J. Park, M. B. Goodman, and B. L. Pruitt, “Analysis of nematode mechanics by piezoresistive displacement clamp,” Proc. Natl. Acad. Sci. U.S.A. 104(44), 17376–17381 (2007).
[Crossref] [PubMed]

Pulver, S. R.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Rasband, M. N.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Rasband, W. S.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Raskar, R.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Renninger, S. L.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Robson, D. N.

M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
[Crossref] [PubMed]

Schafer, W. R.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Schloerb, D. W.

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
[Crossref] [PubMed]

Schneider, C. A.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Schreiter, E. R.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Schrödel, T.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Slone, D.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Soule, P.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Srinivasan, M. A.

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
[Crossref] [PubMed]

Stallinga, S.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Sulston, J.

M. Chalfie and J. Sulston, “Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans,” Dev. Biol. 82(2), 358–370 (1981).
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Sun, Y.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Suzuki, H.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Svoboda, K.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Vaziri, A.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Wardill, T. J.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Wellnitz, S. A.

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

Wetzstein, G.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Wisniewski, J.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Wu, C.

S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
[Crossref] [PubMed]

Xue, J.

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
[Crossref] [PubMed]

Yang, S.

Yao, C. A.

D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
[Crossref] [PubMed]

Yoon, Y.-G.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

Zhang, Z.

M. Levoy, Z. Zhang, and I. McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Microsc. 235(2), 144–162 (2009).
[Crossref] [PubMed]

Zimmer, M.

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
[Crossref] [PubMed]

ACM Trans. Graph. (2)

M. Levoy, R. Ng, A. Adams, M. Footer, and M. Horowitz, “Light field microscopy,” ACM Trans. Graph. 25(3), 924–934 (2006).
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R. Ng, “Fourier slice photography,” ACM Trans. Graph. 24(3), 735–744 (2005).
[Crossref]

Dev. Biol. (1)

M. Chalfie and J. Sulston, “Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans,” Dev. Biol. 82(2), 358–370 (1981).
[Crossref] [PubMed]

eLife (1)

D. R. Lesniak, K. L. Marshall, S. A. Wellnitz, B. A. Jenkins, Y. Baba, M. N. Rasband, G. J. Gerling, and E. A. Lumpkin, “Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors,” eLife 3, e01488 (2014).
[Crossref] [PubMed]

IEEE Trans. Haptics (2)

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Multiscale Layered Biomechanical Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 31–42 (2015).
[Crossref] [PubMed]

A. Biswas, M. Manivannan, and M. A. Srinivasan, “Vibrotactile Sensitivity Threshold: Nonlinear Stochastic Mechanotransduction Model of the Pacinian Corpuscle,” IEEE Trans. Haptics 8(1), 102–113 (2015).
[Crossref] [PubMed]

Integr Biol (Camb) (1)

B. C. Petzold, S.-J. Park, E. A. Mazzochette, M. B. Goodman, and B. L. Pruitt, “MEMS-based force-clamp analysis of the role of body stiffness in C. elegans touch sensation,” Integr Biol (Camb) 5(6), 853–864 (2013).
[Crossref] [PubMed]

J. Biomech. Eng. (1)

S. Kumar, G. Liu, D. W. Schloerb, and M. A. Srinivasan, “Viscoelastic Characterization of the Primate Finger Pad In Vivo by Microstep Indentation and Three-Dimensional Finite Element Models for Tactile Sensation Studies,” J. Biomech. Eng. 137(6), 061002 (2015).
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J. Cell Biol. (1)

E. A. Lumpkin, K. L. Marshall, and A. M. Nelson, “The cell biology of touch,” J. Cell Biol. 191(2), 237–248 (2010).
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J. Microsc. (1)

M. Levoy, Z. Zhang, and I. McDowall, “Recording and controlling the 4D light field in a microscope using microlens arrays,” J. Microsc. 235(2), 144–162 (2009).
[Crossref] [PubMed]

Nat. Methods (5)

R. Prevedel, Y.-G. Yoon, M. Hoffmann, N. Pak, G. Wetzstein, S. Kato, T. Schrödel, R. Raskar, M. Zimmer, E. S. Boyden, and A. Vaziri, “Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy,” Nat. Methods 11(7), 727–730 (2014).
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M. B. Ahrens, M. B. Orger, D. N. Robson, J. M. Li, and P. J. Keller, “Whole-brain functional imaging at cellular resolution using light-sheet microscopy,” Nat. Methods 10(5), 413–420 (2013).
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S. Abrahamsson, J. Chen, B. Hajj, S. Stallinga, A. Y. Katsov, J. Wisniewski, G. Mizuguchi, P. Soule, F. Mueller, C. Dugast Darzacq, X. Darzacq, C. Wu, C. I. Bargmann, D. A. Agard, M. Dahan, and M. G. L. Gustafsson, “Fast multicolor 3D imaging using aberration-corrected multifocus microscopy,” Nat. Methods 10(1), 60–63 (2012).
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B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
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C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
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R. O’Hagan, M. Chalfie, and M. B. Goodman, “The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals,” Nat. Neurosci. 8(1), 43–50 (2005).
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M. Chalfie, “Neurosensory mechanotransduction,” Nat. Rev. Mol. Cell Biol. 10(1), 44–52 (2009).
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D. S. Chelur, G. G. Ernstrom, M. B. Goodman, C. A. Yao, L. Chen, R. O’ Hagan, and M. Chalfie, “The mechanosensory protein MEC-6 is a subunit of the C. elegans touch-cell degenerin channel,” Nature 420(6916), 669–673 (2002).
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[Crossref] [PubMed]

Neuron (1)

H. Suzuki, R. Kerr, L. Bianchi, C. Frøkjaer-Jensen, D. Slone, J. Xue, B. Gerstbrein, M. Driscoll, and W. R. Schafer, “In Vivo Imaging of C. elegans Mechanosensory Neurons Demonstrates a Specific Role for the MEC-4 Channel in the Process of Gentle Touch Sensation,” Neuron 39(6), 1005–1017 (2003).
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Opt. Express (2)

Proc. Natl. Acad. Sci. U.S.A. (2)

S.-J. Park, M. B. Goodman, and B. L. Pruitt, “Analysis of nematode mechanics by piezoresistive displacement clamp,” Proc. Natl. Acad. Sci. U.S.A. 104(44), 17376–17381 (2007).
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Figures (6)

Fig. 1
Fig. 1 Schematic digram of light field microscope and micromanipulation system. Acronyms: MRL – macro relay lens; MLA – microlens array; TL – tube lens; FFC – fluorescence filter cube; MO – microscope objective. Inset I1: photograph showing microscope objective lens, sample and microforce sensing probe. Inset I2: typical force (red) and displacement (black) data versus time for a indentation-retraction experiment.
Fig. 2
Fig. 2 (a) Magnitude of Fast Fourier Transform of a raw light field image of a uniform fluorescent layer captured before (left) and after (right) correction for pincushion / barrel distortion. (b) Corrected raw light field for a uniform fluorescent layer; yellow circles show experimentally determined size and pitch of pupil subimages.
Fig. 3
Fig. 3 (a) Images of a 2.5 μm diameter green fluorescent microsphere acquired as the objective lens is displaced axially. Top row: conventional widefield images. Bottom row: in-focus plane extracted from reconstructed light field focal series. Scale bar in upper left corner is 3 µm. (b) Lateral and (c) axial line profiles taken through the centre of the bead in the focal series reconstruction as the objective lens is axially displaced. (d) Lateral (unfilled circles) and axial (filled circles) 1/e width of the bead image in the focal series reconstruction as the objective lens is displaced axially.
Fig. 4
Fig. 4 (a) Schematic diagram of an adult stage C.elegans organism showing the locations of the six identified touch receptor neurons. (b) Epifluorescence image of tagRFP labelled MEC-4 protein puncta in a C. elegans TRN. Scale bar is 5 µm. (c) DIC image (grayscale) of a C.elegans organism combined with a maximum intensity projection of a epifluorescence z-stack showing the two posterior gentle touch neurons (green) during a typical indentation with the microforce sensing probe. Scale bar is 12 µm.
Fig. 5
Fig. 5 (a) DIC image showing indentation of C.elegans specimen using microforce sensing probe with conventional epifluorescence image of PLMR overlaid in green. Due to the shallow depth of field the PLML is not visible. Scale bar is 10 µm. (b) Colour coded depth projection created from the reconstructed focal series showing the cell bodies of the two posterior TRNs. (c) Measured force (black data points), probe position (tan solid line) and average brightness of the two TRNs (top) versus time, indicating that both neurons are activated by the stimulus.
Fig. 6
Fig. 6 (a) DIC images showing indentation of a C.elegans specimen to depth of approximately 3 μm (top) and 13 μm (bottom) with a microforce sensing probe approximately 110 μm from the tip of the tail. Maximum intensity projection of reconstructed light field (displayed with a red hot colour map) overlaid to show positions of PLML and coelomocyte. (b) Total brightness of the cell body of the PLML indicates that the TRN is only activated by the withdrawl of the probe following the larger indentation (red line). The signal from a nearby GFP transgenic marker (green line) is constant despite similar displacement following withdrawal of the probe. (c) Corresponding force (solid lines) and probe position (dashed lines) measured during the end of the hold phase of indentation and after probe retraction.

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