Abstract

In infrared neural stimulation (INS), laser-evoked thermal transients are used to generate small depolarising currents in neurons. The laser exposure poses a moderate risk of thermal damage to the target neuron. Indeed, exogenous methods of neural stimulation often place the target neurons under stressful non-physiological conditions, which can hinder ordinary neuronal function and hasten cell death. Therefore, quantifying the exposure-dependent probability of neuronal damage is essential for identifying safe operating limits of INS and other interventions for therapeutic and prosthetic use. Using patch-clamp recordings in isolated spiral ganglion neurons, we describe a method for determining the dose-dependent damage probabilities of individual neurons in response to both acute and cumulative infrared exposure parameters based on changes in injection current. The results identify a local thermal damage threshold at approximately 60 °C, which is in keeping with previous literature and supports the claim that damage during INS is a purely thermal phenomenon. In principle this method can be applied to any potentially injurious stimuli, allowing for the calculation of a wide range of dose-dependent neural damage probabilities. Unlike histological analyses, the technique is well-suited to quantifying gradual neuronal damage, and critical threshold behaviour is not required.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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    [Crossref]
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    [Crossref]
  20. S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
    [Crossref]
  21. V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
    [Crossref]
  22. A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
    [Crossref]
  23. W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
    [Crossref]
  24. A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
    [Crossref]
  25. A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
    [Crossref]
  26. K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
    [Crossref]
  27. F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
    [Crossref]
  28. J. R. Lepock, “Cellular effects of hyperthermia: Relevance to the minimum dose for thermal damage,” Int. J. Hyperther. 19(3), 252–266 (2003).
    [Crossref]
  29. J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
    [Crossref]
  30. H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
    [Crossref]
  31. L. D. Brown, T. T. Cai, and A. DasGupta, “Interval Estimation for a Binomial Proportion,” Statist. Sci. 16(2), 101–133 (2001).
  32. J. E. Turner, D. J. Downing, and J. S. Bogard, Statistical Methods in Radiation Physics (Wiley-VCH, 2012).
  33. J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
    [Crossref]
  34. J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
    [Crossref]
  35. R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
    [Crossref]
  36. L. Paris, I. Marc, B. Charlot, M. Dumas, J. Valmier, and F. Bardin, “Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons,” Biomed. Opt. Express 8(10), 4568 (2017).
    [Crossref]
  37. J. Gallaher, K. Wodzińska, T. Heimburg, and M. Bier, “Ion-channel-like behavior in lipid bilayer membranes at the melting transition,” Phys. Rev. E 81(6), 061925 (2010).
    [Crossref]
  38. A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
    [Crossref]
  39. X. He and J. C. Bischof, “The kinetics of thermal injury in human renal carcinoma cells,” Ann. Biomed. Eng. 33(4), 502–510 (2005).
    [Crossref]
  40. M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
    [Crossref]
  41. A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
    [Crossref]
  42. M. A. J. S. van Boekel, “On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells,” Int. J. Food Microbiol. 74(1-2), 139–159 (2002).
    [Crossref]

2019 (2)

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
[Crossref]

A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
[Crossref]

2018 (1)

M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
[Crossref]

2017 (2)

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

L. Paris, I. Marc, B. Charlot, M. Dumas, J. Valmier, and F. Bardin, “Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons,” Biomed. Opt. Express 8(10), 4568 (2017).
[Crossref]

2016 (2)

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
[Crossref]

P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
[Crossref]

2015 (1)

A. C. Thompson, P. R. Stoddart, and E. D. Jansen, “Optical Stimulation of Neurons,” Curr. Mol. Imaging 3(2), 162–177 (2015).
[Crossref]

2014 (7)

S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref]

M. M. Chernov, G. Chen, and A. W. Roe, “Histological assessment of thermal damage in the brain following infrared neural stimulation,” Brain Stimul. 7(3), 476–482 (2014).
[Crossref]

R. Liljemalm and T. Nyberg, “Quantification of a thermal damage threshold for astrocytes using infrared laser generated heat gradients,” Annals Biomed. Eng. 42(4), 822–832 (2014).
[Crossref]

J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
[Crossref]

K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
[Crossref]

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
[Crossref]

2013 (7)

R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
[Crossref]

F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
[Crossref]

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
[Crossref]

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref]

2012 (6)

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
[Crossref]

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
[Crossref]

A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

2010 (2)

J. Gallaher, K. Wodzińska, T. Heimburg, and M. Bier, “Ion-channel-like behavior in lipid bilayer membranes at the melting transition,” Phys. Rev. E 81(6), 061925 (2010).
[Crossref]

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

2009 (1)

J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
[Crossref]

2007 (3)

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref]

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
[Crossref]

2006 (1)

A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
[Crossref]

2005 (2)

J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
[Crossref]

X. He and J. C. Bischof, “The kinetics of thermal injury in human renal carcinoma cells,” Ann. Biomed. Eng. 33(4), 502–510 (2005).
[Crossref]

2003 (2)

M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
[Crossref]

J. R. Lepock, “Cellular effects of hyperthermia: Relevance to the minimum dose for thermal damage,” Int. J. Hyperther. 19(3), 252–266 (2003).
[Crossref]

2002 (1)

M. A. J. S. van Boekel, “On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells,” Int. J. Food Microbiol. 74(1-2), 139–159 (2002).
[Crossref]

2001 (1)

L. D. Brown, T. T. Cai, and A. DasGupta, “Interval Estimation for a Binomial Proportion,” Statist. Sci. 16(2), 101–133 (2001).

Albea, J.

Albert, E. S.

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

Atienzar, F. A.

F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
[Crossref]

Badofsky, B.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

Bardin, F.

L. Paris, I. Marc, B. Charlot, M. Dumas, J. Valmier, and F. Bardin, “Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons,” Biomed. Opt. Express 8(10), 4568 (2017).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

Bec, J. M.

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

Beier, H. T.

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
[Crossref]

Bendett, M.

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

Beskok, A.

A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
[Crossref]

Bezanilla, F.

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
[Crossref]

Bier, M.

J. Gallaher, K. Wodzińska, T. Heimburg, and M. Bier, “Ion-channel-like behavior in lipid bilayer membranes at the melting transition,” Phys. Rev. E 81(6), 061925 (2010).
[Crossref]

Bischof, J. C.

X. He and J. C. Bischof, “The kinetics of thermal injury in human renal carcinoma cells,” Ann. Biomed. Eng. 33(4), 502–510 (2005).
[Crossref]

Bogard, J. S.

J. E. Turner, D. J. Downing, and J. S. Bogard, Statistical Methods in Radiation Physics (Wiley-VCH, 2012).

Bradley, A.

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
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J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
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L. D. Brown, T. T. Cai, and A. DasGupta, “Interval Estimation for a Binomial Proportion,” Statist. Sci. 16(2), 101–133 (2001).

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J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
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J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
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Chekroud, K.

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J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
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K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
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M. M. Chernov, G. Chen, and A. W. Roe, “Histological assessment of thermal damage in the brain following infrared neural stimulation,” Brain Stimul. 7(3), 476–482 (2014).
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E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
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S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
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L. D. Brown, T. T. Cai, and A. DasGupta, “Interval Estimation for a Binomial Proportion,” Statist. Sci. 16(2), 101–133 (2001).

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J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
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E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
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S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
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A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
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L. Paris, I. Marc, B. Charlot, M. Dumas, J. Valmier, and F. Bardin, “Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons,” Biomed. Opt. Express 8(10), 4568 (2017).
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J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
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S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
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P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
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Friedman, R. M.

J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
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E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
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Hart, W. L.

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
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X. He and J. C. Bischof, “The kinetics of thermal injury in human renal carcinoma cells,” Ann. Biomed. Eng. 33(4), 502–510 (2005).
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J. Gallaher, K. Wodzińska, T. Heimburg, and M. Bier, “Ion-channel-like behavior in lipid bilayer membranes at the melting transition,” Phys. Rev. E 81(6), 061925 (2010).
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S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
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M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
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Horn, C. C.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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Hsu, C. W.

K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
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H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
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A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
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E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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A. C. Thompson, P. R. Stoddart, and E. D. Jansen, “Optical Stimulation of Neurons,” Curr. Mol. Imaging 3(2), 162–177 (2015).
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J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
[Crossref]

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
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J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
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A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
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A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
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J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
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E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

Kameneva, T.

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
[Crossref]

Kao, C.

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
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J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
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Kao, C. C.

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
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Kim, J.

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
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Kim, R.

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
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M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
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Koklu, A.

A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
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Konrad, P.

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref]

J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
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Konrad, P. E.

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
[Crossref]

Lei, K. F.

K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
[Crossref]

Lenaers, G.

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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J. R. Lepock, “Cellular effects of hyperthermia: Relevance to the minimum dose for thermal damage,” Int. J. Hyperther. 19(3), 252–266 (2003).
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P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
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R. Liljemalm and T. Nyberg, “Quantification of a thermal damage threshold for astrocytes using infrared laser generated heat gradients,” Annals Biomed. Eng. 42(4), 822–832 (2014).
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R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
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Liu, B.

J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
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M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
[Crossref]

Lothet, E. H.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

Lu, H.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

Mahadevan-Jansen, A.

J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
[Crossref]

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref]

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
[Crossref]

J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
[Crossref]

Mansoorifar, A.

A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
[Crossref]

Marc, I.

L. Paris, I. Marc, B. Charlot, M. Dumas, J. Valmier, and F. Bardin, “Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons,” Biomed. Opt. Express 8(10), 4568 (2017).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

Mariappan, K.

Matic, A. I.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

McArthur, S. L.

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

McManus, J. M.

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

Milner, T.

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref]

Moreno, L. E.

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

Muller, A.

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

Musick, J. D.

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
[Crossref]

Nam, Y.

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
[Crossref]

S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref]

Nayagam, B. A.

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
[Crossref]

Needham, K.

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
[Crossref]

Nyberg, T.

R. Liljemalm and T. Nyberg, “Quantification of a thermal damage threshold for astrocytes using infrared laser generated heat gradients,” Annals Biomed. Eng. 42(4), 822–832 (2014).
[Crossref]

R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
[Crossref]

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S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
[Crossref]

Paris, L.

Park, J. H.

S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref]

Park, J.-H.

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
[Crossref]

Pawsey, N. C.

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref]

Pfeifer, S.

S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
[Crossref]

Plaksin, M.

M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
[Crossref]

Qin, F.

J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
[Crossref]

Rajguru, S.

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

Rajguru, S. M.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

Ralph, H.

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

Richter, C. P.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
[Crossref]

Richter, C.-P.

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
[Crossref]

Robinson, A. M.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
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M. M. Chernov, G. Chen, and A. W. Roe, “Histological assessment of thermal damage in the brain following infrared neural stimulation,” Brain Stimul. 7(3), 476–482 (2014).
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P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
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M. A. J. S. van Boekel, “On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells,” Int. J. Food Microbiol. 74(1-2), 139–159 (2002).
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M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
[Crossref]

Shapiro, M. G.

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
[Crossref]

Shaw, K. M.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

Shoham, S.

M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
[Crossref]

Stock, S.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

Stock, S. R.

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

Stoddart, P. R.

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
[Crossref]

A. C. Thompson, P. R. Stoddart, and E. D. Jansen, “Optical Stimulation of Neurons,” Curr. Mol. Imaging 3(2), 162–177 (2015).
[Crossref]

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
[Crossref]

W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
[Crossref]

Stolz, D. B.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

Thomas, R. J.

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
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Thompson, A. C.

A. C. Thompson, P. R. Stoddart, and E. D. Jansen, “Optical Stimulation of Neurons,” Curr. Mol. Imaging 3(2), 162–177 (2015).
[Crossref]

A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
[Crossref]

Thomsen, S.

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
[Crossref]

Thomson, R. H.

P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
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F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
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S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
[Crossref]

Tolstykh, G. P.

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
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F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
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J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
[Crossref]

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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Valmier, J.

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M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
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Villarreal, S.

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
[Crossref]

Von Holst, H.

R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
[Crossref]

Vujanovic, I.

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

Wade, S. A.

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
[Crossref]

A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
[Crossref]

Walsh, J. T.

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
[Crossref]

Wang, Y. T.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

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A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
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Wells, J.

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
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J. Wells, C. Kao, K. Mariappan, J. Albea, E. D. Jansen, P. Konrad, and A. Mahadevan-Jansen, “Optical stimulation of neural tissue in vivo,” Opt. Lett. 30(5), 504 (2005).
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S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
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Whitaker, P.

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
[Crossref]

Wise, A. W.

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
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K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
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J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
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J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
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Yoo, S.

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
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S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref]

Young, H. K.

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

Yu, A.

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

Zhuo, J.

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
[Crossref]

ACS Nano (2)

S. Yoo, S. Hong, Y. Choi, J. H. Park, and Y. Nam, “Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers,” ACS Nano 8(8), 8040–8049 (2014).
[Crossref]

S. Yoo, R. Kim, J.-H. Park, and Y. Nam, “Electro-optical Neural Platform Integrated with Nanoplasmonic Inhibition Interface,” ACS Nano 10(4), 4274–4281 (2016).
[Crossref]

Adv. Healthcare Mater. (1)

J. Yong, K. Needham, W. G. Brown, B. A. Nayagam, S. L. McArthur, A. Yu, and P. R. Stoddart, “Gold-Nanorod-Assisted Near-Infrared Stimulation of Primary Auditory Neurons,” Adv. Healthcare Mater. 3, 1862–1868 (2014).
[Crossref]

Adv. Opt. Mater. (1)

W. L. Hart, T. Kameneva, A. W. Wise, and P. R. Stoddart, “Biological considerations of optical interfaces for neuromodulation,” Adv. Opt. Mater. 7(19), 1900385 (2019).
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Anal. Chem. (1)

A. Mansoorifar, A. Koklu, and A. Beskok, “Quantification of cell death using an impedance-based microfluidic device,” Anal. Chem. 91(6), 4140–4148 (2019).
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Anat. Rec. (1)

V. Goyal, S. Rajguru, A. I. Matic, S. R. Stock, and C. P. Richter, “Acute damage threshold for infrared neural stimulation of the cochlea: Functional and histological evaluation,” Anat. Rec. 295, 1987–1999 (2012).
[Crossref]

Ann. Biomed. Eng. (1)

X. He and J. C. Bischof, “The kinetics of thermal injury in human renal carcinoma cells,” Ann. Biomed. Eng. 33(4), 502–510 (2005).
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Annals Biomed. Eng. (1)

R. Liljemalm and T. Nyberg, “Quantification of a thermal damage threshold for astrocytes using infrared laser generated heat gradients,” Annals Biomed. Eng. 42(4), 822–832 (2014).
[Crossref]

Biomed. Opt. Express (1)

Biophys. J. (2)

J. Wells, C. Kao, P. Konrad, T. Milner, J. Kim, A. Mahadevan-Jansen, and E. D. Jansen, “Biophysical mechanisms of transient optical stimulation of peripheral nerve,” Biophys. J. 93(7), 2567–2580 (2007).
[Crossref]

J. Yao, B. Liu, and F. Qin, “Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies,” Biophys. J. 96(9), 3611–3619 (2009).
[Crossref]

Biosens. Bioelectron. (1)

K. F. Lei, M. H. Wu, C. W. Hsu, and Y. D. Chen, “Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip,” Biosens. Bioelectron. 51, 16–21 (2014).
[Crossref]

Biosensors (1)

F. A. Atienzar, H. Gerets, K. Tilmant, G. Toussaint, and S. Dhalluin, “Evaluation of impedance-based label-free technology as a tool for pharmacology and toxicology investigations,” Biosensors 3(1), 132–156 (2013).
[Crossref]

Brain Stimul. (1)

M. M. Chernov, G. Chen, and A. W. Roe, “Histological assessment of thermal damage in the brain following infrared neural stimulation,” Brain Stimul. 7(3), 476–482 (2014).
[Crossref]

Curr. Mol. Imaging (1)

A. C. Thompson, P. R. Stoddart, and E. D. Jansen, “Optical Stimulation of Neurons,” Curr. Mol. Imaging 3(2), 162–177 (2015).
[Crossref]

Hear. Res. (1)

S. M. Rajguru, A. I. Matic, A. M. Robinson, A. J. Fishman, L. E. Moreno, A. Bradley, I. Vujanovic, J. Breen, J. D. Wells, M. Bendett, and C. P. Richter, “Optical cochlear implants: Evaluation of surgical approach and laser parameters in cats,” Hear. Res. 269(1-2), 102–111 (2010).
[Crossref]

IEEE Trans. Biomed. Eng. (2)

A. D. Izzo, J. T. Walsh, E. D. Jansen, M. Bendett, J. Webb, H. Ralph, and C. P. Richter, “Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength,” IEEE Trans. Biomed. Eng. 54(6), 1108–1114 (2007).
[Crossref]

A. C. Thompson, S. A. Wade, N. C. Pawsey, and P. R. Stoddart, “Infrared neural stimulation: Influence of stimulation site spacing and repetition rates on heating,” IEEE Trans. Biomed. Eng. 60(12), 3534–3541 (2013).
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Int. J. Food Microbiol. (1)

M. A. J. S. van Boekel, “On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells,” Int. J. Food Microbiol. 74(1-2), 139–159 (2002).
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Int. J. Hyperther. (2)

J. R. Lepock, “Cellular effects of hyperthermia: Relevance to the minimum dose for thermal damage,” Int. J. Hyperther. 19(3), 252–266 (2003).
[Crossref]

M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, and P. J. Hoopes, “Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia,” Int. J. Hyperther. 19(3), 267–294 (2003).
[Crossref]

J. Biomed. Opt. (2)

A. C. Thompson, S. A. Wade, W. G. A. Brown, and P. R. Stoddart, “Modeling of light absorption in tissue during infrared neural stimulation,” J. Biomed. Opt. 17(7), 0750021 (2012).
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A. C. Thompson, S. A. Wade, P. J. Cadusch, W. G. A. Brown, and P. R. Stoddart, “Modeling of the temporal effects of heating during infrared neural stimulation,” J. Biomed. Opt. 18(3), 035004 (2013).
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J. Neural Eng. (1)

H. T. Beier, G. P. Tolstykh, J. D. Musick, R. J. Thomas, and B. L. Ibey, “Plasma membrane nanoporation as a possible mechanism behind infrared excitation of cells,” J. Neural Eng. 11(6), 066006 (2014).
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J. Neurophysiol. (1)

E. S. Albert, J. M. Bec, G. Desmadryl, K. Chekroud, C. Travo, S. Gaboyard, F. Bardin, I. Marc, M. Dumas, G. Lenaers, C. Hamel, A. Muller, and C. Chabbert, “TRPV4 channels mediate the infrared laser-evoked response in sensory neurons,” J. Neurophysiol. 107(12), 3227–3234 (2012).
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S. Diemert, A. M. Dolga, S. Tobaben, J. Grohm, S. Pfeifer, E. Oexler, and C. Culmsee, “Impedance measurement for real time detection of neuronal cell death,” J. Neurosci. Methods 203(1), 69–77 (2012).
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J. Vis. Exp. (1)

W. G. A. Brown, K. Needham, B. A. Nayagam, and P. R. Stoddart, “Whole Cell Patch Clamp for Investigating the Mechanisms of Infrared Neural Stimulation,” J. Vis. Exp. 77, 50444 (2013).
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Lasers Surg. Med. (4)

J. D. Wells, S. Thomsen, P. Whitaker, E. D. Jansen, C. C. Kao, P. E. Konrad, and A. Mahadevan-Jansen, “Optically mediated nerve stimulation: Identification of injury thresholds,” Lasers Surg. Med. 39, 513–526 (2007).
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A. D. Izzo, C. P. Richter, E. D. Jansen, and J. T. Walsh, “Laser stimulation of the auditory nerve,” Lasers Surg. Med. 38, 745–753 (2006).
[Crossref]

J. M. Bec, E. S. Albert, I. Marc, G. Desmadryl, C. Travo, A. Muller, C. Chabbert, F. Bardin, and M. Dumas, “Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons,” Lasers Surg. Med. 44, 736–745 (2012).
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R. Liljemalm, T. Nyberg, and H. Von Holst, “Heating during infrared neural stimulation,” Lasers Surg. Med. 45, 469–481 (2013).
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Nat. Commun. (1)

M. G. Shapiro, K. Homma, S. Villarreal, C.-P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. 3(1), 736 (2012).
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NeuroImage (1)

J. M. Cayce, R. M. Friedman, G. Chen, E. D. Jansen, A. Mahadevan-Jansen, and A. W. Roe, “Infrared neural stimulation of primary visual cortex in non-human primates,” NeuroImage 84, 181–190 (2014).
[Crossref]

Neuroscientist (1)

P. M. Lewis, R. H. Thomson, J. V. Rosenfeld, and P. B. Fitzgerald, “Brain Neuromodulation Techniques: A Review,” Neuroscientist 22(4), 406–421 (2016).
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Opt. Lett. (1)

Phys. Rev. E (1)

J. Gallaher, K. Wodzińska, T. Heimburg, and M. Bier, “Ion-channel-like behavior in lipid bilayer membranes at the melting transition,” Phys. Rev. E 81(6), 061925 (2010).
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Phys. Rev. X (1)

M. Plaksin, E. Shapira, E. Kimmel, and S. Shoham, “Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects,” Phys. Rev. X 8(1), 011043 (2018).
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PLoS One (1)

A. I. Matic, A. M. Robinson, H. K. Young, B. Badofsky, S. M. Rajguru, S. Stock, and C. P. Richter, “Behavioral and Electrophysiological Responses Evoked by Chronic Infrared Neural Stimulation of the Cochlea,” PLoS One 8(3), e58189 (2013).
[Crossref]

Sci. Rep. (2)

A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. 3(1), 2600 (2013).
[Crossref]

E. H. Lothet, K. M. Shaw, H. Lu, J. Zhuo, Y. T. Wang, S. Gu, D. B. Stolz, E. D. Jansen, C. C. Horn, H. J. Chiel, and M. W. Jenkins, “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. 7(1), 3275 (2017).
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Statist. Sci. (1)

L. D. Brown, T. T. Cai, and A. DasGupta, “Interval Estimation for a Binomial Proportion,” Statist. Sci. 16(2), 101–133 (2001).

Other (1)

J. E. Turner, D. J. Downing, and J. S. Bogard, Statistical Methods in Radiation Physics (Wiley-VCH, 2012).

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Figures (5)

Fig. 1.
Fig. 1. Experimental setup. SGN cultures were immersed in extracellular solution, and healthy cells were located through a phase contrast microscope (not to scale). Infrared light was delivered through an optical fibre attached to a micromanipulator, and electrophysiological recordings were obtained through a patch-clamping electrode attached to an amplifier.
Fig. 2.
Fig. 2. A relatively rapid decline in cell viability. This rapid increase in injection current (indicated by the arrow) during a voltage clamp recording provided a clear indication of cell damage.
Fig. 3.
Fig. 3. Acute damage probabilities. Histograms (left axis) and corresponding damage probabilities (right axis) for the following illumination parameters: (a, b) laser peak power, (c, d) energy per pulse, and (e, f) average power. Data points represent damage probabilities with standard errors. Plots (a, c, e) are for room temperature recordings (22.4 °C) and plots (b, d, f) are for elevated (30.4 °C) temperature recordings. Solid lines are best-fit equations for the MTSH model.
Fig. 4.
Fig. 4. Damage probability due to cumulative energy exposure. Histograms (left axis) and corresponding damage probabilities (right axis) for cumulative energy exposures at ambient extracellular temperatures of (a) 22.4°C and (b) 30.4°C. Data points represent damage probabilities with standard errors, and solid lines are best-fit Weibull distribution models for each data set.
Fig. 5.
Fig. 5. Thermal threshold for infrared-evoked cell damage. Damage probability is plotted as a function of the estimated maximum temperature exposure per recording, including data from both room temperature and elevated temperature conditions. The solid line is a best-fit MTSH model for the room temperature condition. Data from He and Bischof [39] is included for comparison (see text).

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1 1 + 1 / N z 2 ( P d + 1 2 N z 2 ± 1 N P d ( 1 P d ) + 1 4 N 2 z 2 ) ,
P a ( x ) = [ 1 e x p ( x x 0 ) ] n
P c ( x ) = 1 e x p [ ( x η ) ν ]

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