Abstract

For more than a century, the traditional method of stimulating neural activity has been based on electrical methods, and it remains the gold standard to date. We report a technological breakthrough in neural activation in which low-level, pulsed infrared laser light is used to elicit compound nerve and muscle potentials in mammalian peripheral nerve in vivo. Optically induced neural action potentials are spatially precise, artifact free, and damage free and are generated by use of energies well below tissue ablation threshold. Thus optical stimulation presents a simple yet novel approach to contact-free in vivo neural activation that has major implications for clinical neurosurgery, basic neurophysiology, and neuroscience.

© 2005 Optical Society of America

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  1. G. Fritsch and E. Hitzig, Arch. Anat. Physiol. Wiss. Med. 37, 300 (1870).
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    [CrossRef] [PubMed]
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    [CrossRef]
  4. D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).
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    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef]
  8. G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
    [CrossRef]
  9. H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
    [CrossRef] [PubMed]
  10. H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
    [CrossRef]
  11. F. E. Roux and M. Tremoulet, J. Neurosurg. 97, 857 (2002).
    [CrossRef] [PubMed]
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    [CrossRef]
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    [CrossRef] [PubMed]
  14. E. R. Kandel, J. H. Schwartz, and T. M. Jessell, eds., Principles of Neural Science, 4th ed. (McGraw-Hill, New York, 2000).
  15. G. S. Edwards and R. H. Austin, Rev. Sci. Instrum. 74, 3207 (2003).
    [CrossRef]
  16. G. M. Hale and M. R. Querry, Appl. Opt. 12, 555 (1973).
    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]

2004

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

2003

J. K. Song, B. Abou-Khalil, and P. E. Konrad, J. Neurol. Neurosurg. Psych. 74, 561 (2003).
[CrossRef]

G. S. Edwards and R. H. Austin, Rev. Sci. Instrum. 74, 3207 (2003).
[CrossRef]

S. I. Norton, Biomed. Eng. Online 2, 6 (2003).
[CrossRef]

2002

F. E. Roux and M. Tremoulet, J. Neurosurg. 97, 857 (2002).
[CrossRef] [PubMed]

P. A. Starr, Stereotact. Funct. Neurosurg. 79, 118 (2002).
[CrossRef]

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

2001

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

1999

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

1994

G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
[CrossRef]

1991

S. Thomsen, Photochem. Photobiol. 53, 825 (1991).
[CrossRef] [PubMed]

1985

L. A. Geddes and J. D. Bourland, IEEE. Trans. Biomed. Eng. 32, 458 (1985).
[CrossRef] [PubMed]

L. A. Geddes and J. D. Bourland, Med. Biol. Eng. Comput. 23, 131 (1985).
[CrossRef] [PubMed]

1982

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

1973

1870

G. Fritsch and E. Hitzig, Arch. Anat. Physiol. Wiss. Med. 37, 300 (1870).

Abou-Khalil, B.

J. K. Song, B. Abou-Khalil, and P. E. Konrad, J. Neurol. Neurosurg. Psych. 74, 561 (2003).
[CrossRef]

Albe-Fessard, D.

G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
[CrossRef]

Allegre, G.

G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
[CrossRef]

Anschel, D.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Austin, R. H.

G. S. Edwards and R. H. Austin, Rev. Sci. Instrum. 74, 3207 (2003).
[CrossRef]

Avrillier, S.

G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
[CrossRef]

Berlizot, B. B.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Bourland, J. D.

L. A. Geddes and J. D. Bourland, Med. Biol. Eng. Comput. 23, 131 (1985).
[CrossRef] [PubMed]

L. A. Geddes and J. D. Bourland, IEEE. Trans. Biomed. Eng. 32, 458 (1985).
[CrossRef] [PubMed]

Burke, D.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Cuffin, N.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Cummins, K. L.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Daube, J.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Dorfman, L. J.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Edwards, G. S.

G. S. Edwards and R. H. Austin, Rev. Sci. Instrum. 74, 3207 (2003).
[CrossRef]

Fischer, C.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Fritsch, G.

G. Fritsch and E. Hitzig, Arch. Anat. Physiol. Wiss. Med. 37, 300 (1870).

Fuchigami, Y.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Fujimoto, H.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Gangitano, M.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Geddes, L. A.

L. A. Geddes and J. D. Bourland, Med. Biol. Eng. Comput. 23, 131 (1985).
[CrossRef] [PubMed]

L. A. Geddes and J. D. Bourland, IEEE. Trans. Biomed. Eng. 32, 458 (1985).
[CrossRef] [PubMed]

Goldberg, J.

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

Hale, G. M.

Hirase, H.

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

Hitzig, E.

G. Fritsch and E. Hitzig, Arch. Anat. Physiol. Wiss. Med. 37, 300 (1870).

Ives, J.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Jones, S. J.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Kaneko, K.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Kawai, S.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Kobayashi, M.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Konrad, P. E.

J. K. Song, B. Abou-Khalil, and P. E. Konrad, J. Neurol. Neurosurg. Psych. 74, 561 (2003).
[CrossRef]

Leutkemeyer, K.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

McGill, K. C.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Nishimura, D. G.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Norton, S. I.

S. I. Norton, Biomed. Eng. Online 2, 6 (2003).
[CrossRef]

Nuwer, M. R.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Pascual-Leone, A.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Querry, M. R.

Romero, R.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Roux, F. E.

F. E. Roux and M. Tremoulet, J. Neurosurg. 97, 857 (2002).
[CrossRef] [PubMed]

Schomer, D.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Schramm, J.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Song, J. K.

J. K. Song, B. Abou-Khalil, and P. E. Konrad, J. Neurol. Neurosurg. Psych. 74, 561 (2003).
[CrossRef]

Starr, P. A.

P. A. Starr, Stereotact. Funct. Neurosurg. 79, 118 (2002).
[CrossRef]

Taguchi, T.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Theoret, H.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Thomsen, S.

S. Thomsen, Photochem. Photobiol. 53, 825 (1991).
[CrossRef] [PubMed]

S. Thomsen, in Laser-Induced Interstitial Thermotherapy, G. Mueller and A. Roggen, eds., SPIE Press Monograph PM25 (SPIE, Bellingham, Wash., 1995), pp. 459–467.

Tremoulet, M.

F. E. Roux and M. Tremoulet, J. Neurosurg. 97, 857 (2002).
[CrossRef] [PubMed]

Ueno, H.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

Volodymyr, N.

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

Wagner, T.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

Widrow, B.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

Yingling, C. D.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

Yuste, R.

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

Appl. Opt.

Arch. Anat. Physiol. Wiss. Med.

G. Fritsch and E. Hitzig, Arch. Anat. Physiol. Wiss. Med. 37, 300 (1870).

Biomed. Eng. Online

S. I. Norton, Biomed. Eng. Online 2, 6 (2003).
[CrossRef]

Electroencephal. Clin. Neurophysiol. Suppl.

D. Burke, M. R. Nuwer, J. Daube, C. Fischer, J. Schramm, C. D. Yingling, and S. J. Jones, Electroencephal. Clin. Neurophysiol. Suppl. 52, 133 (1999).

IEEE Trans. Biomed. Eng.

K. C. McGill, K. L. Cummins, L. J. Dorfman, B. B. Berlizot, K. Leutkemeyer, D. G. Nishimura, and B. Widrow, IEEE Trans. Biomed. Eng. 29, 129 (1982).
[CrossRef] [PubMed]

IEEE. Trans. Biomed. Eng.

L. A. Geddes and J. D. Bourland, IEEE. Trans. Biomed. Eng. 32, 458 (1985).
[CrossRef] [PubMed]

Int. Orthop.

H. Ueno, K. Kaneko, T. Taguchi, Y. Fuchigami, H. Fujimoto, and S. Kawai, Int. Orthop. 24, 361 (2001).
[CrossRef]

J. Neurobiol.

H. Hirase, N. Volodymyr, J. Goldberg, and R. Yuste, J. Neurobiol. 51, 237 (2002).
[CrossRef] [PubMed]

J. Neurol. Neurosurg. Psych.

J. K. Song, B. Abou-Khalil, and P. E. Konrad, J. Neurol. Neurosurg. Psych. 74, 561 (2003).
[CrossRef]

J. Neurosurg.

F. E. Roux and M. Tremoulet, J. Neurosurg. 97, 857 (2002).
[CrossRef] [PubMed]

Med. Biol. Eng. Comput.

L. A. Geddes and J. D. Bourland, Med. Biol. Eng. Comput. 23, 131 (1985).
[CrossRef] [PubMed]

Neurosci. Lett.

T. Wagner, M. Gangitano, R. Romero, H. Theoret, M. Kobayashi, D. Anschel, J. Ives, N. Cuffin, D. Schomer, and A. Pascual-Leone, Neurosci. Lett. 354, 91 (2004).
[CrossRef]

G. Allegre, S. Avrillier, and D. Albe-Fessard, Neurosci. Lett. 180, 261 (1994).
[CrossRef]

Photochem. Photobiol.

S. Thomsen, Photochem. Photobiol. 53, 825 (1991).
[CrossRef] [PubMed]

Rev. Sci. Instrum.

G. S. Edwards and R. H. Austin, Rev. Sci. Instrum. 74, 3207 (2003).
[CrossRef]

Stereotact. Funct. Neurosurg.

P. A. Starr, Stereotact. Funct. Neurosurg. 79, 118 (2002).
[CrossRef]

Other

E. R. Kandel, J. H. Schwartz, and T. M. Jessell, eds., Principles of Neural Science, 4th ed. (McGraw-Hill, New York, 2000).

S. Thomsen, in Laser-Induced Interstitial Thermotherapy, G. Mueller and A. Roggen, eds., SPIE Press Monograph PM25 (SPIE, Bellingham, Wash., 1995), pp. 459–467.

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Figures (3)

Fig. 1
Fig. 1

Compound nerve and muscle action potentials recorded from a sciatic nerve in a frog in vivo: (a) CNAP recorded by use of electrical stimulation λ=4.0 µm, (b) CNAP from optical stimulation, (c) hamstring CMAP recorded by use of electrical optical stimulation λ=4.0 µm, (d) hamstring CMAP by optical stimulation.

Fig. 2
Fig. 2

Safety ratio of stimulation by use of the FEL as well as of the Ho:YAG laser. The solid curve denotes water absorption as determined by Fourier-transform IR spectroscopy.

Fig. 3
Fig. 3

Histological samples (H&E stain) of rat sciatic nerve tissue (excision immediately after stimulation). The irradiated zones are marked by striped boxes: Left, normal tissue (sham) without laser irradiation; center, stimulation site irradiated by ten pulses at λ=2.12 µm and 0.65 J/cm2; right, control lesion irradiated by 20 pulses at λ=2.12 µm and 2.5 J/cm2.

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