Abstract

We demonstrate non-contact sub-nanometer optical measurement of neural surface displacement associated with action potential propagation. Experimental results are recorded from nerve bundles dissected from crayfish walking leg using a phase-sensitive optical low coherence reflectometer. No exogenous chemicals or reflection coatings are applied. Transient neural surface displacement is less than 1 nm in amplitude, 1 ms in duration and is coincident with action potential arrival to the optical measurement site. Because the technique uses back-reflected light, noninvasive detection of various neuropathies may be possible.

© 2004 Optical Society of America

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References

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  1. D. K. Hill, “The volume change resulting from stimulation of a giant nerve fibre,” J. Physiol. 111, 304–327 (1950).
    [PubMed]
  2. S. H. Bryant and J. M. Tobias, “Optical and mechanical concomitants of activity in carcinus nerve I. Effect of sodium azide on the optical response II. Shortening of the nerve with activity,” J. Cell. Comp. Physiol. 46, 71–95 (1955).
    [Crossref]
  3. L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
    [PubMed]
  4. B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
    [Crossref] [PubMed]
  5. K. Iwasa and I. Tasaki, “Mechanical changes in squid giant axons associated with production of action potentials,” Biochem. Biophysic. Res. Comm. 95, 1328–1331 (1980).
    [Crossref]
  6. I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
    [Crossref]
  7. I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophysical J. 57, 633–635 (1990).
    [Crossref]
  8. X. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42, 2972–2978 (2003).
    [Crossref] [PubMed]
  9. R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
    [Crossref]
  10. M. Lazebnik, D. L. Marks, K. Potgieter, R. Gillette, and S. A. Boppart, “Functional optical coherence tomography for detecting neural activity through scattering changes,” Opt. Lett. 28, 1218–1220 (2003).
    [Crossref] [PubMed]
  11. T. Akkin, “Biomedical applications of a fiber based low-coherence interferometer for quantitative differential phase measurements,” Dissertation: The University of Texas at Austin, Austin, (2003).
  12. C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.
  13. G. J. Tearney, B. E. Bouma, and J. G. Fujimoto, “High-speed phase- and group- delay scanning with a grating-based phase control delay line,” Opt. Lett. 22, 1811–1813 (1997).
    [Crossref]
  14. D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
    [Crossref]
  15. T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
    [Crossref]
  16. L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).
  17. L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).
  18. A. von Muralt, “The optical spike,” Phil. Trans. B270, 411–42 (1975).
  19. M. Born and E. Wolf, Principles of Optics, 7th (expended) ed. (Cambridge University Press, Cambridge, UK, 1999) pp. 837–840.

2003 (4)

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

X. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42, 2972–2978 (2003).
[Crossref] [PubMed]

M. Lazebnik, D. L. Marks, K. Potgieter, R. Gillette, and S. A. Boppart, “Functional optical coherence tomography for detecting neural activity through scattering changes,” Opt. Lett. 28, 1218–1220 (2003).
[Crossref] [PubMed]

2001 (1)

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

1997 (1)

1990 (1)

I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophysical J. 57, 633–635 (1990).
[Crossref]

1989 (1)

I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
[Crossref]

1980 (1)

K. Iwasa and I. Tasaki, “Mechanical changes in squid giant axons associated with production of action potentials,” Biochem. Biophysic. Res. Comm. 95, 1328–1331 (1980).
[Crossref]

1977 (1)

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

1975 (1)

A. von Muralt, “The optical spike,” Phil. Trans. B270, 411–42 (1975).

1973 (1)

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
[PubMed]

1970 (1)

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).

1969 (1)

L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).

1955 (1)

S. H. Bryant and J. M. Tobias, “Optical and mechanical concomitants of activity in carcinus nerve I. Effect of sodium azide on the optical response II. Shortening of the nerve with activity,” J. Cell. Comp. Physiol. 46, 71–95 (1955).
[Crossref]

1950 (1)

D. K. Hill, “The volume change resulting from stimulation of a giant nerve fibre,” J. Physiol. 111, 304–327 (1950).
[PubMed]

Akkin, T.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

T. Akkin, “Biomedical applications of a fiber based low-coherence interferometer for quantitative differential phase measurements,” Dissertation: The University of Texas at Austin, Austin, (2003).

Badizadegan, K.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Boppart, S. A.

Born, M.

M. Born and E. Wolf, Principles of Optics, 7th (expended) ed. (Cambridge University Press, Cambridge, UK, 1999) pp. 837–840.

Bouma, B. E.

Bryant, S. H.

S. H. Bryant and J. M. Tobias, “Optical and mechanical concomitants of activity in carcinus nerve I. Effect of sodium azide on the optical response II. Shortening of the nerve with activity,” J. Cell. Comp. Physiol. 46, 71–95 (1955).
[Crossref]

Byrne, P. M.

I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophysical J. 57, 633–635 (1990).
[Crossref]

I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
[Crossref]

Chu, M.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Cohen, L. B.

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
[PubMed]

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).

L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).

Dasari, R. R.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Davé, D. P.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

Fang-Yen, C.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Feld, M. S.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Fujimoto, J. G.

George, J. S.

Gillette, R.

Hill, B. C.

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

Hill, D. K.

D. K. Hill, “The volume change resulting from stimulation of a giant nerve fibre,” J. Physiol. 111, 304–327 (1950).
[PubMed]

Hille, B.

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).

L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).

Homma, R.

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

Iwasa, K.

K. Iwasa and I. Tasaki, “Mechanical changes in squid giant axons associated with production of action potentials,” Biochem. Biophysic. Res. Comm. 95, 1328–1331 (1980).
[Crossref]

Kadono, H.

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

Keynes, R. D.

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).

L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).

Kusano, K.

I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
[Crossref]

Lazebnik, M.

Maheswari, R. U.

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

Marks, D. L.

Michelson, R. P.

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

Milner, T. E.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

Nokes, M. A.

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

Potgieter, K.

Rector, D. M.

Rylander III, H. G.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

Schubert, E. D.

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

Seung, H. S.

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

Takaoka, H.

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

Tanifuji, M.

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

Tasaki, I.

I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophysical J. 57, 633–635 (1990).
[Crossref]

I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
[Crossref]

K. Iwasa and I. Tasaki, “Mechanical changes in squid giant axons associated with production of action potentials,” Biochem. Biophysic. Res. Comm. 95, 1328–1331 (1980).
[Crossref]

Tearney, G. J.

Telenkov, S. A.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

Tobias, J. M.

S. H. Bryant and J. M. Tobias, “Optical and mechanical concomitants of activity in carcinus nerve I. Effect of sodium azide on the optical response II. Shortening of the nerve with activity,” J. Cell. Comp. Physiol. 46, 71–95 (1955).
[Crossref]

von Muralt, A.

A. von Muralt, “The optical spike,” Phil. Trans. B270, 411–42 (1975).

Wolf, E.

M. Born and E. Wolf, Principles of Optics, 7th (expended) ed. (Cambridge University Press, Cambridge, UK, 1999) pp. 837–840.

Yao, X.

Youn, J.

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

Appl. Opt. (1)

Biochem. Biophysic. Res. Comm. (1)

K. Iwasa and I. Tasaki, “Mechanical changes in squid giant axons associated with production of action potentials,” Biochem. Biophysic. Res. Comm. 95, 1328–1331 (1980).
[Crossref]

Biophysical J. (2)

I. Tasaki, K. Kusano, and P. M. Byrne, “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse,” Biophysical J. 55, 1033–1040 (1989).
[Crossref]

I. Tasaki and P. M. Byrne, “Volume expansion of nonmyelinated nerve fibers during impulse conduction,” Biophysical J. 57, 633–635 (1990).
[Crossref]

J. Cell. Comp. Physiol. (1)

S. H. Bryant and J. M. Tobias, “Optical and mechanical concomitants of activity in carcinus nerve I. Effect of sodium azide on the optical response II. Shortening of the nerve with activity,” J. Cell. Comp. Physiol. 46, 71–95 (1955).
[Crossref]

J. Neuroscience Methods (1)

R. U. Maheswari, H. Takaoka, H. Kadono, R. Homma, and M. Tanifuji, “Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo,” J. Neuroscience Methods 124, 83–92 (2003).
[Crossref]

J. of Physiology (1)

L. B. Cohen, B. Hille, and R. D. Keynes, “Light scattering and birefringence changes during activity in the electric organ of electrophorus,” J. of Physiology 203, 489–509 (1969).

J. Physiol. (1)

D. K. Hill, “The volume change resulting from stimulation of a giant nerve fibre,” J. Physiol. 111, 304–327 (1950).
[PubMed]

J. Physiology (1)

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiology 211, 495–515 (1970).

Lasers in Surg Med. (1)

T. Akkin, D. P. Davé, J. Youn, S. A. Telenkov, H. G. Rylander III, and T. E. Milner, “Imaging tissue response to electrical and photothermal stimulation with nanometer sensitivity,” Lasers in Surg Med. 33, 219–225 (2003).
[Crossref]

Opt. Commun. (1)

D. P. Davé, T. Akkin, T. E. Milner, and H. G. Rylander III, “Phase-sensitive frequency-multiplexed optical low-coherence reflectometry,” Opt. Commun. 193, 39–43 (2001).
[Crossref]

Opt. Lett. (2)

Phil. Trans. (1)

A. von Muralt, “The optical spike,” Phil. Trans. B270, 411–42 (1975).

Physiol. Rev. (1)

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
[PubMed]

Science (1)

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196, 426–428 (1977).
[Crossref] [PubMed]

Other (3)

T. Akkin, “Biomedical applications of a fiber based low-coherence interferometer for quantitative differential phase measurements,” Dissertation: The University of Texas at Austin, Austin, (2003).

C. Fang-Yen, M. Chu, H. S. Seung, K. Badizadegan, R. R. Dasari, and M. S. Feld, “Neural interferometry: first non-contact measurements of action potential-induced nerve swelling,” in Biomedical Topical Meetings on CD-ROM (The Optical Society of America, Washington, DC, 2004), WE6.

M. Born and E. Wolf, Principles of Optics, 7th (expended) ed. (Cambridge University Press, Cambridge, UK, 1999) pp. 837–840.

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Figures (6)

Fig. 1.
Fig. 1.

Phase Sensitive Optical Low Coherence Reflectometer (PS-OLCR). A/D-analog to digital converter, C-collimator, D-photo-receiver, G-diffraction grating, L-lens, M-mirror, W-Wollaston prism.

Fig. 2.
Fig. 2.

Electrical and optical readouts from the nerve chamber. Double-sided arrows indicate the orthogonal polarization channels of PS-OLCR.

Fig. 3.
Fig. 3.

Optical path length change due to surface displacement of a stimulated crayfish leg nerve. Stimulus (300 µA, 50 µs) is at 2 ms. (a) and (b) are recorded from spatially close (<1 mm), but different points on the nerve. 500 responses are averaged in each trace.

Fig. 4.
Fig. 4.

Optical path length change due to surface displacement of a stimulated crayfish leg nerve. Stimulus (300 µA, 50 µs) is at 2 ms. (a) and (b) are recorded from top surface and 15 µm below the top surface, respectively. 250 responses are averaged in each trace.

Fig. 5.
Fig. 5.

Control experiment of surface displacement with stimulus amplitude below and above the action potential threshold. Stimulus duration is 50 µs and presented at 2 ms. (a) and (c) with stimulus amplitude of 60 µA, and (b) and (d) with stimulus amplitude of 100 µA. 100 responses are averaged in each trace.

Fig. 6.
Fig. 6.

Histology (trichrome staining) of a crayfish walking leg nerve.

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