Abstract

Intrinsic optical properties, such as optical birefringence, may serve as a tool for minimally invasive neuroimaging methods with high spatiotemporal resolution to aid in the study of neuronal activation patterns. To facilitate imaging neuronal activity by sensing dynamic birefringence, temporal characteristics behind the signal must be better understood. We have developed a novel nerve chamber to investigate changes in birefringence at the stimulation site, and at distances ~4-28 mm from that site. Using crustacean nerves with either heterogeneous or homogeneous size distributions of axon diameters, we found that the gradual (slow) recovery of the crossed-polarized signal is not explained by the arrival times of action potentials in smaller axons. Through studying the effects of stimulating current and voltage pulses, we hypothesize that the recovery may be caused by a capacitive-like coupling between firing axons and adjacent tissue structures, and we report data consistent with this hypothesis. This study will aid in the utilization of action-potential-related changes in birefringence to study fast changes in neuronal network activity.

© 2015 Optical Society of America

Full Article  |  PDF Article
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References

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2011 (2)

D. Debanne, E. Campanac, A. Bialowas, E. Carlier, and G. Alcaraz, “Axon physiology,” Physiol. Rev. 91(2), 555–602 (2011).
[Crossref] [PubMed]

J. P. Dreier, “The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease,” Nat. Med. 17(4), 439–447 (2011).
[Crossref] [PubMed]

2010 (1)

C. W. Shuttleworth, “Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation,” Neurochem. Int. 56(3), 379–386 (2010).
[Crossref] [PubMed]

2009 (1)

J. S. Liu and C. L. Passaglia, “Using the horseshoe crab, Limulus Polyphemus, in vision research,” J. Vis. Exp. 29, 1384 (2009).
[PubMed]

2008 (2)

A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
[Crossref] [PubMed]

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
[Crossref] [PubMed]

2007 (1)

A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145(3), 887–899 (2007).
[Crossref] [PubMed]

2006 (1)

B.-A. Battelle, “The eyes of Limulus polyphemus (Xiphosura, Chelicerata) and their afferent and efferent projections,” Arthropod Struct. Dev. 35(4), 261–274 (2006).
[Crossref] [PubMed]

2005 (5)

C. R. Butson and C. C. McIntyre, “Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation,” Clin. Neurophysiol. 116(10), 2490–2500 (2005).
[Crossref] [PubMed]

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
[Crossref] [PubMed]

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

K. L. Briggman, H. D. I. Abarbanel, and W. B. Kristan., “Optical imaging of neuronal populations during decision-making,” Science 307(5711), 896–901 (2005).
[Crossref] [PubMed]

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

2004 (3)

N. K. Logothetis and J. Pfeuffer, “On the nature of the BOLD fMRI contrast mechanism,” Magn. Reson. Imaging 22(10), 1517–1531 (2004).
[Crossref] [PubMed]

A. Grinvald and R. Hildesheim, “VSDI: a new era in functional imaging of cortical dynamics,” Nat. Rev. Neurosci. 5(11), 874–885 (2004).
[Crossref] [PubMed]

K. M. Carter, J. S. George, and D. M. Rector, “Simultaneous birefringence and scattered light measurements reveal anatomical features in isolated crustacean nerve,” J. Neurosci. Methods 135(1-2), 9–16 (2004).
[Crossref] [PubMed]

2003 (2)

X.-C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
[Crossref] [PubMed]

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
[Crossref] [PubMed]

2002 (1)

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

1999 (1)

D. Smetters, A. Majewska, and R. Yuste, “Detecting action potentials in neuronal populations with calcium imaging,” Methods 18(2), 215–221 (1999).
[Crossref] [PubMed]

1993 (1)

I. Tasaki and P. M. Byrne, “The origin of rapid changes in birefringence, light scattering and dye absorbance associated with excitation of nerve fibers,” Jpn. J. Physiol. 43(Suppl 1), S67–S75 (1993).
[PubMed]

1991 (2)

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
[Crossref] [PubMed]

B. A. MacVicar and D. Hochman, “Imaging of synaptically evoked intrinsic optical signals in hippocampal slices,” J. Neurosci. 11(5), 1458–1469 (1991).
[PubMed]

1989 (1)

K. R. Foster and H. P. Schwan, “Dielectric properties of tissues and biological materials: a critical review,” Crit. Rev. Biomed. Eng. 17(1), 25–104 (1989).
[PubMed]

1985 (1)

D. Landowne, “Molecular motion underlying activation and inactivation of sodium channels in squid giant axons,” J. Membr. Biol. 88(2), 173–185 (1985).
[Crossref] [PubMed]

1977 (1)

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

1975 (1)

W. H. Fahrenbach, “The visual system of the horseshoe crab Limulus polyphemus,” Int. Rev. Cytol. 41, 285–349 (1975).
[Crossref] [PubMed]

1973 (1)

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53(2), 373–418 (1973).
[PubMed]

1971 (2)

L. B. Cohen, B. Hille, R. D. Keynes, D. Landowne, and E. Rojas, “Analysis of the potential-dependent changes in optical retardation in the squid giant axon,” J. Physiol. 218(1), 205–237 (1971).
[Crossref] [PubMed]

L. B. Cohen and R. D. Keynes, “Changes in light scattering associated with the action potential in crab nerves,” J. Physiol. 212(1), 259–275 (1971).
[Crossref] [PubMed]

1970 (1)

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiol. 211(2), 495–515 (1970).
[Crossref] [PubMed]

1969 (1)

L. B. Cohen, B. Hille, R. D. Keynes, and R. Cohen, “Light scattering and birefringence changes during activity in the electric organ of Electrophorus electricus,” J. Physiol. 203(2), 489–509 (1969).
[Crossref] [PubMed]

1968 (2)

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Natl. Acad. Sci. U.S.A. 61(3), 883–888 (1968).
[Crossref] [PubMed]

A. J. De Lorenzo, M. Brzin, and W. D. Dettbarn, “Fine structure and organization of nerve fibers and giant axons in Homarus americanus,” J. Ultrastruct. Res. 24(5), 367–384 (1968).
[Crossref] [PubMed]

1954 (1)

A. L. Hodgkin, “A note on conduction velocity,” J. Physiol. 125(1), 221–224 (1954).
[Crossref] [PubMed]

1929 (1)

K. Furusawa, “The depolarization of crustacean nerve by stimulation or oxygen want,” J. Physiol. 67(4), 325–342 (1929).
[Crossref] [PubMed]

Abarbanel, H. D. I.

K. L. Briggman, H. D. I. Abarbanel, and W. B. Kristan., “Optical imaging of neuronal populations during decision-making,” Science 307(5711), 896–901 (2005).
[Crossref] [PubMed]

Alcaraz, G.

D. Debanne, E. Campanac, A. Bialowas, E. Carlier, and G. Alcaraz, “Axon physiology,” Physiol. Rev. 91(2), 555–602 (2011).
[Crossref] [PubMed]

Ba, A. M.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Barrowes, B.

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
[Crossref] [PubMed]

Barthó, P.

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
[Crossref] [PubMed]

Battelle, B.-A.

B.-A. Battelle, “The eyes of Limulus polyphemus (Xiphosura, Chelicerata) and their afferent and efferent projections,” Arthropod Struct. Dev. 35(4), 261–274 (2006).
[Crossref] [PubMed]

Bialowas, A.

D. Debanne, E. Campanac, A. Bialowas, E. Carlier, and G. Alcaraz, “Axon physiology,” Physiol. Rev. 91(2), 555–602 (2011).
[Crossref] [PubMed]

Blonder, G. E.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
[Crossref] [PubMed]

Brázdil, M.

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Briggman, K. L.

K. L. Briggman, H. D. I. Abarbanel, and W. B. Kristan., “Optical imaging of neuronal populations during decision-making,” Science 307(5711), 896–901 (2005).
[Crossref] [PubMed]

Brzin, M.

A. J. De Lorenzo, M. Brzin, and W. D. Dettbarn, “Fine structure and organization of nerve fibers and giant axons in Homarus americanus,” J. Ultrastruct. Res. 24(5), 367–384 (1968).
[Crossref] [PubMed]

Butson, C. R.

C. R. Butson and C. C. McIntyre, “Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation,” Clin. Neurophysiol. 116(10), 2490–2500 (2005).
[Crossref] [PubMed]

Buzsáki, G.

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
[Crossref] [PubMed]

Byrne, P. M.

I. Tasaki and P. M. Byrne, “The origin of rapid changes in birefringence, light scattering and dye absorbance associated with excitation of nerve fibers,” Jpn. J. Physiol. 43(Suppl 1), S67–S75 (1993).
[PubMed]

Campanac, E.

D. Debanne, E. Campanac, A. Bialowas, E. Carlier, and G. Alcaraz, “Axon physiology,” Physiol. Rev. 91(2), 555–602 (2011).
[Crossref] [PubMed]

Cannestra, A. F.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Carlier, E.

D. Debanne, E. Campanac, A. Bialowas, E. Carlier, and G. Alcaraz, “Axon physiology,” Physiol. Rev. 91(2), 555–602 (2011).
[Crossref] [PubMed]

Carnay, L.

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Natl. Acad. Sci. U.S.A. 61(3), 883–888 (1968).
[Crossref] [PubMed]

Carter, K. M.

K. M. Carter, J. S. George, and D. M. Rector, “Simultaneous birefringence and scattered light measurements reveal anatomical features in isolated crustacean nerve,” J. Neurosci. Methods 135(1-2), 9–16 (2004).
[Crossref] [PubMed]

Chen, J. W. Y.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Chlebus, P.

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Cohen, L. B.

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53(2), 373–418 (1973).
[PubMed]

L. B. Cohen, B. Hille, R. D. Keynes, D. Landowne, and E. Rojas, “Analysis of the potential-dependent changes in optical retardation in the squid giant axon,” J. Physiol. 218(1), 205–237 (1971).
[Crossref] [PubMed]

L. B. Cohen and R. D. Keynes, “Changes in light scattering associated with the action potential in crab nerves,” J. Physiol. 212(1), 259–275 (1971).
[Crossref] [PubMed]

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiol. 211(2), 495–515 (1970).
[Crossref] [PubMed]

L. B. Cohen, B. Hille, R. D. Keynes, and R. Cohen, “Light scattering and birefringence changes during activity in the electric organ of Electrophorus electricus,” J. Physiol. 203(2), 489–509 (1969).
[Crossref] [PubMed]

Cohen, R.

L. B. Cohen, B. Hille, R. D. Keynes, and R. Cohen, “Light scattering and birefringence changes during activity in the electric organ of Electrophorus electricus,” J. Physiol. 203(2), 489–509 (1969).
[Crossref] [PubMed]

Csicsvari, J.

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
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W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
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W. H. Fahrenbach, “The visual system of the horseshoe crab Limulus polyphemus,” Int. Rev. Cytol. 41, 285–349 (1975).
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A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
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Foster, K. R.

K. R. Foster and H. P. Schwan, “Dielectric properties of tissues and biological materials: a critical review,” Crit. Rev. Biomed. Eng. 17(1), 25–104 (1989).
[PubMed]

Foust, A.

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
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Foust, A. J.

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
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A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
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A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145(3), 887–899 (2007).
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X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
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K. M. Carter, J. S. George, and D. M. Rector, “Simultaneous birefringence and scattered light measurements reveal anatomical features in isolated crustacean nerve,” J. Neurosci. Methods 135(1-2), 9–16 (2004).
[Crossref] [PubMed]

X.-C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
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W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
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A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
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A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
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J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
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J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
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A. Grinvald and R. Hildesheim, “VSDI: a new era in functional imaging of cortical dynamics,” Nat. Rev. Neurosci. 5(11), 874–885 (2004).
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L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiol. 211(2), 495–515 (1970).
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L. B. Cohen, B. Hille, R. D. Keynes, D. Landowne, and E. Rojas, “Analysis of the potential-dependent changes in optical retardation in the squid giant axon,” J. Physiol. 218(1), 205–237 (1971).
[Crossref] [PubMed]

L. B. Cohen, B. Hille, and R. D. Keynes, “Changes in axon birefringence during the action potential,” J. Physiol. 211(2), 495–515 (1970).
[Crossref] [PubMed]

L. B. Cohen, B. Hille, R. D. Keynes, and R. Cohen, “Light scattering and birefringence changes during activity in the electric organ of Electrophorus electricus,” J. Physiol. 203(2), 489–509 (1969).
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Kleinfeld, D.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
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K. L. Briggman, H. D. I. Abarbanel, and W. B. Kristan., “Optical imaging of neuronal populations during decision-making,” Science 307(5711), 896–901 (2005).
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M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
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D. Landowne, “Molecular motion underlying activation and inactivation of sodium channels in squid giant axons,” J. Membr. Biol. 88(2), 173–185 (1985).
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L. B. Cohen, B. Hille, R. D. Keynes, D. Landowne, and E. Rojas, “Analysis of the potential-dependent changes in optical retardation in the squid giant axon,” J. Physiol. 218(1), 205–237 (1971).
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LaPorta, A.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
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J. S. Liu and C. L. Passaglia, “Using the horseshoe crab, Limulus Polyphemus, in vision research,” J. Vis. Exp. 29, 1384 (2009).
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N. K. Logothetis and J. Pfeuffer, “On the nature of the BOLD fMRI contrast mechanism,” Magn. Reson. Imaging 22(10), 1517–1531 (2004).
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Luft, A. R.

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

Macko, R. F.

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

MacVicar, B. A.

B. A. MacVicar and D. Hochman, “Imaging of synaptically evoked intrinsic optical signals in hippocampal slices,” J. Neurosci. 11(5), 1458–1469 (1991).
[PubMed]

Majewska, A.

D. Smetters, A. Majewska, and R. Yuste, “Detecting action potentials in neuronal populations with calcium imaging,” Methods 18(2), 215–221 (1999).
[Crossref] [PubMed]

McCluskey, M. D.

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
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McCombe-Waller, S.

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

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C. R. Butson and C. C. McIntyre, “Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation,” Clin. Neurophysiol. 116(10), 2490–2500 (2005).
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Mikl, M.

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Muthialu, A.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Passaglia, C. L.

J. S. Liu and C. L. Passaglia, “Using the horseshoe crab, Limulus Polyphemus, in vision research,” J. Vis. Exp. 29, 1384 (2009).
[PubMed]

Pazourková, M.

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Pfeuffer, J.

N. K. Logothetis and J. Pfeuffer, “On the nature of the BOLD fMRI contrast mechanism,” Magn. Reson. Imaging 22(10), 1517–1531 (2004).
[Crossref] [PubMed]

Pouratian, N.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Raccuia-Behling, F.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
[Crossref] [PubMed]

Rector, D. M.

A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
[Crossref] [PubMed]

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
[Crossref] [PubMed]

A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145(3), 887–899 (2007).
[Crossref] [PubMed]

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
[Crossref] [PubMed]

K. M. Carter, J. S. George, and D. M. Rector, “Simultaneous birefringence and scattered light measurements reveal anatomical features in isolated crustacean nerve,” J. Neurosci. Methods 135(1-2), 9–16 (2004).
[Crossref] [PubMed]

X.-C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
[Crossref] [PubMed]

Rektor, I.

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Rex, D. E.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

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L. B. Cohen, B. Hille, R. D. Keynes, D. Landowne, and E. Rojas, “Analysis of the potential-dependent changes in optical retardation in the squid giant axon,” J. Physiol. 218(1), 205–237 (1971).
[Crossref] [PubMed]

Rojas, M. J.

A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
[Crossref] [PubMed]

Ross, W. N.

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

Salzberg, B. M.

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

Sandlin, R.

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Natl. Acad. Sci. U.S.A. 61(3), 883–888 (1968).
[Crossref] [PubMed]

Schei, J. L.

A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
[Crossref] [PubMed]

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
[Crossref] [PubMed]

Schwan, H. P.

K. R. Foster and H. P. Schwan, “Dielectric properties of tissues and biological materials: a critical review,” Crit. Rev. Biomed. Eng. 17(1), 25–104 (1989).
[PubMed]

Shuttleworth, C. W.

C. W. Shuttleworth, “Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation,” Neurochem. Int. 56(3), 379–386 (2010).
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Sirota, A.

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
[Crossref] [PubMed]

Slusher, R. E.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
[Crossref] [PubMed]

Smetters, D.

D. Smetters, A. Majewska, and R. Yuste, “Detecting action potentials in neuronal populations with calcium imaging,” Methods 18(2), 215–221 (1999).
[Crossref] [PubMed]

Stepnoski, R. A.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A. 88(21), 9382–9386 (1991).
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I. Tasaki and P. M. Byrne, “The origin of rapid changes in birefringence, light scattering and dye absorbance associated with excitation of nerve fibers,” Jpn. J. Physiol. 43(Suppl 1), S67–S75 (1993).
[PubMed]

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Natl. Acad. Sci. U.S.A. 61(3), 883–888 (1968).
[Crossref] [PubMed]

Toga, A. W.

A. M. Ba, M. Guiou, N. Pouratian, A. Muthialu, D. E. Rex, A. F. Cannestra, J. W. Y. Chen, and A. W. Toga, “Multiwavelength optical intrinsic signal imaging of cortical spreading depression,” J. Neurophysiol. 88(5), 2726–2735 (2002).
[Crossref] [PubMed]

Villagra, F.

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

Waggoner, A. S.

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

Wang, C. H.

W. N. Ross, B. M. Salzberg, L. B. Cohen, A. Grinvald, H. V. Davila, A. S. Waggoner, and C. H. Wang, “Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential,” J. Membr. Biol. 33(1-2), 141–183 (1977).
[Crossref] [PubMed]

Watanabe, A.

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Natl. Acad. Sci. U.S.A. 61(3), 883–888 (1968).
[Crossref] [PubMed]

Whitall, J.

A. R. Luft, L. Forrester, R. F. Macko, S. McCombe-Waller, J. Whitall, F. Villagra, and D. F. Hanley, “Brain activation of lower extremity movement in chronically impaired stroke survivors,” Neuroimage 26(1), 184–194 (2005).
[Crossref] [PubMed]

Wise, K. D.

J. Csicsvari, D. A. Henze, B. Jamieson, K. D. Harris, A. Sirota, P. Barthó, K. D. Wise, and G. Buzsáki, “Massively parallel recording of unit and local field potentials with silicon-based electrodes,” J. Neurophysiol. 90(2), 1314–1323 (2003).
[Crossref] [PubMed]

Yao, X.-C.

J. L. Schei, M. D. McCluskey, A. J. Foust, X.-C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40(3), 1034–1043 (2008).
[Crossref] [PubMed]

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
[Crossref] [PubMed]

X.-C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
[Crossref] [PubMed]

Yuste, R.

D. Smetters, A. Majewska, and R. Yuste, “Detecting action potentials in neuronal populations with calcium imaging,” Methods 18(2), 215–221 (1999).
[Crossref] [PubMed]

Appl. Opt. (1)

Arthropod Struct. Dev. (1)

B.-A. Battelle, “The eyes of Limulus polyphemus (Xiphosura, Chelicerata) and their afferent and efferent projections,” Arthropod Struct. Dev. 35(4), 261–274 (2006).
[Crossref] [PubMed]

Biophys. J. (1)

X.-C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88(6), 4170–4177 (2005).
[Crossref] [PubMed]

Clin. Neurophysiol. (1)

C. R. Butson and C. C. McIntyre, “Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation,” Clin. Neurophysiol. 116(10), 2490–2500 (2005).
[Crossref] [PubMed]

Crit. Rev. Biomed. Eng. (1)

K. R. Foster and H. P. Schwan, “Dielectric properties of tissues and biological materials: a critical review,” Crit. Rev. Biomed. Eng. 17(1), 25–104 (1989).
[PubMed]

Eur. J. Neurol. (1)

M. Brázdil, P. Chlebus, M. Mikl, M. Pazourková, P. Krupa, and I. Rektor, “Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study,” Eur. J. Neurol. 12(4), 268–275 (2005).
[Crossref] [PubMed]

Int. Rev. Cytol. (1)

W. H. Fahrenbach, “The visual system of the horseshoe crab Limulus polyphemus,” Int. Rev. Cytol. 41, 285–349 (1975).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

A. J. Foust, J. L. Schei, M. J. Rojas, and D. M. Rector, “In vitro and in vivo noise analysis for optical neural recording,” J. Biomed. Opt. 13(4), 044038 (2008).
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Figures (5)

Fig. 1
Fig. 1

A) Diagram of the optical components and readout. B) An expanded depiction of the custom-built nerve chamber with quartz top and bottom in all wells. The chamber was divided into wells that are electrically isolated, except through the nerve. Blackened petroleum jelly was used to electrically insulate the areas around the nerve between each well. An example of the illumination area on the nerve in a typical experiment is shown, at ~12 mm from the positive stimulus well.

Fig. 2
Fig. 2

A) Crossed-polarizer signal (XPS) for the lobster walking leg nerve (WLN) from a 1-ms, 1-mA stimulus pulse, measured at the negative stimulus electrode (origin of APs) as well as at 6 mm, 12 mm and 24 mm from the site of stimulation. The XPS peak decreases in magnitude and widens in time as a function of distance. Four phases are noted: a slow onset, a fast onset, a fast recovery of the peak, and a gradual recovery to baseline. The gradual recovery takes ~300-400 ms to return fully to baseline (not shown). B) The same data is temporally shifted to match the start of the onset of the XPSs to compare the onset and recovery times. The gradual recovery is similar for any distance from the stimulus, but is different at the stimulus site. C) Computational model of the compound XPS for the WLN as a function of distance. Both onset phases and the fast recovery phase can be reproduced, but the gradual recovery cannot. D) The electrical recording matches the peak width and recovery time of the XPS measured at the electrical recording site (~24 mm from the site of stimulation). AP activity is detected until the start of the gradual recovery of the XPS.

Fig. 3
Fig. 3

A) Horseshoe crab lateral optic nerve (LON) XPS measured at a distance ~12 mm from the stimulus site, overlaid with the lobster WLN XPS at the same location. The signal spreads with propagation distance for the heterogeneous WLN, but the same is not true for the homogeneous LON. The gradual recovery phase happens from above baseline for the LON and below baseline for the WLN. B) The corresponding electrical recording for the LON is time-adjusted and plotted over the peak of the XPS from Fig. 3(A) to show that this narrow optical peak can be explained by the concurrent arrivals of APs. The filter was set to remove frequencies below 300 Hz, allowing only for the detection of APs. As for the WLN, the gradual recovery of the XPS for the LON cannot be explained by the presence of APs.

Fig. 4
Fig. 4

A) The XPS in the positive and negative stimulus wells with a 1-ms, 1-mA stimulus pulse in a live nerve shows an immediate peak correlated with the stimulus pulse followed by a standard shape associated with normal AP activity. B) A 10-mA stimulus pulse in a live nerve causes the XPS to recover from above baseline instead of below. C) The dead nerve XPS for a 1-mA stimulus is much smaller than for the live nerve, but is still present. D) For a 10-mA stimulus on a dead nerve, the XPS onset is an order of magnitude larger than for a 1-mA stimulus, and the gradual recovery is significantly longer (>2x).

Fig. 5
Fig. 5

A) Example of a stimulus used in the experiment. 1V and −1V, 128-ms square voltage pulses were applied to nerve, and the XPS and stimulus voltage traces are shown together. The birefringence signal closely follows the applied electric field, with time constants of 14 ms rising and 19 ms falling. B) The XPS demonstrates a positive, linear relationship (shown here with a linear fit) to the amplitude of an applied voltage stimulus in the range −2 V to 2 V (data is normalized to the XPS at 100 mV for each nerve, n = 5). The signal saturates beyond that range, possibly related to limitations in the availability of the physiological structures causing changes in birefringence.

Equations (2)

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XP S axon =rXPS T w ( 5[ mm ms ] d[ μm ] 100μm )
Ψ=kΦ( d,μ,σ ){ k=0.5μm, μ=1.2μm, σ=5μm, 0.1μm<d<5μm k=0.25μm, μ=26.7μm, σ=8μm, 20μm<d<30μm k=0.25μm, μ=67μm, σ=10μm, 50μm<d<100μm }

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