Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 May 10;91(10):4604–4608. doi: 10.1073/pnas.91.10.4604

Cable properties of a straight neurite of a leech neuron probed by a voltage-sensitive dye.

P Fromherz 1, C O Müller 1
PMCID: PMC43834  PMID: 8183956

Abstract

We measured a time-resolved map of electrical activity in a thin straight neurite (1.5 microns thick, 500 microns long) at a resolution of 8 microns and 0.4 ms. The neurite was obtained by guided outgrowth of an identified neuron of the leech on lanes of extracellular matrix protein. The electrical signals were detected by a fluorescent voltage-sensitive dye. We observed the voltage that was caused by an action potential elicited at the soma and by a Gaussian hyperpolarization induced at the soma, respectively. We compared the data with numerical solutions of the cable equation using the Hodgkin-Huxley parametrization. We could attribute the experimental results of depolarization and of hyperpolarization to the propagation of an action potential along an "active" cable and to the spread along a "passive" cable, respectively, if we assigned rather high specific resistances to the cytoplasm (RI = 250 omega.cm) and to the membrane (RM = 22 k omega.cm2). This assignment explained the slow velocity of 150 microns/ms of a pulse by active propagation and the limited range of 200 microns of a pulse by passive spread.

Full text

PDF
4604

Images in this article

4605Image
on p.4605
4606Image
on p.4606
4606Image
on p.4606
4607Image
on p.4607

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Chien C. B., Pine J. Voltage-sensitive dye recording of action potentials and synaptic potentials from sympathetic microcultures. Biophys J. 1991 Sep;60(3):697–711. doi: 10.1016/S0006-3495(91)82099-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chiquet M., Masuda-Nakagawa L., Beck K. Attachment to an endogenous laminin-like protein initiates sprouting by leech neurons. J Cell Biol. 1988 Sep;107(3):1189–1198. doi: 10.1083/jcb.107.3.1189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cohen L. B., Lesher S. Optical monitoring of membrane potential: methods of multisite optical measurement. Soc Gen Physiol Ser. 1986;40:71–99. [PubMed] [Google Scholar]
  4. Dietzel I. D., Drapeau P., Nicholls J. G. Voltage dependence of 5-hydroxytryptamine release at a synapse between identified leech neurones in culture. J Physiol. 1986 Mar;372:191–205. doi: 10.1113/jphysiol.1986.sp016004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fleshman J. W., Segev I., Burke R. B. Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. J Neurophysiol. 1988 Jul;60(1):60–85. doi: 10.1152/jn.1988.60.1.60. [DOI] [PubMed] [Google Scholar]
  6. Fromherz P., Gaede V. Exclusive-OR function of single arborized neuron. Biol Cybern. 1993;69(4):337–344. doi: 10.1007/BF00203130. [DOI] [PubMed] [Google Scholar]
  7. Fromherz P., Müller C. O. Voltage-sensitive fluorescence of amphiphilic hemicyanine dyes in neuron membrane. Biochim Biophys Acta. 1993 Aug 15;1150(2):111–122. doi: 10.1016/0005-2736(93)90079-f. [DOI] [PubMed] [Google Scholar]
  8. Fromherz P., Schaden H., Vetter T. Guided outgrowth of leech neurons in culture. Neurosci Lett. 1991 Aug 5;129(1):77–80. doi: 10.1016/0304-3940(91)90724-8. [DOI] [PubMed] [Google Scholar]
  9. Fromherz P., Vetter T. Cable properties of arborized Retzius cells of the leech in culture as probed by a voltage-sensitive dye. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2041–2045. doi: 10.1073/pnas.89.6.2041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fromherz P., Vetter T. Propagation of voltage transients in arborized neurites of Retzius cells of the leech in culture. Z Naturforsch C. 1991 Jul-Aug;46(7-8):687–696. doi: 10.1515/znc-1991-7-828. [DOI] [PubMed] [Google Scholar]
  11. Grinvald A., Fine A., Farber I. C., Hildesheim R. Fluorescence monitoring of electrical responses from small neurons and their processes. Biophys J. 1983 May;42(2):195–198. doi: 10.1016/S0006-3495(83)84386-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grinvald A., Frostig R. D., Lieke E., Hildesheim R. Optical imaging of neuronal activity. Physiol Rev. 1988 Oct;68(4):1285–1366. doi: 10.1152/physrev.1988.68.4.1285. [DOI] [PubMed] [Google Scholar]
  13. Grinvald A., Ross W. N., Farber I. Simultaneous optical measurements of electrical activity from multiple sites on processes of cultured neurons. Proc Natl Acad Sci U S A. 1981 May;78(5):3245–3249. doi: 10.1073/pnas.78.5.3245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gross D., Loew L. M., Webb W. W. Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys J. 1986 Aug;50(2):339–348. doi: 10.1016/S0006-3495(86)83467-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hounsgaard J., Midtgaard J. Dendrite processing in more ways than one . Trends Neurosci. 1989 Sep;12(9):313–315. doi: 10.1016/0166-2236(89)90036-2. [DOI] [PubMed] [Google Scholar]
  17. Johansen J., Kleinhaus A. L. Differential sensitivity of tetrodotoxin of nociceptive neurons in 4 species of leeches. J Neurosci. 1986 Dec;6(12):3499–3504. doi: 10.1523/JNEUROSCI.06-12-03499.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kleinhaus A. L., Prichard J. W. Differential action of tetrodotoxin on identified leech neurons. Comp Biochem Physiol C. 1983;74(1):211–218. doi: 10.1016/0742-8413(83)90176-7. [DOI] [PubMed] [Google Scholar]
  19. Koch C., Poggio T., Torre V. Retinal ganglion cells: a functional interpretation of dendritic morphology. Philos Trans R Soc Lond B Biol Sci. 1982 Jul 27;298(1090):227–263. doi: 10.1098/rstb.1982.0084. [DOI] [PubMed] [Google Scholar]
  20. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol. 1980 Aug;305:197–213. doi: 10.1113/jphysiol.1980.sp013358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nelson P. G., Lux H. D. Some electrical measurements of motoneuron parameters. Biophys J. 1970 Jan;10(1):55–73. doi: 10.1016/S0006-3495(70)86285-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Parsons T. D., Kleinfeld D., Raccuia-Behling F., Salzberg B. M. Optical recording of the electrical activity of synaptically interacting Aplysia neurons in culture using potentiometric probes. Biophys J. 1989 Jul;56(1):213–221. doi: 10.1016/S0006-3495(89)82666-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. RALL W. Membrane potential transients and membrane time constant of motoneurons. Exp Neurol. 1960 Oct;2:503–532. doi: 10.1016/0014-4886(60)90029-7. [DOI] [PubMed] [Google Scholar]
  24. Ross W. N., Arechiga H., Nicholls J. G. Optical recording of calcium and voltage transients following impulses in cell bodies and processes of identified leech neurons in culture. J Neurosci. 1987 Dec;7(12):3877–3887. doi: 10.1523/JNEUROSCI.07-12-03877.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ross W. N., Krauthamer V. Optical measurements of potential changes in axons and processes of neurons of a barnacle ganglion. J Neurosci. 1984 Mar;4(3):659–672. doi: 10.1523/JNEUROSCI.04-03-00659.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Salzberg B. M., Davila H. V., Cohen L. B. Optical recording of impulses in individual neurones of an invertebrate central nervous system. Nature. 1973 Dec 21;246(5434):508–509. doi: 10.1038/246508a0. [DOI] [PubMed] [Google Scholar]
  27. Senseman D. M., Horwitz I. S., Salzberg B. M. MSORTV imaging of electrotonic conduction in a syncitium: optical recording of polarization spread in a simple salivary gland. J Exp Zool. 1987 Oct;244(1):79–88. doi: 10.1002/jez.1402440110. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES