Direct measurement of specific membrane capacitance in neurons.
Journal: 2000/August - Biophysical Journal
ISSN: 0006-3495
Abstract:
The specific membrane capacitance (C(m)) of a neuron influences synaptic efficacy and determines the speed with which electrical signals propagate along dendrites and unmyelinated axons. The value of this important parameter remains controversial. In this study, C(m) was estimated for the somatic membrane of cortical pyramidal neurons, spinal cord neurons, and hippocampal neurons. A nucleated patch was pulled and a voltage-clamp step was applied. The exponential decay of the capacitative charging current was analyzed to give the total membrane capacitance, which was then divided by the observed surface area of the patch. C(m) was 0.9 microF/cm(2) for each class of neuron. To test the possibility that membrane proteins may alter C(m), embryonic kidney cells (HEK-293) were studied before and after transfection with a plasmid coding for glycine receptor/channels. The value of C(m) was indistinguishable in untransfected cells and in transfected cells expressing a high level of glycine channels, indicating that differences in transmembrane protein content do not significantly affect C(m). Thus, to a first approximation, C(m) may be treated as a "biological constant" across many classes of neuron.
Relations:
Content
Citations
(110)
References
(22)
Drugs
(1)
Chemicals
(2)
Organisms
(4)
Processes
(1)
Anatomy
(7)
Affiliates
(1)
Similar articles
Articles by the same authors
Discussion board
Biophys J 79(1): 314-320

Direct measurement of specific membrane capacitance in neurons.

Abstract

The specific membrane capacitance (C(m)) of a neuron influences synaptic efficacy and determines the speed with which electrical signals propagate along dendrites and unmyelinated axons. The value of this important parameter remains controversial. In this study, C(m) was estimated for the somatic membrane of cortical pyramidal neurons, spinal cord neurons, and hippocampal neurons. A nucleated patch was pulled and a voltage-clamp step was applied. The exponential decay of the capacitative charging current was analyzed to give the total membrane capacitance, which was then divided by the observed surface area of the patch. C(m) was 0.9 microF/cm(2) for each class of neuron. To test the possibility that membrane proteins may alter C(m), embryonic kidney cells (HEK-293) were studied before and after transfection with a plasmid coding for glycine receptor/channels. The value of C(m) was indistinguishable in untransfected cells and in transfected cells expressing a high level of glycine channels, indicating that differences in transmembrane protein content do not significantly affect C(m). Thus, to a first approximation, C(m) may be treated as a "biological constant" across many classes of neuron.

Full Text

The Full Text of this article is available as a PDF (187K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bekkers JM, Stevens CF. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7834–7838.[PMC free article] [PubMed] [Google Scholar]
  • Chitwood RA, Hubbard A, Jaffe DB. Passive electrotonic properties of rat hippocampal CA3 interneurones. J Physiol. 1999 Mar 15;515(Pt 3):743–756.[PMC free article] [PubMed] [Google Scholar]
  • Clements JD, Redman SJ. Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J Physiol. 1989 Feb;409:63–87.[PMC free article] [PubMed] [Google Scholar]
  • Fernández JM, Bezanilla F, Taylor RE. Distribution and kinetics of membrane dielectric polarization. II. Frequency domain studies of gating currents. J Gen Physiol. 1982 Jan;79(1):41–67.[PMC free article] [PubMed] [Google Scholar]
  • Furshpan EJ, Landis SC, Matsumoto SG, Potter DD. Synaptic functions in rat sympathetic neurons in microcultures. I. Secretion of norepinephrine and acetylcholine. J Neurosci. 1986 Apr;6(4):1061–1079.[PMC free article] [PubMed] [Google Scholar]
  • HODGKIN AL, HUXLEY AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544.[PMC free article] [PubMed] [Google Scholar]
  • Jurman ME, Boland LM, Liu Y, Yellen G. Visual identification of individual transfected cells for electrophysiology using antibody-coated beads. Biotechniques. 1994 Nov;17(5):876–881. [PubMed] [Google Scholar]
  • Legendre P. A reluctant gating mode of glycine receptor channels determines the time course of inhibitory miniature synaptic events in zebrafish hindbrain neurons. J Neurosci. 1998 Apr 15;18(8):2856–2870.[PMC free article] [PubMed] [Google Scholar]
  • Major G, Larkman AU, Jonas P, Sakmann B, Jack JJ. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci. 1994 Aug;14(8):4613–4638.[PMC free article] [PubMed] [Google Scholar]
  • Niles WD, Levis RA, Cohen FS. Planar bilayer membranes made from phospholipid monolayers form by a thinning process. Biophys J. 1988 Mar;53(3):327–335.[PMC free article] [PubMed] [Google Scholar]
  • Prakash YS, Smithson KG, Sieck GC. Measurements of motoneuron somal volumes using laser confocal microscopy: comparisons with shape-based stereological estimations. Neuroimage. 1993 Sep;1(2):95–107. [PubMed] [Google Scholar]
  • Rajendra S, Lynch JW, Pierce KD, French CR, Barry PH, Schofield PR. Startle disease mutations reduce the agonist sensitivity of the human inhibitory glycine receptor. J Biol Chem. 1994 Jul 22;269(29):18739–18742. [PubMed] [Google Scholar]
  • RALL W. Theory of physiological properties of dendrites. Ann N Y Acad Sci. 1962 Mar 2;96:1071–1092. [PubMed] [Google Scholar]
  • Solsona C, Innocenti B, Fernández JM. Regulation of exocytotic fusion by cell inflation. Biophys J. 1998 Feb;74(2 Pt 1):1061–1073.[PMC free article] [PubMed] [Google Scholar]
  • Sukhorukov VL, Arnold WM, Zimmermann U. Hypotonically induced changes in the plasma membrane of cultured mammalian cells. J Membr Biol. 1993 Feb;132(1):27–40. [PubMed] [Google Scholar]
  • Takahashi T, Momiyama A, Hirai K, Hishinuma F, Akagi H. Functional correlation of fetal and adult forms of glycine receptors with developmental changes in inhibitory synaptic receptor channels. Neuron. 1992 Dec;9(6):1155–1161. [PubMed] [Google Scholar]
  • Tapia JC, Aguayo LG. Changes in the properties of developing glycine receptors in cultured mouse spinal neurons. Synapse. 1998 Mar;28(3):185–194. [PubMed] [Google Scholar]
  • Thurbon D, Lüscher HR, Hofstetter T, Redman SJ. Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol. 1998 May;79(5):2485–2502. [PubMed] [Google Scholar]
  • Twyman RE, Macdonald RL. Kinetic properties of the glycine receptor main- and sub-conductance states of mouse spinal cord neurones in culture. J Physiol. 1991 Apr;435:303–331.[PMC free article] [PubMed] [Google Scholar]
  • Unwin N. Nicotinic acetylcholine receptor at 9 A resolution. J Mol Biol. 1993 Feb 20;229(4):1101–1124. [PubMed] [Google Scholar]
  • von Kitzing E, Soumpasis DM. Electrostatics of a simple membrane model using Green's functions formalism. Biophys J. 1996 Aug;71(2):795–810.[PMC free article] [PubMed] [Google Scholar]
  • Ye JH, Schaefer R, Wu WH, Liu PL, Zbuzek VK, Mcardle JJ. Inhibitory effect of ondansetron on glycine response of dissociated rat hippocampal neurons. J Pharmacol Exp Ther. 1999 Jul;290(1):104–111. [PubMed] [Google Scholar]
John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory 0200, Australia.
John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory 0200, Australia.

Abstract

The specific membrane capacitance (C(m)) of a neuron influences synaptic efficacy and determines the speed with which electrical signals propagate along dendrites and unmyelinated axons. The value of this important parameter remains controversial. In this study, C(m) was estimated for the somatic membrane of cortical pyramidal neurons, spinal cord neurons, and hippocampal neurons. A nucleated patch was pulled and a voltage-clamp step was applied. The exponential decay of the capacitative charging current was analyzed to give the total membrane capacitance, which was then divided by the observed surface area of the patch. C(m) was 0.9 microF/cm(2) for each class of neuron. To test the possibility that membrane proteins may alter C(m), embryonic kidney cells (HEK-293) were studied before and after transfection with a plasmid coding for glycine receptor/channels. The value of C(m) was indistinguishable in untransfected cells and in transfected cells expressing a high level of glycine channels, indicating that differences in transmembrane protein content do not significantly affect C(m). Thus, to a first approximation, C(m) may be treated as a "biological constant" across many classes of neuron.

Abstract
Full Text
Selected References
Collaboration tool especially designed for Life Science professionals.Drag-and-drop any entity to your messages.