Membrane Capacitance Measurements Revisited: Dependence of Capacitance Value on Measurement Method in Nonisopotential Neurons
- 1 October 2009
- journal article
- research article
- Published by American Physiological Society in Journal of Neurophysiology
- Vol. 102 (4), 2161-2175
- https://doi.org/10.1152/jn.00160.2009
Abstract
During growth or degeneration neuronal surface area can change dramatically. Measurements of membrane protein concentration, as in ion channel or ionic conductance density, are often normalized by membrane capacitance, which is proportional to the surface area, to express changes independently from cell surface variations. Several electrophysiological protocols are used to measure cell capacitance, all based on the assumption of membrane isopotentiality. Yet, most neurons violate this assumption because of their complex anatomical structure, raising the question of which protocol yields measurements that are closest to the actual total membrane capacitance. We measured the capacitance of identified neurons from crab stomatogastric ganglia using three different protocols: the current-clamp step, the voltage-clamp step, and the voltage-clamp ramp protocols. We observed that the current-clamp protocol produced significantly higher capacitance values than those of either voltage-clamp protocol. Computational models of various anatomical complexities suggest that the current-clamp protocol can yield accurate capacitance estimates. In contrast, the voltage-clamp protocol estimates rapidly deteriorate as isopotentiality is reduced. We provide a mathematical description of these results by analyzing a simple two-compartment model neuron to facilitate an intuitive understanding of these methods. Together, the experiments, modeling, and mathematical analysis indicate that accurate total membrane capacitance measurements cannot be obtained with voltage-clamp protocols in nonisopotential neurons. Furthermore, although current-clamp steps can theoretically yield accurate measurements, experimentalists should be aware of limitations imposed by step duration and numerical errors during fitting procedures to obtain the membrane time constant.Keywords
This publication has 28 references indexed in Scilit:
- The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance MeasurementsBiophysical Journal, 2009
- Low-Voltage-Activated Potassium Channels Underlie the Regulation of Intrinsic Firing Properties of Rat Vestibular Ganglion CellsJournal of Neurophysiology, 2008
- Neuronal morphology and neuropil structure in the stomatogastric ganglion of the lobster,Homarus americanusJournal of Comparative Neurology, 2007
- Ionic Mechanism Underlying Recovery of Rhythmic Activity in Adult Isolated NeuronsJournal of Neurophysiology, 2006
- Properties of mouse spinal lamina I GABAergic interneurons.Journal of Neurophysiology, 2005
- Cortical rewiring and information storageNature, 2004
- Membrane capacitance measurement using patch clamp with integrated self-balancing lock-in amplifierPflügers Archiv - European Journal of Physiology, 2001
- Interpretation of time constant and electrotonic length estimates in multicylinder or branched neuronal structuresJournal of Neurophysiology, 1992
- Ionic currents of the lateral pyloric neuron of the stomatogastric ganglion of the crabJournal of Neurophysiology, 1992
- A quantitative description of membrane current and its application to conduction and excitation in nerveThe Journal of Physiology, 1952