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Biophysical Journal, Volume 92, Issue 9, 1 May 2007, Pages 3122-3129
G.H. Kim, P. Kosterin, A.L. Obaid and B.M. Salzberg
AbstractLarge and rapid changes in light scattering accompany secretion from nerve terminals of the mammalian neurohypophysis (posterior pituitary). In the mouse, these intrinsic optical signals are intimately related to the arrival of the action potential E-wave and the release of arginine vasopressin and oxytocin (S-wave). Here we have used a high bandwidth atomic force microscope to demonstrate that these light-scattering signals are associated with changes in terminal volume that are detected as nanometer-scale movements of a cantilever positioned on top of the neurohypophysis. The most rapid mechanical response (“spike”), having a duration shorter than the action potential but comparable to that of the E-wave, represents a transient increase in terminal volume due to water movement associated with Na-influx. The slower mechanical event (“dip”), on the other hand, depends upon Ca-entry as well as on intraterminal Ca-transients and, analogously to the S-wave, seems to monitor events associated with secretion.
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Copyright © 2007 The Biophysical Society. All rights reserved.
Biophysical Journal, Volume 92, Issue 9, 2983, 1 May 2007
doi:10.1529/biophysj.107.104364
New and Notable
Mechanical Spikes from Nerve Terminals
Bob Eisenberg
, 
Department of Molecular Biophysics and Physiology, Rush University Medical Center, Chicago, Illinois
Address reprint requests to Bob Eisenberg.Scientists think about what they measure, at least they are supposed to. Biologists have measured electrical signals from nerve cells for a very long time—more than 200 years back to the time of Galvani and Volta—and they have shown that voltages and currents are the most important signals of the nervous system. Electrical impulses (called action potentials or “spikes”) carry information from one cell to another, sometimes for very long distances (as in elephants, sauropod dinosaurs, or blue whales); and electrical impulses signal nerve terminals to secrete transmitter chemicals that in turn induce currents and voltages in attached nerve cells. If the sum of the induced voltages is large enough, the second nerve cell initiates a spike to pass the information further. Spike (in the presynaptic terminal), then summation (in the postsynaptic dendrite or cell body), perhaps then spike (in the postsynaptic axon) is a main method of information processing in nerve terminals and nervous systems.
Nerve terminals are small, hidden away, and as important to information processing in the brain as transistors are to information processing in computers. Transistors are much more important than their wires. Nerve terminals are much more important than their axons. Nerve terminals are hard to study, particularly in mammalian and primate and human nervous systems that have astronomically large numbers of very small terminals. More complex nervous systems have more nerve terminals, just as more powerful computers have more transistors. Complex nervous systems are hard for scientists to study because they stop processing information once they are taken apart. Scientists study what they can, measuring what they can, hoping someday to convert measurements into understanding. Scientists think of nerve terminals reflexively, emphasizing the secretory processes they can measure, hoping someday to understand the role of terminals in information processing as thoroughly as engineers understand the role of transistors.
Nerve terminals have been studied optically for many years, led by measurements of neurosecretion by Salzberg et al. 1,2,3,4. Salzberg’s laboratory 5 has now measured a mechanical spike, a rapid mechanical signal from nerve terminals that is associated with the electrical impulse. They measure the signal with an atomic force microscope and carefully show that the signal is real and not an artifact, using a variety of physical and physiological control experiments in the best tradition of British electrophysiology (see Hodgkin 6,7). Kim et al. 5 report a mechanical spike related to the arrival of the action potential followed by a “dip” that seems to reflect secretion itself.
Salzberg does not know what the mechanical spike does biologically, if it does anything at all, but now that the spike is measured, scientists will think about it, and find out much more, as Hodgkin 8,9 did. Perhaps Salzberg and successors will discover something wonderful. Perhaps they will not; but the quest will undoubtedly turn up important new results and be fun to follow. The fun is important to the science because it motivates scientists in their forbiddingly frustrating quest, a journey without a known destination. The first contribution of Salzberg’s article will be to spike interest and motivate investigation of the rapid volume change and what it does for secretion and function of the nerve terminal.
References
1. (1983). Optical recording of action potentials from vertebrate nerve terminals using potentiometric probes provides evidence for sodium and calcium components. Nature 306, 36–40. CrossRef | PubMed
2. (1985). Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis. J. Gen. Physiol. 86, 395–411. CrossRef | PubMed
3. (1988). Optical studies of the secretory event at vertebrate nerve terminals. J. Exp. Biol. 139, 195–231. PubMed
4. (2005). Changes in FAD and NADH fluorescence in neurosecretory terminals are triggered by calcium entry and by ADP production. J. Membr. Biol. 208, 113–124. CrossRef | PubMed
5. (2007). A mechanical spike accompanies the action potential in mammalian nerve terminals. Biophys. J. 92, 3122–3129. Abstract | Full Text | PDF (331 kb) | PubMed
6. (1937). Evidence for electrical transmission in nerve. I. J. Physiol. (Lond.) 90, 183–210. PubMed
7. (1937). Evidence for electrical transmission in nerve. II. J. Physiol. (Lond.) 90, 211–232. PubMed
8. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544. PubMed
9. (1992). Chance and Design. (New York: Cambridge University Press). PubMed
Publication Information
Received: January 29, 2007
Accepted: February 8, 2007
