The spatial distribution of calcium signals in squid presynaptic terminals.


Journal Article

1. The fluorescent Ca2+ indicator dye, fura-2, was used to examine the spatial distribution of intracellular Ca2+ signals in giant presynaptic terminals of squid. Brief trains of presynaptic action potentials were evoked to open Ca2+ channels within the giant presynaptic terminals and elevate presynaptic Ca2+ concentration. 2. Electrical stimulation produced pronounced rises in presynaptic Ca2+ concentration. These rises were much larger in the terminal region than in the adjacent axonal region of the presynaptic neuron, suggesting that Ca2+ channels are most abundant in the terminal. 3. Stimulation also produced gradients in Ca2+ concentration across the width of the presynaptic terminal. During stimulation, Ca2+ concentration was highest in the compartment of the presynaptic terminal closest to the postsynaptic neuron. This suggests that the Ca2+ channels are localized to this region of the presynaptic terminal. 4. Following the end of action potential trains, the rises in Ca2+ concentration became uniform across the width of the terminal. The redistribution of Ca2+ presumably is due to diffusion of Ca2+ throughout the presynaptic cytoplasm. Stimulus-evoked rises in Ca2+ declined slowly over several tens of seconds. 5. Histological examination of a giant presynaptic terminal used for imaging experiments revealed that the spatial compartments where stimulus-induced rises in Ca2+ concentration were highest were also enriched in active zones, the presynaptic sites of transmitter secretion. The co-localization of Ca2+ transients and active zones strongly suggests that neurons cluster Ca2+ channels selectively at active zones and that they do so to enhance the magnitude of Ca2+ signals in the vicinity of the active zone. 6. Longitudinal gradients in Ca2+ concentration also occur within presynaptic terminals and can be quantitatively accounted for by gradients in surface/volume ratio and density of active zones along the length of the presynaptic terminal.

Full Text

Cited Authors

  • Smith, SJ; Buchanan, J; Osses, LR; Charlton, MP; Augustine, GJ

Published Date

  • December 1993

Published In

Volume / Issue

  • 472 /

Start / End Page

  • 573 - 593

PubMed ID

  • 8145162

Pubmed Central ID

  • 8145162

Electronic International Standard Serial Number (EISSN)

  • 1469-7793

International Standard Serial Number (ISSN)

  • 0022-3751

Digital Object Identifier (DOI)

  • 10.1113/jphysiol.1993.sp019963


  • eng