Abstract
The spatial interactions of synaptic vesicles in synapses were assessed after a detailed characterization of size, shape, and orientation of the synaptic vesicles. We hypothesized that shape and orientation of the synaptic vesicles are influenced by their movement toward the active zone causing deviations from spherical shape and systematic trends in their orientation. We studied three-dimensional representations of synapses obtained by manual annotation of focused ion beam scanning electron microscopy (FIB-SEM) images of male mouse brain. The configurations of synaptic vesicles were regarded as marked point patterns, where the points are the centers of the vesicles, and the mark of a vesicle is given by its size, shape, and orientation characteristics. Statistics for marked point processes were employed to study spatial interactions between vesicles. We found that the synaptic vesicles in excitatory synapses appeared to be of oblate ellipsoid shape and in inhibitory synapses appeared to be of cigar ellipsoid shape, and followed a systematic pattern regarding their orientation toward the active zone. Moreover, there was strong evidence of spatial alignment in the orientations of pairs of synaptic vesicles, and of repulsion between them only in excitatory synapses, beyond that caused by their physical extent.
Highlights
There is extensive knowledge of how neurons communicate and how nerve signal transport from one neuron to another, (Li and Chin, 2003; Jahn, 2004; Jahn and Fasshauer, 2012)
We investigated the electrostatic repulsion between the synaptic vesicles using techniques for spatial marked point processes, in particular variants of the K-function and the mark variogram (Møller and Waagepetersen, 2003; Diggle, 2003; Baddeley, 2010)
This holds for the mean ratios for all vesicles considered jointly. These findings indicate that vesicles are of oblate ellipsoidal shape in the asymmetric synapses
Summary
There is extensive knowledge of how neurons communicate and how nerve signal transport from one neuron to another, (Li and Chin, 2003; Jahn, 2004; Jahn and Fasshauer, 2012). Upon arrival of an action potential at the nerve terminal, the pre-synaptic plasma membrane depolarizes and voltage-gated Ca2+ channels open; the initial rapid rise in intracellular Ca2+ triggers exocytosis of readily releasable synaptic vesicles at the active zone of the pre-synaptic membrane and release of their neurotransmitter into the synaptic cleft (Südhof, 1995; Rosenmund and Stevens, 1996). Synaptic vesicle shape and spatial interaction movement have been observed in different synaptic preparations (Llinás et al, 1989; Koenig et al, 1993; Ryan and Smith, 1995; Henkel et al, 1996). It is conceivable that the synaptic vesicle movement and their electrostatic repulsion could influence their shapes and their spatial distribution within the synapse. The dynamic of vesicle diffusion with the target membrane (vesicle-membrane interaction) was studied using total internal reflection-fluorescence correlation spectroscopy (Kyoung and Sheets, 2008)
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