The morphology of presynaptic specializations can vary greatly ranging from classical single-release-site boutons in the central nervous system to boutons of various sizes harboring multiple vesicle release sites. Multi-release-site boutons can be found in several neural contexts, for example at the neuromuscular junction (NMJ) of body wall muscles of Drosophila larvae. These NMJs are built by two motor neurons forming two types of glutamatergic multi-release-site boutons with two typical diameters. However, it is unknown why these distinct nerve terminal configurations are used on the same postsynaptic muscle fiber. To systematically dissect the biophysical properties of these boutons we developed a full three-dimensional model of such boutons, their release sites and transmitter-harboring vesicles and analyzed the local vesicle dynamics of various configurations during stimulation. Here we show that the rate of transmission of a bouton is primarily limited by diffusion-based vesicle movements and that the probability of vesicle release and the size of a bouton affect bouton-performance in distinct temporal domains allowing for an optimal transmission of the neural signals at different time scales. A comparison of our in silico simulations with in vivo recordings of the natural motor pattern of both neurons revealed that the bouton properties resemble a well-tuned cooperation of the parameters release probability and bouton size, enabling a reliable transmission of the prevailing firing-pattern at diffusion-limited boutons. Our findings indicate that the prevailing firing-pattern of a neuron may determine the physiological and morphological parameters required for its synaptic terminals.
Bibliographical noteFunding Information:
This work was funded by a BMBF grant Bernstein group DMSPiN (BMBF, 01GQ0803) to Christoph M. Schuster and Gabriel Wittum and a grant from the German Ministry of Education and Research (BMBF, 01GQ1003A) to Gillian Queisser and Christoph M. Schuster. Additional funding came from the NeFF Network of Frankfurt University to Gillian Queisser and Gabriel Wittum. We thank I. Heppner, M. Lampe, A. Nägel, S. Reiter and K. Xylouris, for helpful discussions. We would like to thank M. Stepniewski for help with the volume grid generation.
© 2014 Knodel, Geiger, Ge, Bucher, Grillo, Wittum, Schuster and Queisser.
- Firing pattern
- Modeling and simulation
- Neuromuscular junction
- Structure-function relationships
ASJC Scopus subject areas
- Neuroscience (miscellaneous)
- Cellular and Molecular Neuroscience