Abstract
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.
Highlights
Chemical synapses are specialized compartments of neurons for neuron-to-neuron or neuron-to-muscle communication that exist in various morphological layouts (Rollenhagen and Lubke, 2006) ranging from classical single-release site synapses at cortical neurons (Gulyas, 1993) over intermediate-sized multi-releasesite boutons of the calyx of Heldt (Satzler et al, 2002) or the arthropod neuromuscular junctions (NMJs) (Bradacs et al, 1997) to giant multi-release-site terminals at vertebrate NMJs (Dreyer et al, 1973)
Taking into account the total number of vesicles that can be released from a NMJ during vesicle depletion experiments (Delgado et al, 2000) and data from ultrastructural analyses (Sigrist et al, 2002) we estimated a concentration of 150–500 vesicles per μm3 within a bouton at rest
The positioning of the vesicle release sites on the surface of these spherical boutons was guided by serial ultrastructural reconstructions of larval boutons from which we determined the densities of T-bar harboring active zones between 0.37 and 0.46 μm2 (Meinertzhagen et al, 1998; Sigrist et al, 2002, 2003) with an average active zone diameter of 300–400 nm (Meinertzhagen et al, 1998; Sigrist et al, 2002, 2003)
Summary
Chemical synapses are specialized compartments of neurons for neuron-to-neuron or neuron-to-muscle communication that exist in various morphological layouts (Rollenhagen and Lubke, 2006) ranging from classical single-release site synapses at cortical neurons (Gulyas, 1993) over intermediate-sized multi-releasesite boutons of the calyx of Heldt (Satzler et al, 2002) or the arthropod neuromuscular junctions (NMJs) (Bradacs et al, 1997) to giant multi-release-site terminals at vertebrate NMJs (Dreyer et al, 1973). While the principal processes underlying synaptic transmission and plasticity at these synapses are rather well understood, the role that the various morphological layouts may play in shaping synaptic functions is currently unclear One reason for this astonishing discrepancy may be the difficulties to systematically control the morphological and physiological configuration of a given synaptic system. Larval body wall muscles of Drosophila are typically innervated by two motor neurons of which one forms large spherical and somewhat variable type Ib boutons and a second motor neuron forms smaller and more regular type Is boutons Both types of boutons harbor multiple glutamatergic release sites that are spaced according to a strict nearest-neighborhood relationship (Atwood et al, 1993; Meinertzhagen et al, 1998; Sigrist et al, 2003) and that show discrete differences in their release probabilities (Kurdyak et al, 1994; Cooper et al, 1995). In spite of their close functional relationship, it has so far not been possible to systematically assess why both motor neurons maintain their obvious morphological and physiological differences and what their relevance is for the animal’s behavior
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