Presynaptic and postsynaptic molecular complexes linked through transsynaptic assemblies, visualized by electron tomography of rat hippocampal synapses

Authors

• AA Cole
• TS Reese

Abstract

At the chemical synapse, complex molecular interplay enables neuronal communication. Mapping the distribution and interactions of proteins within individual compartments has been crucial to our understanding of synaptic transmission. However, both light and electron microscopy have documented that key synaptic proteins align across the synaptic cleft. This alignment suggests coordination between compartments, indicating that the organization of one compartment may influence the other. Characterizing the underpinnings of these organizational interdependencies is crucial to understand synaptic dynamics. Our 3D renderings visualize electron dense structures, in electron tomograms of high-pressure frozen and freeze-substituted dissociated rat hippocampal cultures. These renderings reveal synapse-spanning structural complexes linking presynaptic and postsynaptic structures, called transsynaptic assemblies. A ~100 nm thick cross-section of a synapse contained as many as 77 assemblies. Only 20 percent of all assemblies directly connected to synaptic vesicles. Each compartment has many morphologically distinct structures that are integrated into transsynaptic assemblies. These components can be used by more than one assembly, linking assemblies together to form larger domains of association. Here, we describe the morphologies of assemblies and their constituent parts, visualize their associations, and map their distribution in the synapse. In our interpretation, assemblies are modular structures composed of an array of possible molecules or complexes that connect onto a structural unit. The synapse coordinates key materials necessary for various synaptic functions through specialized domains physically linked/anchored across the synapse into nanocolumns. The physical connections across the cleft facilitate inter-compartmental coordination. This extends beyond merely facilitating exocytosis.

Scientific Focus Area: Neuroscience

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