A new mathematical model of short-term synaptic plasticity (STP) at the Schaffer collateral is introduced. Like other models of STP, the new model relates short-term synaptic plasticity to an interaction between facilitative and depressive dynamic influences. Unlike previous models, the new model successfully simulates facilitative and depressive dynamics within the framework of the synaptic vesicle cycle. The novelty of the model lies in the description of a competitive interaction between calcium-sensitive proteins for binding sites on the vesicle release machinery. By attributing specific molecular causes to observable presynaptic effects, the new model of STP can predict the effects of specific alterations to the presynaptic neurotransmitter release mechanism. This understanding will guide further experiments into presynaptic functionality, and may contribute insights into the development of pharmaceuticals that target illnesses manifesting aberrant synaptic dynamics, such as Fragile-X syndrome and schizophrenia. The new model of STP will also add realism to brain circuit models that simulate cognitive processes such as attention and memory. The hippocampal processing loop is an example of a brain circuit involved in memory formation. The hippocampus filters and organizes large amounts of spatio-temporal data in real time according to contextual significance. The role of synaptic dynamics in the hippocampal system is speculated to help keep the system close to a region of instability that increases encoding capacity and discriminating capability. In particular, synaptic dynamics at the Schaffer collateral are proposed to coordinate the output of the highly dynamic CA3 region of the hippocampus with the phase-code in the CA1 that modulates communication between the hippocampus and the neocortex.