Alzheimer’s disease (AD) poses a public health crisis. There is an urgent need for effective treatments and disease-modifying therapies. Glutamate dysfunction is a core feature of AD, and glutamate is a validated target for treating AD.  We tested a novel 3rd generation tripeptide prodrug of the glutamate modulator, riluzole, that offers improved bioavailability, safety, and dosing. In this preclinical study, we examined the effects of this drug, troriluzole on synaptic function using the triple transgenic (3xTg) AD model. 3xTg mice received the riluzole prodrug (25 mg/kg/day) from 5 -8 months of age. At 8 months of age, drug-treated 3xTg mice were compared to vehicle-treated 3xTg and nontransgenic controls for alterations in learning, memory, and synaptic plasticity. Basal synaptic transmission was reduced by 50-60% in vehicle-treated 3xTg slices compared to controls, and treatment partially attenuated these basal synaptic transmission deficits. To determine if differences in basal synaptic transmission were related to presynaptic modifications, the probability of neurotransmitter release was examined by measuring paired pulse facilitation (PPF). PPF was significantly reduced in vehicle-treated 3xTg slices, indicating an increase in presynaptic release probability. Drug treatment restored PPF in 3xTg mice to that of controls. The presynaptic readily releasable vesicle pool (RRP) was also significantly reduced in 3xTg mice, indicating increased presynaptic vesicle docking. Treatment significantly increased RRP in 3xTg mice. LTP, a cellular correlate of learning & memory, was reduced by 25% in vehicle-treated 3xTg mice compared to controls. Drug treatment completely restored the synaptic plasticity deficits observed in 3xTg mice. 3xTgs also exhibited deficits in MWM probe trials that were rescued by treatment. These results suggest that troriluzole restores synaptic deficits in 3xTg mice and highlight its potential as a novel therapy for AD.