CLN3 is a lysosomal membrane protein whose precise function is not yet known. Recent studies propose divergent functions for CLN3; as a vesicular trafficking hub or its role in glycerophosphodiester (GPD) efflux from lysosomes. The role of CLN3 in the neurons and at the synapse remains elusive. Mutations in CLN3 gene cause Juvenile Neuronal Ceroid Lipofuscinosis (JNCL), a condition associated with learning impairments and memory deficits in affected children. Using CLN3Δex7/8 mouse model, we investigated the impact of CLN3 loss at synapses. Analysis of synaptic transmission revealed a significant reduction in the frequency of miniature excitatory postsynaptic currents (mEPSCs) at an early disease stage (4 months). Together with a reduced synaptic vesicle release probability and an increase in the readily releasable pool size (RRP), these findings suggest a disturbed presynaptic vesicle cycling and maintenance. We also found a significantly reduced AMPA-NMDA ratio in CLN3Δex7/8 mice indicating that the number of silent synapses is increased. Furthermore, morphological analysis revealed a significant reduction in the number of dendritic spines, in particular of the mushroom and thin spine subtypes. Overall, our study provides evidence of early synaptic and morphological changes in CLN3-deficient neurons, underscoring the role of CLN3 in the maintenance of synaptic homeostasis. Additionally, we posit that synaptic dysfunction may serve as an early indicator in the pathogenesis of NCL disorders, presenting a potential therapeutic target.