Loss-of-function PTEN Induced Kinase 1 (PINK1) mutations cause early-onset familial Parkinson's disease (PD) with similar clinical and neuropathological characteristics as idiopathic PD. While Pink1 knockout (KO) rats have mitochondrial dysfunction, locomotor deficits, and α-synuclein aggregates in several brain regions such as cerebral cortex, dorsal striatum, and substantia nigra, the functional ramifications on synaptic circuits are unknown. Using whole cell patch clamp recordings, we found a significant increase in the frequency of spontaneous excitatory postsynaptic currents (sEPSCs) onto striatal spiny projection neurons (SPNs) in Pink1 KO rats at ages 4 and 6 months compared to wild-type (WT) littermates, suggesting increased excitability of presynaptic neurons. While sEPSC amplitudes were also increased at 2 and 4 months, no changes were observed in AMPAR/NMDAR ratio or receptor expression. Further analysis revealed increased glutamate release probability and decreased recovery of the synaptic vesicle pool following a train of stimulation in Pink1 KO rats. Ultrastructural analysis revealed increased excitatory and inhibitory synapse number and increased levels of presynaptic α-synuclein, while the number and structure of striatal mitochondria appeared normal. Lastly, we found that Pink1 KO rats have altered striatal dopamine tone, which together with the abnormal α- synuclein distribution and dysfunctional mitochondria, could contribute to the increase in excitatory transmission. Together, these studies show that PINK1 is necessary for normal glutamatergic transmission onto striatal SPNs and reveal possible mechanisms underlying striatal circuit dysfunction in PD.