Traditional models of basal ganglia disorders are grounded in the assumption that network dysfunction is driven by alterations in intrinsic excitability of striatal neurons. Recent work has challenged this assumption, showing that in mouse models of Parkinson’s disease there are profound alterations in synaptic strength and connectivity accompanying network pathophysiology. The talk will summarize this work in two steps. The first part of the talk will give a basic overview of basal ganglia structure and function, emphasizing the complementary roles of direct and indirect pathways in regulating goal directed and habitual movement. New insights into the cortical and thalamic connectivity of striatal direct and indirect pathway spiny projection neurons (SPNs) will be outlined along with the mechanisms governing their strength. The second part of the talk will provide a summary of work characterizing cell-specific alterations in the number and strength of synaptic connections driving SPN activity in the hypokinetic parkinsonian state and after administration of levodopa at doses sufficient to produce hyperkinetic dyskinesia. The interplay of homeostatic and dopamine-dependent synaptic plasticity in shaping these alterations in synaptic function will be examined and an attempt made to reconcile synaptic changes with the hypokinetic and hyperkinetic features of these states. Translational opportunities arising from these insights also will be mentioned.