Translational experimental approaches that help us better trace Parkinson’s disease (PD) pathophysiological mechanisms leading to new therapeutic targets are urgently needed. In this article, we review recent experimental and clinical studies addressing abnormal neuronal activity and pathological network oscillations, as well as their underlying mechanisms and modulation. Our aim is to enhance our knowledge about the progression of Parkinson's disease pathology and the timing of its symptom’s manifestation. Here, we present mechanistic insights relevant for the generation of aberrant oscillatory activity within the cortico-basal ganglia circuits. We summarize recent achievements extrapolated from available PD animal models, discuss their advantages and limitations, debate on their differential applicability, and suggest approaches for transferring knowledge on disease pathology into future research and clinical applications.