Compulsive drug seeking is a key behavioral trait when studying transition to cocaine addiction in rodent models. Understanding how neurophysiological changes operate in circuits of compulsion, and searching for molecular markers to distinguish addictive vs. non-addictive individuals may help us to understand the mechanisms underlying cocaine addiction. Cocaine-evoked synaptic plasticity has been shown to correlate with addictive-like behavior in certain brain regions of the mesolimbic dopamine system. In the subthalamic nucleus (STN), specific oscillatory frequencies are associated to compulsive-like cocaine seeking behavior in the rat. However, the cellular and molecular correlates of these changes in firing of STN neurons remain unknown. Here, we performed patch-clamp recordings on STN neurons of adult male previously subjected to the “Intra-Escalation Punishment” (IEP) procedure, which allows the concomitant development of loss of control over cocaine intake and compulsive-like seeking behavior. To better characterize the electrical signature of this neuronal population, we performed recordings of STN neurons in ex vivo horizontal brain slices, using current- and voltage-clamp protocols to investigate i) intrinsic excitability properties and ii) internal capsule-evoked excitatory synaptic responses. Our results show that, after IEP procedure, STN neurons of compulsive-like rats display a significant increase in the AMPA rectification index, a hallmark of calcium-permeable subunit composition, and that this index correlates with compulsive-like behavior.