Aversive events in our environment shape our behaviours. Instrumental behaviours are punished when an action results in an aversive event. Yet there are instances where behaviours appear inappropriately sensitive to potential threats. The neural underpinnings of these inappropriate behaviours are poorly understood. In a conditioned punishment task, we trained rats to press two levers for pellets. Their responding suppressed on one lever when it also earned a conditioned stimulus (CS+) that was paired with a footshock, whilst responding continued on the other lever that earned a neutral conditioned stimulus (CS-) that did not elicit a footshock. Here, we show that regions of the cortico-striatal pathway, including the prelimbic (PL) and infralimbic (IL) cortices, and the nucleus accumbens core (AcbC) and shell (AcbSh) are implicated in punishment and fear expression in different ways. Inhibiting the IL or PL increased responding on the punished, whilst inhibiting the AcbC or AcbSh decreased responding on the unpunished lever. Suppressed responding to both levers during the CS+ was abolished following inhibition of the PL and AcbSh, but not the IL and AcbC. These results suggest there is an effect of cued punishment expression that is distinct from non-cued punishment and fear expression to the target cue, that is mediated by cortico-striatal circuitry. We then proposed to determine whether the neurons that are activated following learning the punishment contingency in the PL and IL are also those that project to the AcbC and AcbSh respectively by double-labelling the neurons with a retrograde tracer and c-Fos.