The current electroencephalography study investigated the relationship between the motor and (language) comprehension systems by simultaneously measuring mu and N400 effects. Specifically, we examined whether the pattern of motor activation elicited by verbs depends on the larger sentential context. A robust N400 congruence effect confirmed the contextual manipulation of action plausibility, a form of semantic congruency. Importantly, this study showed that: (1) Action verbs elicited more mu power decrease than non-action verbs when sentences described plausible actions. Action verbs thus elicited more motor activation than non-action verbs. (2) In contrast, when sentences described implausible actions, mu activity was present but the difference between the verb types was not observed. The increased processing associated with a larger N400 thus coincided with mu activity in sentences describing implausible actions. Altogether, context-dependent motor activation appears to play a functional role in deriving context-sensitive meaning.