Cortical memory circuits that represent words in the brain form the foundation of our mental lexicon; yet, their architecture remains poorly understood. A valuable approach to probing these representations is measuring the Mismatch Negativity (MMN), an electrophysiological brain response sensitive to various psycholinguistic variables; however, its specificity to lexical processing remains debated. To scrutinise its properties as a neural index of word-specific memory trace activity, we adapted the classical passive auditory oddball design to fMRI and recorded the BOLD (blood oxygenation level-dependent) correlate of the MMN elicited by words of different lexical frequencies and by phonologically matched control pseudowords. The results showed significant BOLD-MMN responses in bilateral superior-temporal and middle-temporal cortices. Crucially, these activations were more expressed for meaningful words than meaningless pseudowords, indicating BOLD-MMN sensitivity to the stimulus’ lexicality. We also found the left temporal activity to be more pronounced for high- than low-frequency words, the effect not found for their pseudoword analogues, further confirming the lexical nature of these responses. This pattern of results is best explained by the automatic activation of long-term memory traces for real words formed in the process of previous linguistic experience whose intensity determines the strength of connectivity within these circuits and thus the magnitude of their activation, which thereby reflects the respective stimuli’s status in the brain's mental lexicon.