Complementary functional profiles of mismatch responses mediated by adaptation and deviance detection point to two distinct auditory short-term memory systems.

Mismatch negativity (MMN) is a macroscopic EEG deflection in response to potentially informative auditory events, e.g., rare or unexpected sounds. Mismatch negativity reflects two processes: ) adaptation, a reduction of responses to repeated sounds, and ) deviance detection, an enhancement of responses to sounds violating an expected pattern, likely mediated by predictive coding. Adaptation and deviance detection both reflect information about past sounds and are thus dependent on an auditory memory trace. Although the two processes have been distinguished theoretically, computationally, and anatomically, it is not known whether they use information from the same or different memory systems. To answer this question, macaque monkeys listened to a modified roving standard paradigm with a many-standard control condition designed to split mismatch responses into adaptation and deviance detection as a function of delay and frequency difference. Using computational modeling, we confirm that the requirements for isolating adaptation and deviance detection are met. We show that micro- and macroscopic mismatch responses were dominated by adaptation at short latencies but included a meaningful contribution of deviance detection at longer latencies. Most importantly, we show that mismatch responses mediated by adaptation have a short temporal scope and narrow frequency tuning consistent with its dependence on echoic memory. In contrast, mismatch responses mediated by deviance detection have a longer temporal scope but broader frequency tuning, thus pointing to a different memory system. These clearly distinct functional profiles shed light on the evolutionary need for two separate but complementary mechanisms for guiding attention to potentially informative auditory events. Mismatch negativity has been viewed either as an echoic memory-based comparison process (deviance detection), or as the recruitment of nonadapted fresh afferents (adaptation). Here, we show that lifetime and frequency tuning of adaptation, but not deviance detection, matches that of echoic memory measured behaviorally. These findings provide compelling evidence that the mismatch negativity (MMN) is a mix of two functionally distinct processes whose properties reflect two distinct auditory memory systems.