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Responses of auditory cortical neurons encode sound features of incoming acoustic stimuli and also are shaped by stimulus context and history. Previous studies of mammalian auditory cortex have reported a variable time course for such contextual effects ranging from milliseconds to minutes. However, in secondary auditory forebrain areas of songbirds, long-term stimulus-specific neuronal habituation to acoustic stimuli can persist for much longer periods of time, ranging from hours to days. Such long-term habituation in the songbird is a form of long-term auditory memory that requires gene expression. Although such long-term habituation has been demonstrated in avian auditory forebrain, this phenomenon has not previously been described in the mammalian auditory system. Utilizing a similar version of the avian habituation paradigm, we explored whether such long-term effects of stimulus history also occur in auditory cortex of a mammalian auditory generalist, the ferret. Following repetitive presentation of novel complex sounds, we observed significant response habituation in secondary auditory cortex, but not in primary auditory cortex. This long-term habituation appeared to be independent for each novel stimulus and often lasted for at least 20 min. These effects could not be explained by simple neuronal fatigue in the auditory pathway, because time-reversed sounds induced undiminished responses similar to those elicited by completely novel sounds. A parallel set of pupillometric response measurements in the ferret revealed long-term habituation effects similar to observed long-term neural habituation, supporting the hypothesis that habituation to passively presented stimuli is correlated with implicit learning and long-term recognition of familiar sounds. SIGNIFICANCE STATEMENT Long-term habituation in higher areas of songbird auditory forebrain is associated with gene expression and is correlated with recognition memory. Similar long-term auditory habituation in mammals has not been previously described. We studied such habituation in single neurons in the auditory cortex of awake ferrets that were passively listening to repeated presentations of various complex sounds. Responses exhibited long-lasting habituation (at least 20 min) in the secondary, but not primary auditory cortex. Habituation ceased when stimuli were played backward, despite having identical spectral content to the original sound. This long-term neural habituation correlated with similar habituation of ferret pupillary responses to repeated presentations of the same stimuli, suggesting that stimulus habituation is retained as a long-term behavioral memory.

Implicit Memory for Complex Sounds in Higher Auditory Cortex of the Ferret