Familiar But Unexpected: Effects of Sound Context Statistics on Auditory Responses in the Songbird Forebrain

Rapid discrimination of salient acoustic signals in the noisy natural environment may depend, not only on specific stimulus features, but also on previous experience that generates expectations about upcoming events. We studied the neural correlates of expectation in the songbird forebrain by using natural vocalizations as stimuli and manipulating the category and familiarity of context sounds. In our paradigm, we recorded bilaterally from auditory neurons in awake adult male zebra finches with multiple microelectrodes during repeated playback of a conspecific song, followed by further playback of this test song in different interleaved sequences with other conspecific or heterospecific songs. Significant enhancement in the auditory response to the test song was seen when its acoustic features differed from the statistical distribution of context song features, but not when it shared the same distribution. Enhancement was also seen when the time of occurrence of the test song was uncertain. These results show that auditory forebrain responses in awake animals in the passive hearing state are modulated dynamically by previous auditory experience and imply that the auditory system can identify the category of a sound based on the global features of the acoustic context. Furthermore, this probability-dependent enhancement in responses to surprising stimuli is independent of stimulus-specific adaptation, which tracks familiarity, suggesting that the two processes could coexist in auditory processing. These findings establish the songbird as a model system for studying these phenomena and contribute to our understanding of statistical learning and the origin of human ERP phenomena to unexpected stimuli.

SIGNIFICANCE STATEMENT Traditional auditory neurophysiology has mapped acoustic features of sounds to the response properties of neurons; however, growing evidence suggests that neurons can also encode the probability of sounds. We recorded responses of songbird auditory neurons in a novel paradigm that presented a familiar test stimulus in a sequence with similar or dissimilar sounds. The responses encode, not only stimulus familiarity, but also the expectation for a class of sounds based on the recent statistics of varying sounds in the acoustic context. Our approach thus provides a model system that uses a controlled stimulus paradigm to understand the mechanisms by which top-down processes (expectation and memory) and bottom-up processes (based on stimulus features) interact in sensory coding.