Neural Correlate of Transition Violation and Deviance Detection in the Songbird Auditory Forebrain

Deviants are stimuli that violate one's prediction about the incoming stimuli. Studying deviance detection helps us understand how nervous system learns temporal patterns between stimuli and forms prediction about the future. Detecting deviant stimuli is also critical for animals' survival in the natural environment filled with complex sounds and patterns. Using natural songbird vocalizations as stimuli, we recorded multi-unit and single-unit activity from the zebra finch auditory forebrain while presenting rare repeated stimuli after regular alternating stimuli (alternating oddball experiment) or rare deviant among multiple different common stimuli (context oddball experiment). The alternating oddball experiment showed that neurons were sensitive to rare repetitions in regular alternations. In the absence of expectation, repetition suppresses neural responses to the 2nd stimulus in the repetition. When repetition violates expectation, neural responses to the 2nd stimulus in the repetition were stronger than expected. The context oddball experiment showed that a stimulus elicits stronger neural responses when it is presented infrequently as a deviant among multiple common stimuli. As the acoustic differences between deviant and common stimuli increase, the response enhancement also increases. These results together showed that neural encoding of a stimulus depends not only on the acoustic features of the stimulus but also on the preceding stimuli and the transition patterns between them. These results also imply that the classical oddball effect may result from a combination of repetition suppression and deviance enhancement. Classification analyses showed that the difficulties in decoding the stimulus responsible for the neural responses differed for deviants in different experimental conditions. These findings suggest that learning transition patterns and detecting deviants in natural sequences may depend on a hierarchy of neural mechanisms, which may be involved in more complex forms of auditory processing that depend on the transition patterns between stimuli, such as speech processing.