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

Abstract

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.

Unilateral vocal nerve resection alters neurogenesis in the avian song system in a region-specific manner

“…On the other hand, we suggest that perhaps the increased response in the left NCM reflects a left-dominant sensitivity to aberrant information, resonating with our findings. The left hemisphere of NCM has been shown to be sensitive to novel auditory experience more broadly [ 76 , 77 ] consistent with the idea that NCM (in these studies, bilaterally) is sensitive to expectation [ 78 , 79 ]. Thus perhaps it is the novelty of the distorted song, and not feedback about the bird’s own song per se , that underlies the observed decrease in new neurons in the left NCM.…”

Statistical learning of transition patterns in the songbird auditory forebrain

“…For example, after being exposed to sequences of tones with fixed transition patterns, human infants and adults showed surprise responses when they heard sequences that violated the transition patterns in the previously experienced sequences 4,6,7 . Similar statistical learning phenomena have also been reported in songbirds, monkeys and other animals 5,8,9 . However, most laboratory studies at the neural level used the oddball paradigm, in which one stimulus is presented with low probability as oddball while the other stimulus is presented with high probability as standard.…”

“…However, the enhanced neural responses to the oddball may be because the oddball is rare and therefore unexpected rather than because the oddball violates the repetition pattern of the standard. In addition, in the natural environment, the intervals between sounds are often variable instead of fixed and can span multiple time scales whereas most previous studies have used short and fixed inter-stimulus intervals (ISI) 3,[6][7][8][9]12,14 . Consequently, it is unknown whether there exists a neural correlate of statistical learning of transition patterns when ISI is long or variable.…”

Mismatch Responses Evoked by Sound Pattern Violation in the Songbird Forebrain Suggest Common Auditory Processing With Human

“…This suggests that detecting deviance in natural complex sounds is critical for animal survival. Electrophysiological recording studies have reported that the auditory forebrain of songbirds shows larger responses to deviant calls than to standard calls using an oddball paradigm ( Beckers and Gahr, 2012 ; Dong and Vicario, 2018 ). We demonstrated MMR elicited by deviant sounds using an oddball paradigm with song elements and calls.…”

“…It has been reported that neurons in NCM show stimulus-specific habituation to natural sounds such as conspecific and heterospecific vocalizations ( Mello et al, 1995 ; Chew et al, 1996 ). In addition, neurons in the secondary auditory areas, i.e., NCM and caudomedial mesopallium (CMM), show response bias to deviant sounds in an oddball paradigm during multiunit and single-unit recordings in both anesthetized birds ( Beckers and Gahr, 2012 ; Ono et al, 2016 ) and awake-restrained birds ( Dong and Vicario, 2018 ). These studies suggest that the NCM integrates auditory information over both long- and short-time windows, and focal attention to auditory stimuli is not required for this process.…”