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

Abstract

Learning sound patterns in the natural auditory scene and detecting deviant patterns are adaptive behaviors that aid animals in predicting future events and behaving accordingly. Mismatch negativity (MMN) is a component of the event-related potential (ERP) that is reported in humans when they are exposed to unexpected or rare stimuli. MMN has been studied in several non-human animals using an oddball task by presenting deviant pure tones that were interspersed within a sequence of standard pure tones and comparing the neural responses. While accumulating evidence suggests the homology of non-human animal MMN-like responses (MMRs) and human MMN, it is still not clear whether the function and neural mechanisms of MMRs and MMN are comparable. The Java sparrow (Lonchura oryzivora) is a songbird that is a vocal learner, is highly social, and maintains communication with flock members using frequently repeated contact calls and song. We expect that the songbird is a potentially useful animal model that will broaden our understanding of the characterization of MMRs. Due to this, we chose this species to explore MMRs to the deviant sounds in the single sound oddball task using both pure tones and natural vocalizations. MMRs were measured in the caudomedial nidopallium (NCM), a higher-order auditory area. We recorded local field potentials under freely moving conditions. Significant differences were observed in the negative component between deviant and standard ERPs, both to pure tones and natural vocalizations in the oddball sequence. However, the subsequent experiments using the randomized standard sequence and regular pattern sequence suggest the possibility that MMR elicited in the oddball paradigm reflects the adaptation to a repeated standard sound but not the genuine deviance detection. Furthermore, we presented contact call triplet sequences and investigated MMR in the NCM in response to sound sequence order. We found a significant negative shift in response to a difference in sequence pattern. This demonstrates MMR elicited by violation of the pattern of the triplet sequence and the ability to extract sound sequence information in the songbird auditory forebrain. Our study sheds light on the electrophysiological properties of auditory sensory memory processing, expanding the scope of characterization of MMN-like responses beyond simple deviance detection, and provides a comparative perspective on syntax processing in human.

Evidence for auditory stimulus-specific adaptation but not deviance detection in larval zebrafish brains

“…Studies in rodents and pigeons successfully identified responses meeting these criteria 14,15,18 . However, efforts to identify an equivalent of MMN in songbirds and frogs failed to find similarly deviant-specific responses that cannot be explained by stimulus salience or SSA 19,21 . From our findings, the larval zebrafish fit into the latter category.…”

“…An equivalent of the auditory MMN response is well established in rodents [13][14][15] . MMN-like responses are also present in the equivalent of the auditory cortex in macaques 16 , cats 17 , pigeons 18 and songbirds 19 , and there is preliminary evidence for auditory deviance responses in dogs 20 and frogs 21 , though interpretation of these findings are confounded by lack of role reversal for the expected and unexpected sounds. MMN can also be elicited in other sensory modalities 1 , and indeed visual MMN has been characterized in mice using calcium imaging 22 While the full complexity of the human MMN response may not be reflected in other species 14 , it stands to reason that the ability to detect changes in the sensory landscape would have arisen early in evolutionary time.…”