Mori Chihiro, Okanoya Kazuo
Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan.
RIKEN Center for Brain Science, Wako, Japan.
Front Physiol. 2022 Mar 3;13:822098. doi: 10.3389/fphys.2022.822098. eCollection 2022.
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 () 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.
在自然听觉场景中学习声音模式并检测异常模式是有助于动物预测未来事件并据此做出行为的适应性行为。失配负波（MMN）是事件相关电位（ERP）的一个组成部分，当人类暴露于意外或罕见刺激时会出现。通过在一系列标准纯音中穿插呈现异常纯音并比较神经反应，利用oddball任务在几种非人类动物中对MMN进行了研究。虽然越来越多的证据表明非人类动物的MMN样反应（MMRs）与人类MMN具有同源性，但MMRs和MMN的功能及神经机制是否具有可比性仍不清楚。爪哇雀是一种鸣禽，是声音学习者，具有高度社会性，通过频繁重复的联络叫声和歌声与群体成员保持交流。我们期望这种鸣禽是一种潜在有用的动物模型，将拓宽我们对MMRs特征的理解。因此，我们选择这个物种，在单声音oddball任务中使用纯音和自然发声来探索对异常声音的MMRs。在高阶听觉区域尾内侧巢皮质（NCM）中测量MMRs。我们在自由活动条件下记录局部场电位。在oddball序列中，无论是对纯音还是自然发声，异常ERP和标准ERP的负性成分之间均观察到显著差异。然而，随后使用随机标准序列和规则模式序列的实验表明，oddball范式中引发的MMR可能反映了对重复标准声音的适应，而非真正的异常检测。此外，我们呈现联络叫声三联体序列，并研究NCM中对声音序列顺序的MMR。我们发现对序列模式差异的反应存在显著负向偏移。这证明了由三联体序列模式违反引发的MMR以及鸣禽听觉前脑提取声音序列信息的能力。我们的研究揭示了听觉感觉记忆处理的电生理特性，将MMN样反应的特征描述范围扩展到简单异常检测之外，并为人类的句法处理提供了一个比较视角。
