McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, Quebec H3A2B4, Canada.
Mila, Quebec AI Institute, Montreal, Quebec H2S 3H1, Canada.
J Neurosci. 2022 May 4;42(18):3823-3835. doi: 10.1523/JNEUROSCI.0630-21.2022. Epub 2022 Mar 29.
Processing auditory sequences involves multiple brain networks and is crucial to complex perception associated with music appreciation and speech comprehension. We used time-resolved cortical imaging in a pitch change detection task to detail the underlying nature of human brain network activity, at the rapid time scales of neurophysiology. In response to tone sequence presentation to the participants, we observed slow inter-regional signaling at the pace of tone presentations (2-4 Hz) that was directed from auditory cortex toward both inferior frontal and motor cortices. Symmetrically, motor cortex manifested directed influence onto auditory and inferior frontal cortices via bursts of faster (15-35 Hz) activity. These bursts occurred precisely at the expected latencies of each tone in a sequence. This expression of interdependency between slow/fast neurophysiological activity yielded a form of local cross-frequency phase-amplitude coupling in auditory cortex, which strength varied dynamically and peaked when pitch changes were anticipated. We clarified the mechanistic relevance of these observations in relation to behavior by including a group of individuals afflicted by congenital amusia, as a model of altered function in processing sound sequences. In amusia, we found a depression of inter-regional slow signaling toward motor and inferior frontal cortices, and a chronic overexpression of slow/fast phase-amplitude coupling in auditory cortex. These observations are compatible with a misalignment between the respective neurophysiological mechanisms of stimulus encoding and internal predictive signaling, which was absent in controls. In summary, our study provides a functional and mechanistic account of neurophysiological activity for predictive, sequential timing of auditory inputs. Auditory sequences are processed by extensive brain networks, involving multiple systems. In particular, fronto-temporal brain connections participate in the encoding of sequential auditory events, but so far, their study was limited to static depictions. This study details the nature of oscillatory brain activity involved in these inter-regional interactions in human participants. It demonstrates how directed, polyrhythmic oscillatory interactions between auditory and motor cortical regions provide a functional account for predictive timing of incoming items in an auditory sequence. In addition, we show the functional relevance of these observations in relation to behavior, with data from both normal hearing participants and a rare cohort of individuals afflicted by congenital amusia, which we considered here as a model of altered function in processing sound sequences.
处理听觉序列涉及多个大脑网络，对于音乐欣赏和言语理解等复杂感知至关重要。我们使用时分辨 cortical 成像在音高变化检测任务中，详细描述了人类大脑网络活动的潜在性质，其时间尺度与神经生理学的快速时间尺度相匹配。在对参与者呈现音调序列时，我们观察到以音调呈现的速度（2-4 Hz）缓慢的区域间信号，该信号从听觉皮层指向额下回和运动皮层。对称地，运动皮层通过快速（15-35 Hz）活动的爆发表现出对听觉和额下回皮层的有向影响。这些爆发恰好出现在序列中每个音调的预期潜伏期。这种慢/快神经生理活动之间的相互依赖关系表现为听觉皮层中局部交叉频率相位-幅度耦合的一种形式，其强度随时间动态变化，并在预期音高变化时达到峰值。我们通过包括一组患有先天性失歌症的个体来澄清这些观察结果与行为的机制相关性，作为处理声音序列功能改变的模型。在失歌症中，我们发现朝向运动和额下回皮层的区域间慢信号减弱，以及听觉皮层中慢/快相位-幅度耦合的慢性过度表达。这些观察结果与刺激编码和内部预测信号的相应神经生理机制之间的失准一致，而对照组中则没有这种失准。总之，我们的研究提供了一个功能性和机制性的解释，用于预测听觉输入的顺序时间。听觉序列由广泛的大脑网络处理，涉及多个系统。特别是额颞脑连接参与了序列听觉事件的编码，但到目前为止，它们的研究仅限于静态描述。本研究详细描述了人类参与者中涉及这些区域间相互作用的振荡大脑活动的性质。它表明，听觉和运动皮层区域之间的定向、多节奏振荡相互作用如何为听觉序列中传入项目的预测时间提供功能解释。此外，我们展示了这些观察结果与行为的功能相关性，既有正常听力参与者的数据，也有罕见的先天性失歌症患者的数据，我们认为这是处理声音序列功能改变的模型。
