Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA; Department of Neurosurgery, University of Tsukuba, Tsukuba, 3058575, Japan.
Department of Pediatrics, Children's Hospital of Michigan, Detroit Medical Center, Wayne State University, Detroit, MI, 48201, USA; Department of Neurosurgery, Yokohama City University, Yokohama, Kanagawa, 2360004, Japan.
Neuroimage. 2022 Sep;258:119342. doi: 10.1016/j.neuroimage.2022.119342. Epub 2022 May 30.
A prominent view of language acquisition involves learning to ignore irrelevant auditory signals through functional reorganization, enabling more efficient processing of relevant information. Yet, few studies have characterized the neural spatiotemporal dynamics supporting rapid detection and subsequent disregard of irrelevant auditory information, in the developing brain. To address this unknown, the present study modeled the developmental acquisition of cost-efficient neural dynamics for auditory processing, using intracranial electrocorticographic responses measured in individuals receiving standard-of-care treatment for drug-resistant, focal epilepsy. We also provided evidence demonstrating the maturation of an anterior-to-posterior functional division within the superior-temporal gyrus (STG), which is known to exist in the adult STG.
We studied 32 patients undergoing extraoperative electrocorticography (age range: eight months to 28 years) and analyzed 2,039 intracranial electrode sites outside the seizure onset zone, interictal spike-generating areas, and MRI lesions. Patients were given forward (normal) speech sounds, backward-played speech sounds, and signal-correlated noises during a task-free condition. We then quantified sound processing-related neural costs at given time windows using high-gamma amplitude at 70-110 Hz and animated the group-level high-gamma dynamics on a spatially normalized three-dimensional brain surface. Finally, we determined if age independently contributed to high-gamma dynamics across brain regions and time windows.
Group-level analysis of noise-related neural costs in the STG revealed developmental enhancement of early high-gamma augmentation and diminution of delayed augmentation. Analysis of speech-related high-gamma activity demonstrated an anterior-to-posterior functional parcellation in the STG. The left anterior STG showed sustained augmentation throughout stimulus presentation, whereas the left posterior STG showed transient augmentation after stimulus onset. We found a double dissociation between the locations and developmental changes in speech sound-related high-gamma dynamics. Early left anterior STG high-gamma augmentation (i.e., within 200 ms post-stimulus onset) showed developmental enhancement, whereas delayed left posterior STG high-gamma augmentation declined with development.
Our observations support the model that, with age, the human STG refines neural dynamics to rapidly detect and subsequently disregard uninformative acoustic noises. Our study also supports the notion that the anterior-to-posterior functional division within the left STG is gradually strengthened for efficient speech-sound perception after birth.
语言习得的一个突出观点涉及通过功能重组来学习忽略不相关的听觉信号，从而更有效地处理相关信息。然而，很少有研究描述了支持在发育中的大脑中快速检测和随后忽略不相关听觉信息的神经时空动力学。为了解决这个未知问题，本研究使用在接受标准治疗的药物难治性局灶性癫痫患者中测量的颅内脑电图反应，对听觉处理的成本效益神经动力学的发育获得进行了建模。我们还提供了证据，证明了已知在成人 STG 中存在的颞上回（STG）前到后的功能分区的成熟。
我们研究了 32 名接受手术外脑电图（年龄范围：八个月至 28 岁）的患者，并分析了 2039 个位于发作起始区、间发性棘波产生区和 MRI 病变之外的颅内电极。在任务空闲期间，患者被给予正向（正常）语音、倒放语音和信号相关噪声。然后，我们使用 70-110 Hz 的高伽马幅度在给定的时间窗口量化与声音处理相关的神经成本，并在空间归一化的三维脑表面上动画化组水平的高伽马动力学。最后，我们确定年龄是否独立地影响大脑区域和时间窗口的高伽马动力学。
STG 中与噪声相关的神经成本的组水平分析显示，早期高伽马增强和延迟增强的减少增强。语音相关高伽马活动的分析显示，STG 中存在前到后的功能分区。左前 STG 在整个刺激呈现过程中显示出持续的增强，而左后 STG 在刺激开始后显示出短暂的增强。我们发现语音相关高伽马动力学的位置和发育变化之间存在双重分离。早期左前 STG 高伽马增强（即在刺激后 200 毫秒内）表现出发育增强，而延迟左后 STG 高伽马增强随发育而下降。
我们的观察结果支持这样的模型，即随着年龄的增长，人类 STG 会调整神经动力学，以快速检测和随后忽略无信息的声音。我们的研究还支持这样的观点，即在出生后，左 STG 中的前到后的功能分区逐渐增强，以实现有效的语音感知。
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