High-resolution fMRI reveals a dorsal brain pathway selective for conspecific vocalizations in macaques.

Imaging neuroscience (Cambridge, Mass.) Pub Date : 2025-08-13 eCollection Date: 2025-01-01 DOI:10.1162/IMAG.a.108
Mathilda Froesel, Koh Ikuchi, Qi Zhu, Haiyan Wang, Marc Hauser, Suliann Ben Hamed, Wim Vanduffel
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Abstract

Understanding the neural basis of social communication and vocal perception in primates is a key challenge in systems neuroscience. Vocalizations are fundamental for communication, and several cortical areas, known as "voice patches," have been identified as being sensitive to conspecific vocalizations in primates, vital for distinguishing species-specific calls. While the dorsal stream's role in complex auditory-motor functions and human speech processing is established, its specific contribution to processing species-specific vocalizations in non-human primates remains unclear. Using high-resolution fMRI (0.6 mm isotropic voxels), we investigated brain regions involved in processing vocalizations in awake rhesus monkeys exposed to coos, screams, and aggressive calls, among control sounds. Our analyses revealed a widespread network involved in vocalization processing, encompassing auditory-associated areas including the core and belt auditory cortices, as well as premotor, and somatosensory-related areas. Moreover, we found selective activation in the caudal part of the lateral sulcus (area Tpt) and the dorsal premotor cortex (area 6DR/F2) in response to vocalizations. Also, the population responses in these areas could discriminate between different vocalizations. Our results enhance our understanding of the neural basis of vocal communication in primates. Specifically, they highlight the involvement of a voice-related dorsal network in macaques, including Tpt and part of 6DR/F2, in processing the acoustic features of salient vocal stimuli, potentially linking them to motor representations. These findings provide insights into potential evolutionary precursors of auditory-motor pathways that support complex auditory communication systems in primates, including human speech.

高分辨率功能磁共振成像揭示了猕猴的背侧脑通路选择性的同向发声。
理解灵长类动物社会沟通和声音感知的神经基础是系统神经科学的一个关键挑战。发声是沟通的基础,在灵长类动物的大脑皮层中,有几个被称为“声音补丁”的区域被认为对同种发声很敏感,这对于区分物种特异性的叫声至关重要。虽然背流在复杂的听觉-运动功能和人类语言处理中的作用已经确立,但它在处理非人类灵长类动物特定物种发声方面的具体贡献仍不清楚。利用高分辨率的功能磁共振成像(0.6毫米各向同性体素),我们研究了清醒的猕猴在接触到咕噜声、尖叫声和攻击性叫声以及控制声音时处理发声的大脑区域。我们的分析揭示了一个广泛参与发声处理的网络,包括听觉相关区域,包括核心和听觉带皮层,以及前运动和体感相关区域。此外,我们发现侧沟尾侧部分(Tpt区)和背侧运动前皮层(6DR/F2区)在响应鸣叫时选择性激活。此外,这些区域的种群反应可以区分不同的发声。我们的研究结果增强了我们对灵长类动物声音交流的神经基础的理解。具体来说,他们强调了猕猴中与声音相关的背侧网络的参与,包括Tpt和部分6DR/F2,在处理显著声音刺激的声学特征时,可能将它们与运动表征联系起来。这些发现为支持包括人类语言在内的灵长类动物复杂听觉交流系统的听觉-运动通路的潜在进化前体提供了见解。
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