Functional mapping of auditory responses to complex sounds under light anesthesia in rhesus macaques

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  1. Régis Trapeau ,  
  2. Luc Renaud
    ,  
  3. Melina Cordeau ,  
  4. Yoan Esposito ,  
  5. Pascal Belin
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Abstract

We investigated the auditory responses of anesthetized rhesus macaques to complex natural sounds using functional magnetic resonance imaging (fMRI) and a near-awake anesthesia protocol combining low-dose sevoflurane and dexmedetomidine. Eleven animals were scanned while listening to macaque vocalizations and non-vocal sounds. Robust activation was observed in primary and belt auditory cortices as well as subcortical structures, indicating preserved auditory responsiveness under anesthesia. However, unlike in awake animals, selective responses to vocalizations in anterior temporal voice areas (aTVAs) were absent. Instead, vocalization sensitivity emerged in the ventral premotor cortex, prefrontal cortex, and posterior middle temporal gyrus, regions associated with the dorsal auditory stream and multisensory integration. These findings suggest that while anesthesia preserves basic auditory processing, it modulates higher-order cortical responses involved in voice perception. Anesthetized fMRI thus offers a valuable tool for large-scale studies of primary auditory functions, while it must be approached with caution when studying higher-order auditory functions.

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Plain summary

Understanding how primates process sounds, especially vocalizations, is essential to uncovering the roots of human speech and communication. Typically, this kind of brain research in monkeys is done while the animals are awake, which is challenging and time-consuming. In this study, we used a gentle anesthesia protocol in eleven macaques to see if their brains could still respond to different types of sounds during functional magnetic resonance imaging. We found strong responses in early auditory regions, showing that these parts of the brain still process complex sounds under light anesthesia. However, auditory areas usually involved in processing voices in awake animals did not show the same patterns. Surprisingly, some areas linked to action and multisensory processing were still sensitive to vocalizations. This means that while light anesthesia can help with large-scale brain studies of basic hearing, it may not fully reveal how the brain processes more complex sounds like voices.

Corresponding author
Régis Trapeau
Grant information

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 788240). This work was performed in the Center IRM-INT (UMR 7289, AMU-CNRS), platform member of France Life Imaging network (grant ANR-11-INBS-0006).

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright
© 2025 Régis Trapeau (Corresponding Author, Co-Author); Luc Renaud (Co-Author); Melina Cordeau (Co-Author); Yoan Esposito (Co-Author); Pascal Belin (Co-Author) Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

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Authors & roles

Régis Trapeau

Institut de Neurosciences de la Timone, Aix-Marseille Université, UMR 7289 CNRS, Marseille, Provence-Alpes-Côte d'Azur, 13005, France

Roles
Corresponding Author, Co-Author, Conceptualization, Data Curation, Formal Analysis, Investigation, Methodology, Software, Visualization, Writing – Original Draft Preparation, Writing – Review & Editing

Luc Renaud

Institut de Neurosciences de la Timone, Aix-Marseille Université, UMR 7289 CNRS, Marseille, Provence-Alpes-Côte d'Azur, 13005, France

Roles
Co-Author, Conceptualization, Investigation, Methodology, Writing – Review & Editing

Melina Cordeau

Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA

Roles
Co-Author, Investigation, Methodology, Writing – Review & Editing

Yoan Esposito

Institut de Neurosciences de la Timone, Aix-Marseille Université, UMR 7289 CNRS, Marseille, Provence-Alpes-Côte d'Azur, 13005, France

Roles
Co-Author, Investigation, Writing – Review & Editing

Pascal Belin

Institut de Neurosciences de la Timone, Aix-Marseille Université, UMR 7289 CNRS, Marseille, Provence-Alpes-Côte d'Azur, 13005, France

Institute of Language Communication and the Brain, Marseille, Provence-Alpes-Côte d'Azur, 13000, France

Roles
Co-Author, Conceptualization, Funding Acquisition, Methodology, Project Administration, Supervision, Writing – Review & Editing

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