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

TL;DR

This study shows that light anesthesia preserves basic auditory processing in macaques but alters higher-order voice perception, affecting how brain regions respond to vocalizations.

Contribution

The study introduces a near-awake anesthesia protocol for fMRI that preserves primary auditory function while revealing altered higher-order processing in vocalization-sensitive regions.

Findings

Primary and belt auditory cortices showed robust activation to complex sounds under anesthesia.

Voice-sensitive responses in anterior temporal voice areas were absent, but emerged in ventral premotor and prefrontal cortices.

Anesthetized fMRI is suitable for studying basic auditory functions but may not capture higher-order voice perception accurately.

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.

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.

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