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bioRxiv · 10.1101/2025.01.10.632201

Dynamic Norm-Based Coding of Vocal Identity in the Primate Auditory Cortex

Esposito, Y.·Boe, L.-J.·Trapeau, R.·Renaud, L.·Brochier, T.·Giamundo, M.·Belin, P.
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Abstract

Recognition of vocal identity is essential for primate social behavior, yet the neural mechanisms supporting this ability remain poorly understood. Cognitive models suggest that the brain may represent identity based on an average voice prototype. Here, we tested this hypothesis by recording spiking activity from single neurons in an fMRI-localized voice-selective region of the anterior temporal lobe in two rhesus macaques. Using synthetic "coo" calls systematically morphed along identity trajectories from "anti-voices" to caricatures, we found that early neuronal responses ([~]100 ms post-stimulus) exhibited robust V-shaped tuning to distance from the average voice. This pattern reflects an energy-efficient representational strategy in which neural activity increases with identity distinctiveness, also applied to face stimuli. Unexpectedly, a distinct subpopulation of neurons showed a delayed ([~]200 ms) rebound response selectively enhanced for the average voice. These findings reveal two temporally dissociable mechanisms for vocal identity encoding in primate auditory cortex, suggesting that the brain emphasizes both distinctiveness and prototypicality to support efficient and flexible voice recognition. Significance statementRecognizing who is speaking is fundamental to primate social life, yet how the brain encodes vocal identity remains poorly understood. Cognitive theories suggest that the brain may represent identity relative to an internal "average" voice, but direct neural evidence has been lacking. Here, we recorded single-neuron activity in a voice-selective brain region of rhesus macaques and found two distinct coding strategies: one that increases neural activity with identity distinctiveness, and another that selectively enhances the average voice itself. These results reveal dual mechanisms for vocal identity encoding in the primate brain, highlighting how the brain balances flexibility and efficiency in social communication.

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Esposito, Y., Boe, L.-J., Trapeau, R., Renaud, L., Brochier, T., Giamundo, M., Belin, P.. 2025-01-12. Dynamic Norm-Based Coding of Vocal Identity in the Primate Auditory Cortex. https://doi.org/10.1101/2025.01.10.632201

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