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Neural substrates of vocalization feedback monitoring in primate auditory cortex

Abstract

Vocal communication involves both speaking and hearing, often taking place concurrently. Vocal production, including human speech and animal vocalization, poses a number of unique challenges for the auditory system. It is important for the auditory system to monitor external sounds continuously from the acoustic environment during speaking despite the potential for sensory masking by self-generated sounds1. It is also essential for the auditory system to monitor feedback of one’s own voice. This self-monitoring may play a part in distinguishing between self-generated or externally generated2,3auditory inputs and in detecting errors in our vocal production4. Previous work in humans5,6,7,8,9,10 and other animals11,12,13 has demonstrated that the auditory cortex is largely suppressed during speaking or vocalizing. Despite the importance of self-monitoring, the underlying neural mechanisms in the mammalian brain, in particular the role of vocalization-induced suppression, remain virtually unknown. Here we show that neurons in the auditory cortex of marmoset monkeys (Callithrix jacchus) are sensitive to auditory feedback during vocal production, and that changes in the feedback alter the coding properties of these neurons. Furthermore, we found that the previously described cortical suppression during vocalization actually increased the sensitivity of these neurons to vocal feedback. This heightened sensitivity to vocal feedback suggests that these neurons may have an important role in auditory self-monitoring.

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Figure 1: Examples of vocal suppression and excitation during altered feedback.
Figure 2: Feedback effects in suppressed and excited neural populations.
Figure 3: Population responses to altered feedback.
Figure 4: Auditory responses and feedback sensitivity.

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Acknowledgements

We thank B. McNaughton for sharing implanted multi-electrode recording methods. We acknowledge A. Pistorio for assistance in animal care, M. Melamed for assistance in data collection and C. Miller for his comments on this manuscript. This work was supported by NIH grants to X.W.

Author Contributions S.J.E. and X.W. designed the experiments and co-wrote the paper. S.J.E. carried out the experimental recordings and data analysis.

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Correspondence to Steven J. Eliades or Xiaoqin Wang.

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The file contains Supplementary Methods, Supplementary Discussion, additional references and Supplementary Figures S1-S10 with Legends. (PDF 6914 kb)

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Eliades, S., Wang, X. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 453, 1102–1106 (2008). https://doi.org/10.1038/nature06910

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