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Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

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Abstract

Vowels make a strong contribution to speech perception under natural conditions. Vowels are encoded in the auditory nerve primarily through neural synchrony to temporal fine structure and to envelope fluctuations rather than through average discharge rate. Neural synchrony is thought to contribute less to vowel coding in central auditory nuclei, consistent with more limited synchronization to fine structure and the emergence of average-rate coding of envelope fluctuations. However, this hypothesis is largely unexplored, especially in background noise. The present study examined coding mechanisms at the level of the midbrain that support behavioral sensitivity to simple vowel-like sounds using neurophysiological recordings and matched behavioral experiments in the budgerigar. Stimuli were harmonic tone complexes with energy concentrated at one spectral peak, or formant frequency, presented in quiet and in noise. Behavioral thresholds for formant-frequency discrimination decreased with increasing amplitude of stimulus envelope fluctuations, increased in noise, and were similar between budgerigars and humans. Multiunit recordings in awake birds showed that the midbrain encodes vowel-like sounds both through response synchrony to envelope structure and through average rate. Whereas neural discrimination thresholds based on either coding scheme were sufficient to support behavioral thresholds in quiet, only synchrony-based neural thresholds could account for behavioral thresholds in background noise. These results reveal an incomplete transformation to average-rate coding of vowel-like sounds in the midbrain. Model simulations suggest that this transformation emerges due to modulation tuning, which is shared between birds and mammals. Furthermore, the results underscore the behavioral relevance of envelope synchrony in the midbrain for detection of small differences in vowel formant frequency under real-world listening conditions.

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Acknowledgments

This work was supported by National Institutes of Health Grants R01-DC001641 to L.H.C. and R00-DC013792 to K.S.H. Mitchell L. Day provided analysis code for calculating the discrimination performance of optimally pooled neural populations.

Author Contributions

KSH, JF, FI, and LHC designed the research; KSH, KSA, MJM, and EGN performed the experiments; KSH, KSA, MJM, FI, and LHC analyzed the data; and KSH wrote the manuscript.

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Authors and Affiliations

  1. Department of Biomedical Engineering, University of Rochester, Rochester, NY, 14642, USA

    Kenneth S. Henry, Johanna Forst, Matthew J. Mender & Laurel H. Carney

  2. Department of Neuroscience, University of Rochester, Rochester, NY, 14642, USA

    Kristina S. Abrams & Laurel H. Carney

  3. Department of Psychology, University at Buffalo, Buffalo, NY, 14260, USA

    Erikson G. Neilans

  4. Department of Psychological and Brain Sciences, Boston University, Boston, MA, 02215, USA

    Fabio Idrobo

  5. Universidad de Los Andes, Bogotá, Colombia

    Fabio Idrobo

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  1. Kenneth S. Henry
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  2. Kristina S. Abrams
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  3. Johanna Forst
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Correspondence to Kenneth S. Henry.

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Henry, K.S., Abrams, K.S., Forst, J. et al. Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise. JARO 18, 165–181 (2017). https://doi.org/10.1007/s10162-016-0594-4

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