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Rate and Temporal Coding of Regular and Irregular Pulse Trains in Auditory Midbrain of Normal-Hearing and Cochlear-Implanted Rabbits

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Abstract

Although pitch is closely related to temporal periodicity, stimuli with a degree of temporal irregularity can evoke a pitch sensation in human listeners. However, the neural mechanisms underlying pitch perception for irregular sounds are poorly understood. Here, we recorded responses of single units in the inferior colliculus (IC) of normal hearing (NH) rabbits to acoustic pulse trains with different amounts of random jitter in the inter-pulse intervals and compared with responses to electric pulse trains delivered through a cochlear implant (CI) in a different group of rabbits. In both NH and CI animals, many IC neurons demonstrated tuning of firing rate to the average pulse rate (APR) that was robust against temporal jitter, although jitter tended to increase the firing rates for APRs ≥ 1280 Hz. Strength and limiting frequency of spike synchronization to stimulus pulses were also comparable between periodic and irregular pulse trains, although there was a slight increase in synchronization at high APRs with CI stimulation. There were clear differences between CI and NH animals in both the range of APRs over which firing rate tuning was observed and the prevalence of synchronized responses. These results suggest that the pitches of regular and irregular pulse trains are coded differently by IC neurons depending on the APR, the degree of irregularity, and the mode of stimulation. In particular, the temporal pitch produced by periodic pulse trains lacking spectral cues may be based on a rate code rather than a temporal code at higher APRs.

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Acknowledgements

The authors thank Connie Miller, Melissa McKinnon, Camille Shaw, Alice Gelman, and Joseph Wagner for surgical assistance and Cochlear Ltd. for providing the cochlear implants.

Funding

This work was supported by National Institutes of Health grants R01 DC002258 and R01 DC005775 to BD.

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Authors and Affiliations

  1. Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, MA, USA

    Yaqing Su, Yoojin Chung, Dan F. M. Goodman, Kenneth E. Hancock & Bertrand Delgutte

  2. Department of Biomedical Engineering, Boston University, Boston, MA, USA

    Yaqing Su

  3. Department of Basic Neurosciences, University of Geneva, Geneva, Switzerland

    Yaqing Su

  4. Department of Otolaryngology, Harvard Medical School, Boston, MA, USA

    Yoojin Chung, Dan F. M. Goodman, Kenneth E. Hancock & Bertrand Delgutte

  5. Present Address: Department of Electrical and Electronic Engineering, Imperial College London, London, England

    Dan F. M. Goodman

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  1. Yaqing Su
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Contributions

BD, YS, and YC designed the study. YS, YC, DG, and KH collected the data. BD, YS, YC, and KH analyzed the data. BD and YS wrote the manuscript. BD, YS, YC, DG, and KH edited the manuscript and approved the final version.

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Correspondence to Yaqing Su or Bertrand Delgutte.

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Animal procedures were approved by the Animal Care Committee of Massachusetts Eye and Ear.

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Su, Y., Chung, Y., Goodman, D.F.M. et al. Rate and Temporal Coding of Regular and Irregular Pulse Trains in Auditory Midbrain of Normal-Hearing and Cochlear-Implanted Rabbits. JARO 22, 319–347 (2021). https://doi.org/10.1007/s10162-021-00792-5

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