Pitch of Harmonic Complex Tones: Rate-Place Coding of Resolved Components in Harmonic and Inharmonic Complex Tones in Auditory Midbrain

Abstract

Financial conflicts:The authors declare no competing financial interests. Acknowledgement:This work is supported by NIH grant R01 DC 002258. We thank Yoojin Chung for help with experimental procedures, Ken Hancock for technical support, Oded Barzelay for providing the algorithm for estimating characteristic frequency, Kameron Clayton for providing the fitting of rabbit auditory nerve bandwidth, Camille Shaw, Alice Gelman, and Joseph Wagner for assisting with surgeries. AbstractHarmonic complex tones (HCT) commonly occurring in speech and music evoke a strong pitch at their fundamental frequency (F0), especially when they contain harmonics individually resolved by the cochlea. When all frequency components of an HCT are shifted by the same amount, the pitch of the resulting inharmonic tone (IHCT) also shifts although the envelope repetition rate is unchanged. A rateplace code whereby resolved harmonics are represented by local maxima in firing rates along the tonotopic axis has been characterized in the auditory nerve and primary auditory cortex, but little is known about intermediate processing stages. We recorded single neuron responses to HCT and IHCT with varying F0 and sound level in the inferior colliculus (IC) of unanesthetized rabbits. Many neurons showed peaks in firing rates when a low-numbered harmonic aligned with the neuron's characteristic frequency, demonstrating "rate-place" coding. The IC rate-place code was most prevalent for F0>800 Hz, was only moderately dependent on sound level over a 40 dB range, and was not sensitive to stimulus harmonicity. A spectral receptive-field model incorporating broadband inhibition better predicted the neural responses than a purely excitatory model, suggesting an enhancement of the rate-place representation by inhibition. Some IC neurons showed facilitation in response to HCT, similar to cortical "harmonic template neurons" (Feng and Wang 2017), but to a lesser degree. Our findings shed light on the transformation of rate-place coding of resolved harmonics along the auditory pathway, and suggest a gradual emergence of harmonic templates from low to high processing centers. Significance statementHarmonic complex tones are ubiquitous in speech and music and produce strong pitch percepts in human listeners when they contain frequency components that are individually resolved by the cochlea.Here, we characterize a "rate-place" code for resolved harmonics in the auditory midbrain that is more robust across sound levels than the peripheral rate-place code and insensitive to the harmonic relationships among frequency components. We use a computational model to show that inhibition may play an important role in shaping the rate-place code. We also show that midbrain auditory neurons can demonstrate similar properties as cortical harmonic template neurons. Our study fills a gap in understanding the transformation in neural representations of resolved harmonics along the auditory pathway.

Human discrimination and modeling of high-frequency complex tones shed light on the neural codes for pitch

“…The rate-place observer tended to be more sensitive to changes in level than the all-information observer ( Fig 8A ). Generally, rate-place thresholds were poorer at higher levels, consistent with the fact that higher levels degrade representations of stimulus harmonics in the average rate responses of auditory-nerve fibers [ 61 ]. At much higher levels, rate-place thresholds worsened significantly, consistent with saturation of the simulated high-spontaneous-rate fibers at high levels ( S3 Text ).…”