Formant-frequency encoding in the inferior colliculus of awake rabbit: Physiological and model responses

Most neurons in the inferior colliculus (IC), a key integration hub in the ascending auditory pathway, are sensitive to important features of vowels, periodic sounds with spectral peaks referred to as formants. A recent psychoacoustic study found that increased formant bandwidth elevates formant-frequency discrimination thresholds in human listeners, hypothesized to be due to reduced neural fluctuation (NF) contrast along the tonotopic axis (Carney et al., 2023). The current study tested this hypothesis and investigated the neural mechanisms underlying IC responses in awake rabbit to single-formant, synthetic, vowel-like stimuli with varied bandwidths. Formant frequencies were shifted past the neural characteristic frequency to infer response profiles across the tonotopic axis. The NF profile is converted into a rate-place profile by IC neurons that are sensitive to amplitude modulations. Two stimulus paradigms were used to assess the role of energy cues, which vary when formant bandwidths are changed: one matched the overall levels of synthetic formants across conditions, and the other matched the peak levels. The discharge-rate profiles as a function of formant bandwidth were consistent across both paradigms, thus energy alone did not determine IC rates, which were typically higher for narrower formant bandwidths. Formant-frequency discrimination thresholds estimated from single-neuron responses were higher than human thresholds but had similar trends. IC neurons are also sensitive to fast frequency sweeps (chirps) which are present in vowels; formant-frequency discrimination thresholds based on neural responses were correlated with the sensitivity of IC neurons to chirp velocity but not direction. Responses of IC neurons with band-suppressed, but not band-enhanced, modulation transfer functions supported the hypothesis that IC neurons encode vowels as predicted by neural-fluctuation profiles. Trends in responses of IC neurons with both types of modulation transfer function were explained for a range of formant bandwidths and both stimulus paradigms by a model with same-frequency inhibition and excitation plus broadband, modulation-sensitive inhibition.