Combining ultra-high-field fMRI adaptation and computational modelling to estimate neuronal frequency selectivity in human auditory cortex

Frequency selectivity is a ubiquitous property of auditory neurons. Measuring it in human auditory cortex may be crucial for understanding common auditory deficits, but current non-invasive neuroimaging techniques can only measure the aggregate response of large populations of cells, thereby overestimating tuning width. Here we attempted to estimate neuronal frequency tuning in human auditory cortex using a combination of fMRI-adaptation paradigm at 7T and computational modelling. We measured the BOLD response in the auditory cortex of eleven participants to a high frequency (3.8 kHz) probe presented alone or preceded by adaptors at different frequencies (0.5 to 3.8 kHz). From these data, we derived both the response tuning curves (the BOLD response to adaptors alone as a function of adaptor frequency) and adaptation tuning curves (the degree of response suppression to the probe as a function of adaptor frequency, assumed to reflect neuronal tuning) in primary and secondary auditory cortical areas, delineated in each participant. Results suggested the existence of both frequency-independent and frequency-specific adaptation components, with the latter being more frequency-tuned than response tuning curves. Using a computational model of neuronal adaptation and BOLD non-linearity in topographically-organized cortex, we demonstrate both that the frequency-specific adaptation component overestimates the underlying neuronal frequency tuning and that frequency-specific and frequency-independent adaptation component cannot easily be disentangled from the adaptation tuning curve. By fitting our model directly to the response and adaptation tuning curves, we derive a range of plausible values for neuronal frequency tuning. Our results suggest that fMRI adaptation is suitable for measuring neuronal frequency tuning properties in human auditory cortex, provided population effects and the non-linearity of BOLD response are taken into account.

Two Stages of Speech Envelope Tracking in Human Auditory Cortex Modulated by Speech Intelligibility

The envelope is essential for speech perception. Recent studies have shown that cortical activity can track the acoustic envelope. However, whether the tracking strength reflects the extent of speech intelligibility processing remains controversial. Here, using stereo-electroencephalogram (sEEG) technology, we directly recorded the activity in human auditory cortex while subjects listened to either natural or noise-vocoded speech. These two stimuli have approximately identical envelopes, but the noise-vocoded speech does not have speech intelligibility. We found two stages of envelope tracking in auditory cortex: an early high-γ (60-140 Hz) power stage (delay ≈ 49 ms) that preferred the noise-vocoded speech, and a late θ (4-8 Hz) phase stage (delay ≈ 178 ms) that preferred the natural speech. Furthermore, the decoding performance of high-γ power was better in primary auditory cortex than in non-primary auditory cortex, consistent with its short tracking delay. We also found distinct lateralization effects: high-γ power envelope tracking dominated left auditory cortex, while θ phase showed better decoding performance in right auditory cortex. In sum, we suggested a functional dissociation between high-γ power and θ phase: the former reflects fast and automatic processing of brief acoustic features, while the latter correlates to slow build-up processing facilitated by speech intelligibility.

Naturalistic Audiovisual Stimulation Reveals the Topographic Organization of Human Auditory Cortex

Despite the importance of audition in spatial, semantic, and social function, there is no consensus regarding the detailed organisation of human auditory cortex. Using a novel computational model to analyse a high-powered naturalistic audiovisual movie-watching dataset, we simultaneously estimate spectral tuning properties and category selectivity to reveal the modes of organisation and computational motifs that characterise human auditory cortex. We find that regions more remote from the auditory core exhibit more compressive, non-linear response properties and finely-tuned, speech-selective receptive fields in low frequency portions of the tonotopic map. These patterns of organisation mirror aspects of the visual cortical hierarchy, wherein tuning properties progress from a stimulus category-agnostic front end towards more advanced regions increasingly optimised for behaviorally relevant stimulus categories.

Neural representations of own-voice in the human auditory cortex

We have a keen sensitivity when it comes to the perception of our own voices. We can detect not only the differences between ourselves and others, but also slight modifications of our own voices. Here, we examined the neural correlates underlying such sensitive perception of one’s own voice. In the experiments, we modified the subjects’ own voices by using five types of filters. The subjects rated the similarity of the presented voices to their own. We compared BOLD (Blood Oxygen Level Dependent) signals between the voices that subjects rated as least similar to their own voice and those they rated as most similar. The contrast revealed that the bilateral superior temporal gyrus exhibited greater activities while listening to the voice least similar to their own voice and lesser activation while listening to the voice most similar to their own. Our results suggest that the superior temporal gyrus is involved in neural sharpening for the own-voice. The lesser degree of activations observed by the voices that were similar to the own-voice indicates that these areas not only respond to the differences between self and others, but also respond to the finer details of own-voices.