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.

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Faculty Opinions recommendation of Rapid tuning shifts in human auditory cortex enhance speech intelligibility.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.727127476.793554522 ◽

2018 ◽

Author(s):

Pascal Mamassian ◽

Yves Boubenec

Keyword(s):

Auditory Cortex ◽

Speech Intelligibility ◽

Human Auditory Cortex

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Fine frequency tuning in monkey auditory cortex and thalamus

Journal of Neurophysiology ◽

10.1152/jn.00559.2010 ◽

2011 ◽

Vol 106 (2) ◽

pp. 849-859 ◽

Cited By ~ 28

Author(s):

Edward L. Bartlett ◽

Srivatsun Sadagopan ◽

Xiaoqin Wang

Keyword(s):

Auditory Cortex ◽

Auditory Nerve ◽

Animal Studies ◽

De Novo ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Auditory Pathway ◽

Nerve Fibers ◽

Frequency Resolution ◽

Human Auditory Cortex

The frequency resolution of neurons throughout the ascending auditory pathway is important for understanding how sounds are processed. In many animal studies, the frequency tuning widths are about 1/5th octave wide in auditory nerve fibers and much wider in auditory cortex neurons. Psychophysical studies show that humans are capable of discriminating far finer frequency differences. A recent study suggested that this is perhaps attributable to fine frequency tuning of neurons in human auditory cortex (Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I. Nature 451: 197–201, 2008). We investigated whether such fine frequency tuning was restricted to human auditory cortex by examining the frequency tuning width in the awake common marmoset monkey. We show that 27% of neurons in the primary auditory cortex exhibit frequency tuning that is finer than the typical frequency tuning of the auditory nerve and substantially finer than previously reported cortical data obtained from anesthetized animals. Fine frequency tuning is also present in 76% of neurons of the auditory thalamus in awake marmosets. Frequency tuning was narrower during the sustained response compared to the onset response in auditory cortex neurons but not in thalamic neurons, suggesting that thalamocortical or intracortical dynamics shape time-dependent frequency tuning in cortex. These findings challenge the notion that the fine frequency tuning of auditory cortex is unique to human auditory cortex and that it is a de novo cortical property, suggesting that the broader tuning observed in previous animal studies may arise from the use of anesthesia during physiological recordings or from species differences.

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FM-selective Networks in Human Auditory Cortex Revealed Using fMRI and Multivariate Pattern Classification

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00254 ◽

2012 ◽

Vol 24 (9) ◽

pp. 1896-1907 ◽

Cited By ~ 9

Author(s):

I-Hui Hsieh ◽

Paul Fillmore ◽

Feng Rong ◽

Gregory Hickok ◽

Kourosh Saberi

Keyword(s):

Auditory Cortex ◽

Pattern Analysis ◽

Primary Auditory Cortex ◽

Brain Regions ◽

Direction Selectivity ◽

Multivariate Pattern Analysis ◽

Acoustic Feature ◽

Complex Sounds ◽

Human Auditory Cortex ◽

Multivariate Pattern

Frequency modulation (FM) is an acoustic feature of nearly all complex sounds. Directional FM sweeps are especially pervasive in speech, music, animal vocalizations, and other natural sounds. Although the existence of FM-selective cells in the auditory cortex of animals has been documented, evidence in humans remains equivocal. Here we used multivariate pattern analysis to identify cortical selectivity for direction of a multitone FM sweep. This method distinguishes one pattern of neural activity from another within the same ROI, even when overall level of activity is similar, allowing for direct identification of FM-specialized networks. Standard contrast analysis showed that despite robust activity in auditory cortex, no clusters of activity were associated with up versus down sweeps. Multivariate pattern analysis classification, however, identified two brain regions as selective for FM direction, the right primary auditory cortex on the supratemporal plane and the left anterior region of the superior temporal gyrus. These findings are the first to directly demonstrate existence of FM direction selectivity in the human auditory cortex.

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Listening to speech in noisy scenes: Antithetical contribution of primary and non-primary auditory cortex

10.1101/2021.10.26.465858 ◽

2021 ◽

Author(s):

Lars Hausfeld ◽

Elia Formisano

Keyword(s):

Auditory Cortex ◽

Neural Activity ◽

Primary Auditory Cortex ◽

7 Tesla ◽

Non Invasive ◽

Temporal Sampling ◽

Brain Responses ◽

Electrophysiological Measurements ◽

Speech Envelope ◽

Limited Coverage

Invasive and non-invasive electrophysiological measurements during cocktail-party-like listening indicate that neural activity in human auditory cortex (AC) tracks the envelope of relevant speech. Due to the measurement s limited coverage and/or spatial resolution, however, the distinct contribution of primary and non-primary auditory areas remains unclear. Using 7-Tesla fMRI, here we measured brain responses of participants attending to one speaker, without and with another concurrent speaker. Using voxel-wise modeling, we observed significant speech envelope tracking in bilateral Heschl s gyrus (HG) and middle superior temporal sulcus (mSTS), despite the sluggish fMRI responses and slow temporal sampling. Neural activity was either positively (HG) or negatively (mSTS) correlated to the speech envelope. Spatial pattern analyses indicated that whereas tracking in HG reflected both relevant and (to a lesser extent) non-relevant speech, right mSTS selectively represented the relevant speech signal. These results indicate that primary and non-primary AC antithetically process ongoing speech suggesting a push-pull of acoustic and linguistic information.

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Functional Maps of Human Auditory Cortex: Effects of Acoustic Features and Attention

PLoS ONE ◽

10.1371/journal.pone.0005183 ◽

2009 ◽

Vol 4 (4) ◽

pp. e5183 ◽

Cited By ~ 82

Author(s):

David L. Woods ◽

G. Christopher Stecker ◽

Teemu Rinne ◽

Timothy J. Herron ◽

Anthony D. Cate ◽

...

Keyword(s):

Auditory Cortex ◽

Acoustic Features ◽

Human Auditory Cortex

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Spectral and Temporal Acoustic Features Modulate Response Irregularities within Primary Auditory Cortex Columns

PLoS ONE ◽

10.1371/journal.pone.0114550 ◽

2014 ◽

Vol 9 (12) ◽

pp. e114550

Author(s):

Andres Carrasco ◽

Trecia A. Brown ◽

Stephen G. Lomber

Keyword(s):

Auditory Cortex ◽

Primary Auditory Cortex ◽

Acoustic Features

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Neural tracking as an objective measure of auditory perception and speech intelligibility

10.1101/2021.11.26.470129 ◽

2021 ◽

Author(s):

Jana Van Canneyt ◽

Marlies Gillis ◽

Jonas Vanthornhout ◽

Tom Francart

Keyword(s):

Speech Perception ◽

Auditory Cortex ◽

Speech Intelligibility ◽

Objective Assessment ◽

Objective Measure ◽

Primary Auditory Cortex ◽

Auditory Pathway ◽

Natural Speech ◽

Linguistic Features ◽

The Brain

The neural tracking framework enables the analysis of neural responses (EEG) to continuous natural speech, e.g., a story or a podcast. This allows for objective investigation of a range of auditory and linguistic processes in the brain during natural speech perception. This approach is more ecologically valid than traditional auditory evoked responses and has great potential for both research and clinical applications. In this article, we review the neural tracking framework and highlight three prominent examples of neural tracking analyses. This includes the neural tracking of the fundamental frequency of the voice (f0), the speech envelope and linguistic features. Each of these analyses provides a unique point of view into the hierarchical stages of speech processing in the human brain. f0-tracking assesses the encoding of fine temporal information in the early stages of the auditory pathway, i.e. from the auditory periphery up to early processing in the primary auditory cortex. This fundamental processing in (mostly) subcortical stages forms the foundation of speech perception in the cortex. Envelope tracking reflects bottom-up and top-down speech-related processes in the auditory cortex, and is likely necessary but not sufficient for speech intelligibility. To study neural processes more directly related to speech intelligibility, neural tracking of linguistic features can be used. This analysis focuses on the encoding of linguistic features (e.g. word or phoneme surprisal) in the brain. Together these analyses form a multi-faceted and time-effective objective assessment of the auditory and linguistic processing of an individual.

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Multiscale integration organizes hierarchical computation in human auditory cortex

10.1101/2020.09.30.321687 ◽

2020 ◽

Cited By ~ 1

Author(s):

Sam V Norman-Haignere ◽

Laura K. Long ◽

Orrin Devinsky ◽

Werner Doyle ◽

Ifeoma Irobunda ◽

...

Keyword(s):

Auditory Cortex ◽

Temporal Analysis ◽

Acoustic Features ◽

Human Epilepsy ◽

Neural Integration ◽

Neural Computations ◽

Novel Method ◽

Human Auditory Cortex ◽

Hierarchical Computation ◽

Intracranial Recordings

AbstractTo derive meaning from sound, the brain must integrate information across tens (e.g. phonemes) to hundreds (e.g. words) of milliseconds, but the neural computations that enable multiscale integration remain unclear. Prior evidence suggests that human auditory cortex analyzes sound using both generic acoustic features (e.g. spectrotemporal modulation) and category-specific computations, but how these putatively distinct computations integrate temporal information is unknown. To answer this question, we developed a novel method to estimate neural integration periods and applied the method to intracranial recordings from human epilepsy patients. We show that integration periods increase three-fold as one ascends the auditory cortical hierarchy. Moreover, we find that electrodes with short integration periods (~50-150 ms) respond selectively to spectrotemporal modulations, while electrodes with long integration periods (~200-300 ms) show prominent selectivity for sound categories such as speech and music. These findings reveal how multiscale temporal analysis organizes hierarchical computation in human auditory cortex.

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Multivoxel codes for representing and integrating acoustic features in human cortex

10.1101/730234 ◽

2019 ◽

Author(s):

Ediz Sohoglu ◽

Sukhbinder Kumar ◽

Maria Chait ◽

Timothy D. Griffiths

Keyword(s):

Auditory Cortex ◽

Parietal Cortex ◽

Posterior Parietal Cortex ◽

Activity Patterns ◽

Primary Auditory Cortex ◽

Neural Representation ◽

Acoustic Features ◽

Human Cortex ◽

Spectral Frequency ◽

Multivariate Pattern

AbstractUsing fMRI and multivariate pattern analysis, we determined whether acoustic features are represented by independent or integrated neural codes in human cortex. Male and female listeners heard band-pass noise varying simultaneously in spectral (frequency) and temporal (amplitude-modulation [AM] rate) features. In the superior temporal plane, changes in multivoxel activity due to frequency were largely invariant with respect to AM rate (and vice versa), consistent with an independent representation. In contrast, in posterior parietal cortex, neural representation was exclusively integrated and tuned to specific conjunctions of frequency and AM features. Direct between-region comparisons show that whereas independent coding of frequency and AM weakened with increasing levels of the hierarchy, integrated coding strengthened at the transition between non-core and parietal cortex. Our findings support the notion that primary auditory cortex can represent component acoustic features in an independent fashion and suggest a role for parietal cortex in feature integration and the structuring of acoustic input.Significance statementA major goal for neuroscience is discovering the sensory features to which the brain is tuned and how those features are integrated into cohesive perception. We used whole-brain human fMRI and a statistical modeling approach to quantify the extent to which sound features are represented separately or in an integrated fashion in cortical activity patterns. We show that frequency and AM rate, two acoustic features that are fundamental to characterizing biological important sounds such as speech, are represented separately in primary auditory cortex but in an integrated fashion in parietal cortex. These findings suggest that representations in primary auditory cortex can be simpler than previously thought and also implicate a role for parietal cortex in integrating features for coherent perception.

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