Phase Alignment of Low-Frequency Neural Activity to the Amplitude Envelope of Speech Reflects Evoked Responses to Acoustic Edges, Not Oscillatory Entrainment
- Yulia Oganian1,2,*,
- Katsuaki Kojima1,3,4,5,6,*,
- Assaf Breska7,
- Chang Cai3,
- Anne Findlay3,
- Edward F. Chang1,†, and
- Srikantan S. Nagarajan3,†
- 1Department of Neurological Surgery, University of California–San Francisco, San Francisco, California 94158
- 2Center for Integrative Neuroscience, University Medical Center Tuebingen, Tuebingen 72076, Germany
- 3Department of Radiology, University of California–San Francisco, San Francisco, California 94143-0628
- 4Department of Pediatrics, University of California, San Francisco, Box 0734, 550 16th Street, 5th Floor, San Francisco, CA 94158, USA
- 5Neurodevelomental Disorders Prevention Center, Perinatal Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio 45229-3039
- 6Department of Pediatrics, University of Cincinnati College of Medicine, 3230 Eden Avenue, Cincinnati, OH 45267
- 7Max-Planck-Institute for biological Cybernetics, Tuebingen 72076, Germany
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Author contributions: Y.O., K.K., E.F.C., and S.S.N. designed research; Y.O., K.K., C.C., and A.F. performed research; Y.O., A.B., and C.C. contributed unpublished reagents/analytic tools; Y.O., K.K., A.B., and S.S.N. analyzed data; Y.O. and K.K. wrote the first draft of the paper; Y.O., K.K., A.B., E.F.C., and S.S.N. edited the paper; Y.O. wrote the paper.
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↵*Y.O. and K.K. contributed equally to this work.
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↵†E.F.C. and S.S.N. contributed equally to this work.
Abstract
The amplitude envelope of speech is crucial for accurate comprehension. Considered a key stage in speech processing, the phase of neural activity in the theta-delta bands (1-10 Hz) tracks the phase of the speech amplitude envelope during listening. However, the mechanisms underlying this envelope representation have been heavily debated. A dominant model posits that envelope tracking reflects entrainment of endogenous low-frequency oscillations to the speech envelope. Alternatively, envelope tracking reflects a series of evoked responses to acoustic landmarks within the envelope. It has proven challenging to distinguish these two mechanisms. To address this, we recorded MEG while participants (n = 12, 6 female) listened to natural speech, and compared the neural phase patterns to the predictions of two computational models: an oscillatory entrainment model and a model of evoked responses to peaks in the rate of envelope change. Critically, we also presented speech at slowed rates, where the spectro-temporal predictions of the two models diverge. Our analyses revealed transient theta phase-locking in regular speech, as predicted by both models. However, for slow speech, we found transient theta and delta phase-locking, a pattern that was fully compatible with the evoked response model but could not be explained by the oscillatory entrainment model. Furthermore, encoding of acoustic edge magnitudes was invariant to contextual speech rate, demonstrating speech rate normalization of acoustic edge representations. Together, our results suggest that neural phase-locking to the speech envelope is more likely to reflect discrete representation of transient information rather than oscillatory entrainment.
SIGNIFICANCE STATEMENT This study probes a highly debated topic in speech perception: the neural mechanisms underlying the cortical representation of the temporal envelope of speech. It is well established that the slow intensity profile of the speech signal, its envelope, elicits a robust brain response that “tracks” these envelope fluctuations. The oscillatory entrainment model posits that envelope tracking reflects phase alignment of endogenous neural oscillations. Here the authors provide evidence for a distinct mechanism. They show that neural speech envelope tracking arises from transient evoked neural responses to rapid increases in the speech envelope. Explicit computational modeling provides direct and compelling evidence that evoked responses are the primary mechanism underlying cortical speech envelope representations, with no evidence for oscillatory entrainment.
- Received August 23, 2022.
- Revision received February 27, 2023.
- Accepted March 2, 2023.
- Copyright © 2023 Oganian et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.





