Coupled rhythms in early auditory cortex mirror speech acoustics

  1. Víctor J. López-Madrona
  2. Jérémy Giroud
  3. Manuel Mercier
  4. Léonardo Lancia
  5. Bruno L. Giordano
  6. Agnès Trébuchon
  7. David Poeppel
  8. Anne-Lise Giraud
  9. Luc H. Arnal
  10. Benjamin Morillon
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Abstract

Theta and gamma neural dynamics dominate the human auditory cortex during speech perception and have been proposed to track syllable boundaries and encode phonemic information, respectively. To what extent these rhythms engage intrinsic mechanisms or mirror the phase and frequency of the speech acoustics remains unsolved. Applying signal processing techniques from neuroscience to speech audio corpora from 17 languages, we found that canonical brain features —theta, gamma, and their phase-amplitude coupling— are distinctive and visible in the speech envelope. They represent syllabic rate (2–6 Hz), vocalic features (30–50 Hz), and fundamental frequency (100–150 Hz). Intracerebral (sEEG) recordings from the auditory cortex of 18 epilepsy patients revealed that theta-gamma dynamics and their coupling are absent at rest but emerge during speech perception, linearly driven by the acoustic envelope. These responses originate from distinct neural populations within overlapping auditory regions. Thus, theta-gamma auditory dynamics primarily mirror speech acoustics rather than being generated by endogenous mechanisms.

SIGNIFICANCE STATEMENT

Phase–amplitude coupling (PAC) is a fundamental coding principle in neuroscience, yet whether it is also exploited by natural communication signals has remained unknown. By applying PAC analyses to speech across 17 languages, we reveal that a theta–gamma coding scheme is embedded in the acoustic envelope itself. Using stereotactic EEG during naturalistic speech listening, we further show that theta and gamma oscillations are linearly driven by specific speech features (syllabic rate, vowel energy, fundamental frequency), each arising from distinct sources within primary auditory cortex. Overall, our results suggest that auditory theta–gamma PAC mirrors the rhythmic structure of speech, rather than being an intrinsic neural mechanism for encoding acoustic information.

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