[Paper Review] Rhythmic production of consonant-vowel syllables synchronizes traveling waves in speech-processing brain regions

Joaquín Rapela|arXiv (Cornell University)|May 3, 2017

Neural dynamics and brain function25 references3 citations

TL;DR

This study demonstrates that rhythmic production of consonant-vowel syllables (CVSs) induces precise phase synchronization of neural oscillators across speech-processing brain regions in humans, leading to the emergence of traveling waves (TWs) in both voltage and high-gamma amplitude. Using intracranial electrocorticography (ECoG), the authors identify two counter-propagating TWs—one in low-frequency voltage oscillations and another in high-gamma amplitude—synchronized to CVS production, revealing a neural mechanism for sensorimotor integration in speech.

ABSTRACT

Nature is abundant in oscillatory activity, with oscillators that have the remarkable ability of synchronizing to external events. Using electrocorticographic (ECoG) recordings from a subject rhythmically producing consonant-vowel syllables (CVSs) we show that neural oscillators recorded at individual ECoG electrodes become precisely synchronized to initiations of the production of CVSs (i.e., that these initiations occur at precise phases of bandpassed-filtered voltages recorded at most ECoG electrodes). This synchronization is not a trivial consequence of the rhythmic production of CVSs, since it takes several minutes to be fully established and is observed at the frequency of CVS production and at its second harmonic. The phase of filtered voltages at which CVSs are produced varies systematically across the grid of electrodes, consistently with the propagation of traveling waves (TWs). Using these synchronized phases we isolate a first TW in voltages (filtered at the median CVS-production frequency) moving from primary auditory to premotor cortex, and a second TW in high-gamma amplitude (coupled to phase at the CVS-production frequency) moving along the same path but in opposite direction. To our knowledge, this is the first report of rhythmic motor acts synchronizing spatio-temporally organized cortical activity in the human brain.

Motivation & Objective

• To investigate whether rhythmic motor acts, such as speech production, can synchronize neural oscillators in the human brain.
• To determine if such synchronization leads to the emergence of spatio-temporally organized traveling waves (TWs) in cortical activity.
• To examine whether the synchronization occurs at the fundamental frequency of CVS production and its second harmonic.
• To identify the direction and nature of TW propagation in relation to speech motor and auditory processing regions.
• To explore the neural mechanisms underlying the coordination between self-generated speech and cortical oscillatory dynamics.

Proposed method

• Electrocorticographic (ECoG) recordings were acquired from a human subject performing rhythmic production of consonant-vowel syllables (CVSs).
• CVS phases were calculated by measuring the time difference between syllable initiation and the nearest peak in bandpassed-filtered ECoG voltages, normalized to radians.
• Phase-locking index (PLI) was computed using circular statistics to quantify synchronization precision across electrodes, with PLI defined as the mean resultant length of phase vectors.
• Traveling wave (TW) patterns were reconstructed by analyzing the systematic spatial progression of synchronized phases across the ECoG grid.
• Two distinct TWs were isolated: one in low-frequency voltage oscillations (filtered at median CVS frequency) and another in high-gamma amplitude phase-locked to the CVS frequency.
• Directionality of TWs was determined by fitting phase gradients across electrodes, revealing counter-propagating waves from premotor to primary auditory cortex and vice versa.

Experimental results

Research questions

• RQ1 Can rhythmic motor acts like speech production synchronize neural oscillators in human cortex?
• RQ2 Does this synchronization manifest as spatio-temporally organized traveling waves (TWs) in speech-related brain regions?
• RQ3 Is the synchronization observed at both the fundamental frequency of CVS production and its second harmonic?
• RQ4 What is the direction and propagation pattern of the induced traveling waves in relation to speech motor and auditory processing areas?
• RQ5 How do the phase and amplitude dynamics of neural oscillations interact to support sensorimotor integration during speech?

Key findings

• Neural oscillators across the ECoG grid became precisely phase-locked to the initiation of consonant-vowel syllables (CVSs), with synchronization developing over ~4 minutes.
• Synchronization was observed not only at the fundamental CVS production frequency but also at its second harmonic, indicating multi-timescale entrainment.
• Systematic variation in CVS phase across electrodes revealed a consistent spatial progression, consistent with traveling wave (TW) propagation.
• A first traveling wave was identified in voltage oscillations filtered at the median CVS-production frequency, propagating from premotor to primary auditory cortex.
• A second traveling wave was found in high-gamma amplitude, phase-locked to the CVS frequency, propagating in the opposite direction—from auditory to premotor cortex.
• The two TWs were spatially and temporally coordinated, suggesting a dual mechanism for integrating motor output with sensory feedback during speech.