Theta-gamma phase-amplitude coupling in auditory cortex is modulated by language proficiency

Abstract

The coordination between the theta phase (3-7 Hz) and gamma power (25-35 Hz) oscillations (namely theta-gamma phase-amplitude coupling, PAC) in the auditory cortex has been proposed as an essential neural mechanism involved in speech processing. However, it has not been established how this mechanism is related to the efficiency with which a listener processes speech. Speech processing in a non-native language offers a useful opportunity to evaluate if theta-gamma PAC is modulated by the challenges imposed by the reception of speech input in a non-native language. The present study investigates how auditory theta-gamma PAC (recorded with magnetoencephalography) is modulated in both native and non-native speech reception. Participants were Spanish native (L1) speakers studying Basque (L2) at three different levels: beginner (Grade 1), intermediate (Grade 2), and advanced (Grade 3). We found that during L2 speech processing (i) theta-gamma PAC was more highly coordinated for intelligible compared to unintelligible speech; (ii) this coupling was modulated by proficiency in Basque being lower for beginners, higher for intermediate, and highest for advanced speakers (no difference observed in Spanish); (iii) gamma power did not differ between languages and groups. These findings highlight how the coordinated theta-gamma oscillatory activity is tightly related to speech comprehension: the stronger this coordination is, the more the comprehension system will proficiently parse the incoming speech input.

Keywords: brain oscillations; cross-frequency coupling; foreign language learning; magnetoencephalography; top-down modulations.

FIGURE 1

Stimuli and procedure. (a) Speech envelopes for the L1 conditions. An example of the speech envelope for a L1 sentence in the natural (dark blue) and its spectrally rotated (light blue) condition. (b) Time course of an individual trial. The structure for the L1 and L2 trials were identical.

FIGURE 2

Language dominance. Mean and standard error of the scores (transformed into percentages) for L1 (Spanish) and L2 (Basque) measures across participants. (a) Picture‐naming: The test consisted of 65 pictures corresponding to non‐cognate words that had to be named in each language. (b) Interview: A personal interview with the participants to estimate their general language skill from 1 (lowest) to 5 (highest). (c) Daily use: approximate percentage of daily use of each language as reported by participants. (d) Daily listening: approximate percentage of daily listening in each language as reported by participants.

FIGURE 3

Coupling between low‐ and high‐frequency oscillations in the auditory cortex. We used mutual information to evaluate the phase‐amplitude coupling (PAC) between low‐frequency (0–10 Hz) and high‐frequency (10–50 Hz) oscillations in the auditory cortex. (a, b) Spectral distribution of the speech‐specific PAC (ssPAC) (speech—spectrally rotated speech) for each language (L1, native language; L2, second language) and auditory cortex (left and right) across all grades. Black contours highlighted significant clusters after corrected for multiple comparisons (p < .05, two‐tailed permutation test, cluster corrected). We also included the box plot display of the first quartile, median, mean (filled big dot) and third quartile of the theta to gamma values obtained for the (c) L1 and the (d) L2 for each language, auditory cortex and Grade (Grade 1, 2 and 3). Small filled dots represent single subject values. The extreme line represented the highest and lowest value excluding outliers. The outliers (unfilled big circles) were the points that fell more than 1.5 times the interquartile range above the third quartile or below the first quartile. Extreme lines represent the highest and lowest value (excluding outliers).

FIGURE 4

Relevance of theta to gamma coupling for L2 proficiency. Circles represent the values obtained for each participant. The black trace is the fit of the linear regression model.

FIGURE 5

Gamma power during speech processing in the auditory cortex. Box plot display of the first quartile, median, mean (filled big dot) and third quartile of the gamma speech‐specific power (ssPow) values obtained for the (a) L1 and the (b) L2 for each language, auditory cortex and Grade (Grade 1, 2, and 3). Small filled dots represent single subject values. The extreme line represented the highest and lowest value excluding outliers. The outliers (unfilled big circles) were the points that fell more than 1.5 times the interquartile range above the third quartile or below the first quartile. Extreme lines represent the highest and lowest value (excluding outliers).