Neurophysiological origin of human brain asymmetry for speech and language

Abstract

The physiological basis of human cerebral asymmetry for language remains mysterious. We have used simultaneous physiological and anatomical measurements to investigate the issue. Concentrating on neural oscillatory activity in speech-specific frequency bands and exploring interactions between gestural (motor) and auditory-evoked activity, we find, in the absence of language-related processing, that left auditory, somatosensory, articulatory motor, and inferior parietal cortices show specific, lateralized, speech-related physiological properties. With the addition of ecologically valid audiovisual stimulation, activity in auditory cortex synchronizes with left-dominant input from the motor cortex at frequencies corresponding to syllabic, but not phonemic, speech rhythms. Our results support theories of language lateralization that posit a major role for intrinsic, hardwired perceptuomotor processing in syllabic parsing and are compatible both with the evolutionary view that speech arose from a combination of syllable-sized vocalizations and meaningful hand gestures and with developmental observations suggesting phonemic analysis is a developmentally acquired process.

Fig. 1.

Auditory and motor oscillatory profiles at rest. (A) Cytoarchitectonic and functional parcellation of (Left) auditory (axial plane) and motor cortices (sagittal plane), respectively. (B and C) Correlation coefficients between each EEG frequency band (1–72 Hz; mean ± SEM) and left (black) or right (gray) (A) auditory Te1.1 and (B) motor lip BOLD time courses. (D and E) Asymmetry indexes (mean ± SEM) for four (D) auditory and (E) motor regions. The index corresponds to left minus right difference in the correlation between BOLD and EEG fluctuations over 1–72 Hz during rest. Three frequency bands of interest are highlighted in gray: delta–theta 2–6 Hz, gamma 38–47 Hz, and gamma 56–72 Hz (*P < 0.05, **P ≤ 0.01, uncorrected).

Fig. 2.

Asymmetry indexes (mean ± SEM) during rest (colored bars) and movie (white bars) averaged over the whole spectrum (1–72 Hz) for each region of interest. Positive values correspond to left dominance and significant interactions are highlighted with brackets [*P < 0.05, **P ≤ 0.01, ***P ≤ 0.001 at the post hoc (Fisher's LSD) comparison].

Fig. 3.

Shared asymmetry profiles (A and B) at rest and (C and D) between rest and movie. (A and C) Pearson's cross-correlation (r) matrices of the normalized asymmetry indexes of 18 regions of interest computed over the whole spectrum (1–72 Hz) data points (A) during rest condition and (C) between rest (horizontal axis) and movie (vertical axis) conditions (see the schematic in the Lower Right part of D). (B and D) Representation of the significant correlations (B) during rest condition over the whole spectrum (P values corrected for multiple comparisons) and (D) driven by rest over movie conditions (uncorrected P values). Note some bidirectional influences (simple traits).

Fig. 4.

Asymmetry indexes (1–72 Hz; mean ± SEM) during movie in (A) auditory and (B) motor regions. Positive values correspond to left dominance (*P < 0.05, **P ≤ 0.01, uncorrected). Frequency bands of interest are highlighted in gray (Fig. 1).