Abstract
Speaking involves coordination of multiple neuromotor systems, including respiration, phonation and articulation. Developing non-invasive imaging methods to study how the brain controls these systems is critical for understanding the neurobiology of speech production. Recent models and animal research suggest that regions beyond the primary motor cortex (M1) help orchestrate the neuromotor control needed for speaking, including cortical and sub-cortical regions. Using contrasts between speech conditions with controlled respiratory behavior, this fMRI study investigates articulatory gestures involving the tongue, lips and velum (i.e., alveolars versus bilabials, and nasals versus orals), and phonatory gestures (i.e., voiced versus whispered speech). Multivariate pattern analysis (MVPA) was used to decode articulatory gestures in M1, cerebellum and basal ganglia. Furthermore, apart from confirming the role of a mid-M1 region for phonation, we found that a dorsal M1 region, linked to respiratory control, showed significant differences for voiced compared to whispered speech despite matched lung volume observations. This region was also functionally connected to tongue and lip M1 seed regions, underlying its importance in the coordination of speech. Our study confirms and extends current knowledge regarding the neural mechanisms underlying neuromotor speech control, which hold promise to study neural dysfunctions involved in motor-speech disorders non-invasively.
Highlights
Speaking involves coordination of multiple neuromotor systems, including respiration, phonation and articulation
Speech was successfully synchronized in all participants with our functional magnetic resonance imaging (fMRI) protocol, i.e., speech was produced within the desired silent periods (900 ms) between consecutive TRs
The three production events composing a single trial were consistent in loudness, variation was small across voiced events (3-way anova, p = 0.99, Fig. 2A lower panel) and the whispered task (p = 0.97)
Summary
Speaking involves coordination of multiple neuromotor systems, including respiration, phonation and articulation. At least three research strategies have been adopted in the past in fMRI: (a) contrasting overt (voiced) and covert (imagery) speech[7,11,13]; (b) production of glottal stops[12]; and (c) contrasting www.nature.com/scientificreports voiced and whispered-like (i.e., exhalation) speech[14] The latter potentially isolates phonation while preserving key naturalistic features of speech, including the sustained and partial adduction of the glottis, the synchronization of phonation, respiration and articulation, and the generation of an acoustic output. We take advantage of several methodological strategies to avoid both head motion and breathing confounds by employing sparse-sampling fMRI18 and experimental conditions with well-matched respiratory demands that are measured, respectively Using these methods, in this study we investigated fMRI representations of speech production, including articulatory and phonatory gestures across the human cortex and subcortex by employing multivariate decoding methods successfully used in fMRI studies of speech perception[22,23,24]. Twenty fluent adults read a list of bi-syllabic non-words, balanced for bilabial and alveolar places of articulation, oral and nasal manners of articulation, and the non-articulated vowel ‘schwa’, using both voiced and whispered speech
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