Human brain activation during phonation and exhalation: Common volitional control for two upper airway functions

Abstract

Phonation is defined as a laryngeal motor behavior used for speech production, which involves a highly specialized coordination of laryngeal and respiratory neuromuscular control. During speech, brief periods of vocal fold vibration for vowels are interspersed by voiced and unvoiced consonants, glottal stops and glottal fricatives (/h/). It remains unknown whether laryngeal/respiratory coordination of phonation for speech relies on separate neural systems from respiratory control or whether a common system controls both behaviors. To identify the central control system for human phonation, we used event-related fMRI to contrast brain activity during phonation with activity during prolonged exhalation in healthy adults. Both whole-brain analyses and region of interest comparisons were conducted. Production of syllables containing glottal stops and vowels was accompanied by activity in left sensorimotor, bilateral temporoparietal and medial motor areas. Prolonged exhalation similarly involved activity in left sensorimotor and temporoparietal areas but not medial motor areas. Significant differences between phonation and exhalation were found primarily in the bilateral auditory cortices with whole brain analysis. The ROI analysis similarly indicated task differences in the auditory cortex with differences also detected in the inferolateral motor cortex and dentate nucleus of the cerebellum. A second experiment confirmed that activity in the auditory cortex only occurred during phonation for speech and did not depend upon sound production. Overall, a similar central neural system was identified for both speech phonation and voluntary exhalation that primarily differed in auditory monitoring. Keywords phonation; exhalation; speech; fMRI Phonation for human speech is a highly specialized manner of laryngeal sensorimotor control that extends beyond generating the sound source of speech vowels and semi-vowels (e.g. /y/ and /r/). Laryngeal gestures for voice onset and offset distinguish voiced and unvoiced consonant pairs through precise timing of voice onset (Raphael et al., 2006). Brief interruptions in phonation by glottal stops (/ʔ/) mark word and syllable boundaries through hyper-adduction of the vocal folds to offset phonation. Each of these vocal fold gestures, in addition to rapid pitch changes for intonation require precisely controlled variations in intrinsic laryngeal activity (Poletto et al., 2004). To understand the neural control of phonation for speech, laryngeal control must be investigated independent of the oral articulators (lips, tongue, jaw). Several neuroimaging studies of phonation for speech included oral articulatory movements Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the producti...

Respiratory, postural and spatio-kinetic motor stabilization, internal models, top-down timed motor coordination and expanded cerebello-cerebral circuitry: a review

“…Like them, this is consistent with them being linked to the cerebello-cerebral cortex circuits (Callan et al, 2007;Callan et al, 2006;Dresel et al, 2005;Loucks et al, 2007;Murphy et al, 1997;Schulz et al, 2005;Spencer and Slocomb, 2007). Further, like dexterity and bipedality, the kinematics of speech production continues to be refined into adolescence and after (Smith and Zelaznik, 2004).…”

A probabilistic map of the human ventral sensorimotor cortex using electrical stimulation

“…18 Activations in this region associated with both phonation and exhalation have been demonstrated with fMRI. 13 Our probabilistic maps for lips, jaw, and tongue showed substantial overlap of the combined-population data, however the dorsal-ventral order of these motor and sensory groups in individuals was largely preserved. This ordered somatotopy with overlap is consistent with the findings in fMRI, ECoG, and microstimulation in primates.…”

Structural Organization of the Laryngeal Motor Cortical Network and Its Implication for Evolution of Speech Production

“…Second, in contrast to its functional homolog in nonhuman primates, the human LMC has direct connections to the nucleus ambiguus of the brainstem (Kuypers, 1958;Iwatsubo et al, 1990), allowing it to bypass the reticular formation and modulate laryngeal motoneurons directly (Simonyan and Jürgens, 2003). Finally, overlap between the LMC and motor areas involved in expiration may have allowed for the convergence of expiration, phonation, and articulation, facilitating better control of complex vocalizations (Ramsay et al, 1993;Loucks et al, 2007;Brown et al, 2009). It is assumed that a combination of these factors in the course of hominid evolution might have led to a caudal "shift" of the LMC representation from the "old" motor cortex to the "new" motor cortex (Rathelot and Strick, 2009), establishing the direct access Figure 2.…”

“…Specifically, the human LMC is situated in area 4 of the primary motor cortex (Penfield and Boldrey, 1937;Rödel et al, 2004;Loucks et al, 2007;Brown et al, 2008;Bouchard et al, 2013;Simonyan, 2014), projects directly to phonatory motoneurons in the nucleus ambiguus (Kuypers, 1958;Iwatsubo et al, 1990), and its electrical stimulation elicits or disrupts production of a range of vocalizations (Penfield and Roberts, 1959;Bouchard et al, 2013;Breshears et al, 2015). In contrast, the functionally isolated LMC region in nonhuman primates is positioned in area 6 of the premotor cortex (Sugar et al, 1948;Hast et al, 1974;Jürgens, 1974;Simonyan and Jürgens, 2002;Coudé et al, 2011) and has only indirect projections to the nucleus ambiguus (Jür-gens, 1976;Simonyan and Jürgens, 2003).…”