Beyond Broca: Neural Architecture and Evolution of a Dual Motor Speech Coordination System

Classical neural architecture models of speech production propose a single system coordinating all the vocal articulators from lips to larynx. Here we propose a dual coordination system in which laryngeal control of pitch-related aspects of prosody and song are controlled by a dorsal premotor system while supralaryngeal articulation at the phonetic/syllabic level is controlled by a ventral premotor system. The separability of these neural systems supports models of the evolution of speech and language in which song-based communication was an early foundational stage.

Singers show enhanced performance and neural representation of vocal imitation

Humans have a remarkable capacity to finely control the muscles of the larynx, via distinct patterns of cortical topography and innervation that may underpin our sophisticated vocal capabilities compared with non-human primates. Here, we investigated the behavioural and neural correlates of laryngeal control, and their relationship to vocal expertise, using an imitation task that required adjustments of larynx musculature during speech. Highly trained human singers and non-singer control participants modulated voice pitch and vocal tract length (VTL) to mimic auditory speech targets, while undergoing real-time anatomical scans of the vocal tract and functional scans of brain activity. Multivariate analyses of speech acoustics, larynx movements and brain activation data were used to quantify vocal modulation behaviour and to search for neural representations of the two modulated vocal parameters during the preparation and execution of speech. We found that singers showed more accurate task-relevant modulations of speech pitch and VTL (i.e. larynx height, as measured with vocal tract MRI) during speech imitation; this was accompanied by stronger representation of VTL within a region of the right somatosensory cortex. Our findings suggest a common neural basis for enhanced vocal control in speech and song. This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part I)’.

Singers and non-singers differ in the performance and neural representation of vocal imitation

Humans have a remarkable capacity to finely control the muscles of the larynx, via distinct patterns of cortical topography and innervation that may underpin our sophisticated vocal capabilities compared with non-human primates. Here, we investigated the behavioural and neural correlates of laryngeal control, and their relationship to vocal expertise, using an imitation task that required adjustments of larynx musculature during speech. Highly-trained human singers and non-singer control participants modulated voice pitch and vocal tract length (VTL) to mimic auditory speech targets, while undergoing real-time anatomical scans of the vocal tract and functional scans of brain activity. Multivariate analyses of speech acoustics, larynx movements and brain activation data were used to quantify vocal modulation behaviour, and to search for neural representations of the two modulated vocal parameters during the preparation and execution of speech. We found that singers showed more accurate task-relevant modulations of speech pitch and VTL (i.e. larynx height, as measured with vocal tract MRI) during speech imitation; this was accompanied by stronger representation of VTL within a region of right dorsal somatosensory cortex. Our findings suggest a common neural basis for enhanced vocal control in speech and song.

Sensory Innervation of the Larynx and the Search for Mucosal Mechanoreceptors

Purpose The larynx is a uniquely situated organ, juxtaposed between the gastrointestinal and respiratory tracts, and endures considerable immunological challenges while providing reflexogenic responses via putative mucosal mechanoreceptor afferents. Laryngeal afferents mediate precise monitoring of sensory events by relay to the internal branch of the superior laryngeal nerve (iSLN). Exposure to a variety of stimuli (e.g., mechanical, chemical, thermal) at the mucosa–airway interface has likely evolved a diverse array of specialized sensory afferents for rapid laryngeal control. Accordingly, mucosal mechanoreceptors in demarcated laryngeal territories have been hypothesized as primary sources of sensory input. The purpose of this article is to provide a tutorial on current evidence for laryngeal afferent receptors in mucosa, the role of mechano-gated ion channels within airway epithelia and mechanisms for mechanoreceptors implicated in laryngeal health and disease. Method An overview was conducted on the distribution and identity of iSLN-mediated afferent receptors in the larynx, with specific focus on mechanoreceptors and their functional roles in airway mucosa. Results/Conclusions Laryngeal somatosensation at the cell and molecular level is still largely unexplored. This tutorial consolidates various animal and human researches, with translational emphasis provided for the importance of mucosal mechanoreceptors to normal and abnormal laryngeal function. Information presented in this tutorial has relevance to both clinical and research arenas. Improved understanding of iSLN innervation and corresponding mechanotransduction events will help shed light upon a variety of pathological reflex responses, including persistent cough, dysphonia, and laryngospasm.

Inter- and Intra-Rater Reliability of Laryngeal Sensation Testing with the Touch Method During Flexible Endoscopic Evaluations of Swallowing

Objectives: Sensation is an integral component of laryngeal control for breathing, swallowing, and vocalization. Laryngeal sensation is assessed by elicitation of the laryngeal adductor reflex (LAR), a brainstem-mediated adduction of the true vocal folds. During Flexible Endoscopic Evaluations of Swallowing (FEES), the touch method can be used to elicit the LAR to judge laryngeal sensation. Despite the prevalence of this method in clinical practice and research, prior studies have yet to examine inter- and intra-rater reliability. Methods: Four speech-language pathologists rated 125 randomized video clips for the presence, absence, or inability to rate the LAR. Fifty percent of video clips were re-randomized and re-rated 1 week later. Raters then created guidelines and participated in formal consensus training sessions on a separate set of videos. Ratings were repeated post-training. Results: Overall inter-rater reliability was fair (κ = 0.22) prior to training. Pre-training intra-rater reliability ranged from fair (κ = 0.35) to almost perfect (κ = 0.89). Inter-rater reliability significantly improved after training (κ = 0.42, P < .001), though agreement did not reach prespecified acceptable levels (κ ≥ 0.80). Post-training intra-rater reliability ranged from moderate (κ = 0.49) to almost perfect (κ = 0.85). Conclusion: Adequate inter-rater reliability was not achieved when rating isolated attempts to elicit the LAR. Acceptable within-rater reliability was observed in some raters 1 week after initial ratings, suggesting that ratings may remain consistent within raters over a short period of time. Limitations and considerations for future research using the touch method are discussed.

Singing training predicts increased insula connectivity with speech and respiratory sensorimotor areas at rest

The insula contributes to the detection of salient events during goal-directed behavior and participates in the coordination of motor, multisensory, and cognitive systems. Recent task-fMRI studies with trained singers suggest that singing experience can enhance the access to these resources. However, the long-term effects of vocal training on insula based networks are still unknown. In this study, we employed resting-state fMRI to assess experience-dependent differences in insula co-activation patterns between conservatory-trained singers and non-singers. Results indicate enhanced bilateral insula connectivity in singers relative to non-singers with constituents of the speech sensorimotor network in both hemispheres. Specifically, with the cerebellum (lobule VI, crus 2), primary somatosensory cortex, the parietal lobes, and the thalamus. Furthermore, singing training predicted enhanced bilateral co-activation of primary sensorimotor areas representing the larynx (with left dorsal anterior insula, dAI) and the diaphragm (with bilateral dAI)—crucial regions for cortico-motor control of complex vocalizations, as well as the thalamus (with bilateral posterior insula/left dAI) and the left putamen (with left dAI). Together, these data support a crucial role of the insula in respiratory and laryngeal control and suggest that singing experience enhances the integration of somatosensory information within the speech motor system, perhaps by strengthening salient associations of bodily signals associated with conscious and non-conscious aspects of expressive language production within a musical framework.

Modulation of articulation muscles during listening and reading: a matter of intention to speak out loud

The articulation of speech sounds is often contingent on the intention to subsequently produce other sounds (co-articulation). Thus, intended acts affect the way current acts are executed. We show that the intention to subsequently repeat a short sentence, overtly or covertly, significantly modulated articulatory muscle activity already during speech perception or reading (input interval) and when delaying response (i.e., prior to production). Young adults were instructed to read (whole sentences or word-by-word) or listen to recordings of sentences to be repeated afterwards, either covertly or overtly. Surface electromyography (sEMG) recordings showed different patterns of articulatory muscle modulation in the two articulatory muscles measured – orbicularis oris inferior (OOI) and sternohyoid (STH). In the OOI, activity increased relative to baseline during speech perception or reading in both intended output conditions (overt and covert); in the STH, articulatory muscle activity decreased, during the input intervals, in both intended output conditions. However, the modulations in EMG activity were contingent on the intention to subsequently repeat the input overtly or covertly, so that activation in the OOI, and inhibition in the STH, were significantly more pronounced when overt responses were intended. Input modality was also a factor; immediately before overt responses, activity in the OOI muscle increased for listening and word-by-word reading, but not in reading whole sentences. The current results suggest that speech perception and articulation interact already during the input phase, listening or reading, reflecting the intended responses. However, this interaction may differentially affect facial-articulatory and laryngeal control mechanisms of speech production.

Behavioral Management of Paradoxical Vocal Fold Motion

Paradoxical vocal fold motion (PVFM), or vocal cord dysfunction (VCD), is a non-organic, behavioral, upper airway disorder primarily characterized by adduction of the true vocal folds during respiration. Recognition of this condition is becoming more prevalent amongst physicians, resulting in an increased number of referrals to speech-language pathologists (SLPs) for assessment and treatment. Diagnosis of PVFM requires a multidisciplinary approach. Treatment for PVFM is also multi-factorial, but is primarily designed to train abduction of the vocal folds during the breathing cycle, allowing easy movement of breath to and from the lungs without laryngeal constriction. Behavioral management is the preferred and most common approach to treatment and may include relaxed throat breathing and laryngeal control exercises during trigger-specific training.