Muscle activity and kinematics show different responses to recurrent laryngeal nerve lesion in mammal swallowing

Abstract

Understanding the interactions between neural and musculoskeletal systems is key to identifying mechanisms of functional failure. Mammalian swallowing is a complex, poorly understood motor process. Lesion of the recurrent laryngeal nerve, a sensory and motor nerve of the upper airway, results in airway protection failure (liquid entry into the airway) during swallowing through an unknown mechanism. We examined how muscle and kinematic changes after recurrent laryngeal nerve lesion relate to airway protection in eight infant pigs. We tested two hypotheses: 1) Kinematics and muscle function will both change in response to lesion in swallows with and without airway protection failure 2) Differences in both kinematics and muscle function will predict whether airway protection failure occurs in lesion and intact pigs. We recorded swallowing with high speed videofluoroscopy and simultaneous electromyography of oropharyngeal muscles pre- and post-recurrent laryngeal nerve lesion. Lesion changed the relationship between airway protection and timing of tongue and hyoid movements. Changes in onset and duration of hyolaryngeal muscles post-lesion were less associated with airway protection outcomes. The tongue and hyoid kinematics all predicted airway protection outcomes differently pre and post-lesion. Onset and duration of activity of activity in only one infrahyoid and one suprahyoid muscle showed a change in predictive relationship pre- and post-lesion. Kinematics of the tongue and hyoid more directly reflect changes in airway protection s pre and post lesion than muscle activation patterns. Identifying mechanisms of airway protection failure requires specific functional hypotheses that link neural motor outputs to muscle activation to specific movements.

Advances in Swallowing Neurophysiology Across Pediatric Development: Current Evidence and Insights

“…Although both types of injuries may temporarily compromise airway safety in term infant pigs, the underlying physiological mechanisms of this compromise differ [45]. More specifically, RLN lesions have been shown to affect hyoid and tongue kinematics [46], volume consumed [47], the neuromuscular control of swallowing [46], and airway safety in infant pigs, and some of these changes can be pervasive. SLN lesions have been associated with higher rates of reduced airway safety as well [48]; however, these changes are mostly explained by temporal dysfunctions in the coordination between suck and swallow cycles [48] or in epiglottic inversion timing [45].…”

Nipple properties affect sensorimotor integration during bottle feeding in an infant pig model

“…Disruptions to normal sucking behavior in infants can result in aspiration, malnourishment, and delayed development (Dodrill, 2011; Hadders‐Algra, 2018; Satter, 1990). One mechanism that shows promise for improving feeding outcomes is varying sensory stimulation to modulate motor output during feeding (DeLozier et al, 2018; Ding et al, 2013; Gould et al, 2020; Mayerl et al, 2020; Tsuji et al, 2015). Oral stimulation via tactile stimulus and nonnutritive sucking (NNS) has been shown to improve feeding outcomes (Aguilar‐Rodríguez et al, 2020; Barlow et al, 2014; Fucile et al, 2011; Song et al, 2019).…”

The effect of stiffness and hole size on nipple compression in infant suckling

“…Infant mammals have highly developed oral sensory abilities at birth, which provides specific input to the central nervous system for efficient and effective suckling. When the sensory connections involved in infant feeding are disrupted, feeding performance is compromised and infants may suffer from illness, malnourishment, and potentially life‐long developmental issues (Adjerid et al, 2021 ; Ballester et al, 2018 ; Catchpole et al, 2020 ; DeLozier et al, 2018 ; Ding et al, 2013 ; Gould et al, 2015 , 2016 , 2017 , 2020 ; Hadders‐Algra, 2018 ; Liu et al, 2018 ; Mayerl, Catchpole, et al, 2020 ; Zimmels et al, 2021 ). Yet, sensory motor integration in human infant suckling is not fully understood, making it difficult to predict how changes to sensory input affect feeding behaviors (Gould et al, 2019 ; Jean, 2001 ; Young et al, 2015 ).…”

“…suffer from illness, malnourishment, and potentially life-long developmental issues (Adjerid et al, 2021;Ballester et al, 2018;Catchpole et al, 2020;DeLozier et al, 2018;Ding et al, 2013;Gould et al, 2015Gould et al, , 2016Gould et al, , 2017Gould et al, , 2020Hadders-Algra, 2018;Liu et al, 2018;Mayerl, Catchpole, et al, 2020;Zimmels et al, 2021). Yet, sensory motor integration in human infant suckling is not fully understood, making it difficult to predict how changes to sensory input affect feeding behaviors (Gould et al, 2019;Jean, 2001;Young et al, 2015).…”

“…We tested the differences among these nipples in individual responses using an animal model, the infant pig (German et al, 2017). This model permitted us to use highspeed videofluoroscopy to record multiple swallows per individual across multiple nipples (Gould et al, 2015(Gould et al, , 2017(Gould et al, , 2020.…”