Central nervous system integration of sensorimotor signals in oral and pharyngeal structures: oropharyngeal kinematics response to recurrent laryngeal nerve lesion

Abstract

Safe, efficient liquid feeding in infant mammals requires the central coordination of oropharyngeal structures innervated by multiple cranial and spinal nerves. The importance of laryngeal sensation and central sensorimotor integration in this system is poorly understood. Recurrent laryngeal nerve lesion (RLN) results in increased aspiration, though the mechanism for this is unclear. This study aimed to determine the effect of unilateral RLN lesion on the motor coordination of infant liquid feeding. We hypothesized that 1) RLN lesion results in modified swallow kinematics, 2) postlesion oropharyngeal kinematics of unsafe swallows differ from those of safe swallows, and 3) nonswallowing phases of the feeding cycle show changed kinematics postlesion. We implanted radio opaque markers in infant pigs and filmed them pre- and postlesion with high-speed videofluoroscopy. Markers locations were digitized, and swallows were assessed for airway protection. RLN lesion resulted in modified kinematics of the tongue relative to the epiglottis in safe swallows. In lesioned animals, safe swallow kinematics differed from unsafe swallows. Unsafe swallow postlesion kinematics resembled prelesion safe swallows. The movement of the tongue was reduced in oral transport postlesion. Between different regions of the tongue, response to lesion was similar, and relative timing within the tongue was unchanged. RLN lesion has a pervasive effect on infant feeding kinematics, related to the efficiency of airway protection. The timing of tongue and hyolaryngeal kinematics in swallows is a crucial locus for swallow disruption. Laryngeal sensation is essential for the central coordination in feeding of oropharyngeal structures receiving motor inputs from different cranial nerves.

Pre-pharyngeal Swallow Effects of Recurrent Laryngeal Nerve Lesion on Bolus Shape and Airway Protection in an Infant Pig Model

“…These results are consistent with our previous work on tongue kinematics [7], and point strongly to existence of sensory motor connections between the afferent signals coming up the recurrent laryngeal nerve to the nucleus tractus solitarius, and the efferent signals emanating from the hypoglossal motor nucleus. Extensive sensory motor connections exist between the oral cavity and the swallow reflex [9,32].…”

“…Swallows were assessed for airway safety using the Infant Mammalian Penetration Aspiration Scale [16] (table 1). A random sample of pre and post lesion swallows with IMPAS scores of 1, 2, and 7 were selected for this analysis, as previous work indicates that lesion-IMPAS interactions can be expected as one outcome of these experiments [7]. Not all IMPAS scores are present in all individuals owing to natural variation in the severity of response to lesion; in particular one individual did not aspirate post lesion.…”

“…Neither these muscles, not these sensory fields, are directly involved in a safe swallow. However, recent work has indicated that airway protection deficits following RLN lesion are associated with changes in the timing and extent of tongue movements during intraoral transport and the swallow [7]. In addition, both anesthesia [8] and stimulation [9] of oral sensory pathways change swallow parameters and airway protection outcomes, highlighting the importance of sensory modulation of the swallow by structures throughout the oral, pharyngeal, and laryngeal complex.…”

“…The complex and changing shape of the tongue and soft palate, which determine much of the two dimensional bolus outline, are functionally relevant variables not easily reducible to simple linear metrics, or standard, single point tracking based kinematic approaches. Thus, although such approaches yield important insights into timing of the relative movements of the structures involved in the swallow [7], they do not tell us about the deformation of these structures, and therefore the formation of the bolus itself.…”

Recurrent laryngeal nerve transection in mice results in translational upper airway dysfunction

“…An infant pig model of RLN injury has provided novel insights concerning the role of the RLN and its neural connections in swallowing behavior. By using videofluoroscopic techniques, RLN injury has been shown to result in compromised airway protection and esophageal dysphagia (Gould et al, 2015), alterations in tongue shape (Gould, Yglesias, Ohlemacher, & German, 2017), and modified tongue and epiglottis kinematics during swallowing (Gould et al, 2016). However, these experiments were performed in neonatal and pre-weanling animals, better representing infants with immature nervous systems.…”