Rebecca Z. German

New Directions for Understanding Neural Control in Swallowing: The Potential and Promise of Motor Learning

Oropharyngeal swallowing is a complex sensorimotor phenomenon that has had decades of research dedicated to understanding it more thoroughly. However, the underlying neural mechanisms responsible for normal and disordered swallowing remain very vague. We consider this gap in knowledge the result of swallowing research that has been broad (identifying phenomena) but not deep (identifying what controls the phenomena). The goals of this review are to address the complexity of motor control of oropharyngeal swallowing and to review the principles of motor learning based on limb movements as a model system. We compare this literature on limb motor learning to what is known about oropharyngeal function as a first step toward suggesting the use of motor learning principles in swallowing research.

Sucking and swallowing rates after palatal anesthesia: an electromyographic study in infant pigs

Infant mammalian feeding consists of rhythmic suck cycles and reflexive pharyngeal swallows. Although we know how oropharyngeal sensation influences the initiation and frequency of suck and swallow cycles, the role of palatal sensation is unknown. We implanted EMG electrodes into the mylohyoid muscle, a muscle active during suckling, and the thyrohyoid muscle, a muscle active during swallowing, in eight infant pigs. Pigs were then bottle-fed while lateral videofluoroscopy was simultaneously recorded from the electrodes. Two treatments were administered prior to feeding and compared with control feedings: 1) palatal anesthesia (0.5% bupivacaine hydrochloride), and 2) palatal saline. Using the timing of mylohyoid muscle and thyrohyoid muscle activity, we tested for differences between treatment and control feedings for swallowing frequency and suck cycle duration. Following palatal anesthesia, four pigs could not suck and exhibited excessive jaw movement. We categorized the four pigs that could suck after palatal anesthesia as group A, and those who could not as group B. Group A had no significant change in suck cycle duration and a higher swallowing frequency after palatal saline (P = 0.021). Group B had significantly longer suck cycles after palatal anesthesia (P < 0.001) and a slower swallowing frequency (P < 0.001). Swallowing frequency may be a way to predict group membership, since it was different in control feedings between groups (P < 0.001). The qualitative and bimodal group response to palatal anesthesia may reflect a developmental difference. This study demonstrates that palatal sensation is involved in the initiation and frequency of suck and swallow cycles in infant feeding.

Unilateral Superior Laryngeal Nerve Lesion in an Animal Model of Dysphagia and Its Effect on Sucking and Swallowing

We tested two hypotheses relating to the sensory deficit that follows a unilateral superior laryngeal nerve (SLN) lesion in an infant animal model. We hypothesized that it would result in (1) a higher incidence of aspiration and (2) temporal changes in sucking and swallowing. We ligated the right-side SLN in six 2–3-week-old female pigs. Using videofluoroscopy, we recorded swallows in the same pre- and post-lesion infant pigs. We analyzed the incidence of aspiration and the duration and latency of suck and swallow cycles. After unilateral SLN lesioning, the incidence of silent aspiration during swallowing increased from 0.7 to 41.5xa0%. The durations of the suck containing the swallow, the suck immediately following the swallow, and the swallow itself were significantly longer in the post-lesion swallows, although the suck prior to the swallow was not different. The interval between the start of the suck containing a swallow and the subsequent epiglottal movement was longer in the post-lesion swallows. The number of sucks between swallows was significantly greater in post-lesion swallows compared to pre-lesion swallows. Unilateral SLN lesion increased the incidence of aspiration and changed the temporal relationships between sucking and swallowing. The longer transit time and the temporal coordinative dysfunction between suck and swallow cycles may contribute to aspiration. These results suggest that swallow dysfunction and silent aspiration are common and potentially overlooked sequelae of unilateral SLN injury. This validated animal model of aspiration has the potential for further dysphagia studies.

Swallowing kinematics and airway protection after palatal local anesthesia in infant pigs.

Abnormal kinematics during swallowing can result in aspiration, which may become life threatening. We tested the role of palatal sensation in the motor control of pharyngeal swallow in infants.

Development, Reliability, and Validation of an Infant Mammalian Penetration–Aspiration Scale

A penetration–aspiration scale exists for assessing airway protection in adult videofluoroscopy and fiberoptic endoscopic swallowing studies; however, no such scale exists for animal models. The aim of this study was threefold: (1) develop a penetration–aspiration scale (PAS) for infant mammals, (2) test the scale’s intra- and interrater reliabilities, and (3) validate the use of the scale for distinguishing between abnormal and normal animals. After discussion and reviewing many videos, the result was a 7-point infant mammal PAS. Reliability was tested by having five judges score 90 swallows recorded with videofluoroscopy across two time points. In these videos, the frame rate was either 30 or 60xa0framesxa0perxa0second and the animals were either normal, had a unilateral superior laryngeal nerve (SLN) lesion, or had hard palate local anesthesia. The scale was validated by having one judge score videos of both normal and SLN lesioned pigs and testing the difference using a t test. Raters had a high intrarater reliability [average κxa0=xa00.82, intraclass correlation coefficient (ICC)xa0=xa00.92] and high interrater reliability (average κxa0=xa00.68, ICCxa0=xa00.66). There was a significant difference in reliability for videos captured at 30 and 60 frames per second for scores of 3 and 7 (Pxa0<xa00.001). The scale was also validated for distinguishing between normal and abnormal pigs (Pxa0<xa00.001). Given the increasing number of animal studies using videofluoroscopy to study dysphagia, this scale provides a valid and reliable measure of airway protection during swallowing in infant pigs that will give these animal models increased translational significance.

The effect of unilateral superior laryngeal nerve lesion on swallowing threshold volume

The superior laryngeal nerve (SLN) is the major sensory nerve for the upper larynx. Damage to this nerve impacts successful swallowing. The first aim of the study was to assess the effect of unilateral SLN lesion on the threshold volume sufficient to elicit swallowing in an intact pig model; this volume was defined radiographically as the maximum bolus area visible in lateral view. The second aim was to determine if a difference existed between ipsilateral and contralateral function as a result of unilateral sensory loss, measured as the radiologic density of fluid seen in the valleculae. Finally, we determined whether there was a relationship between the threshold volume and the occurrence of aspiration after a unilateral SLN lesion.

The Effect of Bilateral Superior Laryngeal Nerve Lesion on Swallowing: A Novel Method to Quantitate Aspirated Volume and Pharyngeal Threshold in Videofluoroscopy

The purpose was to determine the effect of bilateral superior laryngeal nerve (SLN) lesion on swallowing threshold volume and the occurrence of aspiration, using a novel measurement technique for videofluoroscopic swallowing studies (VFSS) in infant pigs. We used a novel radiographic phantom to assess volume of the milk containing barium from fluoroscopy. The custom made phantom was firstly calibrated by comparing image intensity of the phantom with known cylinder depths. Secondly, known volume pouches of milk in a pig cadaver were compared to volumes calculated with the phantom. Using these standards, we calculated the volume of milk in the valleculae, esophagus and larynx, for 205 feeding sequences from four infant pigs feeding before and after had bilateral SLN lesions. Swallow safety was assessed using the tested and validated IMPAS (Dysphagia 28(2):178–187, 2013). The log-linear correlation between image intensity values from the phantom filled with barium milk and the known phantom cylinder depths was strong (R2xa0>xa00.95), as was the calculated volumes of the barium milk pouches. The threshold volume of bolus in the valleculae during feeding was significantly larger after bilateral SLN lesion than in control swallows (pxa0<xa00.001). The IMPAS score increased in the lesioned swallows relative to the controls, indicating substantially impaired swallowing (pxa0<xa00.001). Bilateral SLN lesion dramatically increased the aspiration incidence and the threshold volume of bolus in valleculae. The use of this phantom permits quantification of the aspirated volume of fluid, allowing for more accurate 3D volume estimation from 2D X-ray in VFSS.

Regional Variation in Geniohyoid Muscle Strain During Suckling in the Infant Pig

The geniohyoid muscle (GH) is a critical suprahyoid muscle in most mammalian oropharyngeal motor activities. We used sonomicrometry to evaluate regional strain (i.e., changes in length) in the muscle origin, belly, and insertion during suckling in infant pigs, and compared the results to existing information on strain heterogeneity in the hyoid musculature. We tested the hypothesis that during rhythmic activity, the GH shows regional variation in muscle strain. We used sonomicrometry transducer pairs to divide the muscle into three regions from anterior to posterior. The results showed differences in strain among the regions within a feeding cycle; however, no region consistently shortened or lengthened over the course of a cycle. Moreover, regional strain patterns were not correlated with timing of the suck cycles, neither (1) relative to a swallow cycle (before or after) nor (2) to the time in feeding sequence (early or late). We also found a tight relationship between muscle activity and muscle strain, however, the relative timing of muscle activity and muscle strain was different in some muscle regions and between individuals. A dissection of the C1 innervations of the geniohyoid showed that there are between one and three branches entering the muscle, possibly explaining the variation seen in regional activity and strain. In combination, our findings suggest that regional heterogeneity in muscle strain during patterned suckling behavior functions to stabilize the hyoid bone, whereas the predictable regional strain differences in reflexive behaviors may be necessary for faster and higher amplitude movements of the hyoid bone.

Anatomical anomalies of the laryngeal branches of the vagus nerve in pigs (Sus scrofa).

To delineate the anomaly and frequency of their occurrence in a pig model, we reported the topography of the vagus laryngeal branches and compared the differences with humans. Thirty sides of cervical vagus nerve in 15 fresh cadavers (Sus scrofa) were microdissected. We measured the branch diameters and lengths of the laryngeal branches using a Vernier caliper with a resolution of 0.01 mm. Two patterns of the vagus laryngeal branches were shown: 56.7% with the cranial laryngeal nerve (CLN) and 43.3% without the CLN. The diameters and the length of the CLN were not affected by the side of the neck (P > 0.05), but the diameters of the recurrent laryngeal nerve (RLN) and the nodose ganglion were significantly different between left and right sides (P < 0.05). The left RLN was thinner than the right side in diameter (P < 0.05). Four of the 30 sides had anastomoses between the vagus and the cervical sympathetic chain. There were some differences between the pig anatomy and human anatomy, but the patterns were largely similar. The similarities support the utility of this model, which is closer in size to humans than the standard rodent models.

Variation in the Timing and Frequency of Sucking and Swallowing over an Entire Feeding Session in the Infant Pig Sus scrofa

Feeding is a rhythmic behavior that consists of several component cycle types. How the timing of these cycles changes over a complete feeding sequence is not well known. To test the hypothesis that cycle frequency/duration changes as a function of time spent feeding, we examined complete feeding sequences in six infant pigs, using EMG of mylohyoid and thyrohyoid as cycle markers. We measured the instantaneous frequency of sucking and of swallowing cycles in 19 sequences. Each sequence contained three qualitatively distinctive phases of sucking frequency. Phase 1 started with cycles at a very high frequency and quickly dropped to a more constant level with low variation, which characterized phase 2. Phase 3 had a steady level of frequency but was interspersed with a number of high- or low-frequency cycles. Each phase differed from the others in patterns of within-phase variation and among-phase variation. Phase 2 had the least variation, and phase 3 had the largest range of frequencies. The number of sucks per swallow also differed among phases. These patterns, which characterize normative feeding, could indicate a physiologic basis in satiation. In human infant clinical studies, where data collection is often limited, these results indicated the utility of collecting data in different phases. Finally, these results can be used as a template or pattern with which to assess clinically compromised infants.