Regional Variation in Contractile Patterns and Muscle Activity in Infant Pig Feeding

Abstract

At the level of the whole muscle, contractile patterns during activity are a critical and necessary source of variation in function. Understanding if a muscle is actively lengthening, shorting, or remaining isometric has implications for how it is working to power a given behavior. When feeding, the muscles associated with the tongue, jaws, pharynx, and hyoid act together to transport food through the oral cavity and into the esophagus. These muscles have highly coordinated firing patterns, yet also exhibit high levels of regional heterogeneity in both their timing of activity and their contractile characteristics when active. These high levels of variation make investigations into function challenging, especially in systems where muscles power multiple behaviors. We used infant pigs as a model system to systematically evaluate variation in muscle firing patterns in two muscles (mylohyoid and genioglossus) during two activities (sucking and swallowing). We also evaluated the contractile characteristics of mylohyoid during activity in the anterior and posterior regions of the muscle. We found that the posterior regions of both muscles had different patterns of activity during sucking versus swallowing, whereas the anterior regions of the muscles did not. Furthermore, the anterior portion of mylohyoid exhibited concentric contractions when active during sucking, whereas the posterior portion was isometric during sucking and swallowing. This difference suggests that the anterior portion of mylohyoid in infant pigs is functioning in concert with the tongue and jaws to generate suction, whereas the posterior portion is likely acting as a hyoid stabilizer during sucking and swallowing. Our results demonstrate the need to evaluate both the contractile characteristics and activity patterns of a muscle in order to understand its function, especially in cases where there is potential for variation in either factor within a single muscle.

Fig. 1

Contrast-enhanced CT scan with an anteroposterior slice (a, left is anterior), dorsoventral slice (b, bottom is ventral), and lateral (c, left is anterior) and ventral (d) three dimensional renders of anterior mylohyoid (blue), posterior mylohyoid (Yellow) and genioglossus (pink). The symbol * in D represents locations of bead placement for fluoromicrometry; + and ^ in D represent placement of electrodes for EMG in mylohyoid and genioglossus respectively. Labels in (a) and (b) are provided for reference.

Fig. 2

EMG duration of genioglossus (a) and mylohyoid (b) between sucking and swallowing bursts does not differ in the anterior portion of the muscle (blue) but is longer in the posterior belly during a swallow (yellow). During sucks, the posterior part of the muscle was active shorter than the anterior part for both muscles. Lines connecting plots indicate statistical significance as identified by planned contrast analyses.

Fig. 3

The time of muscle onset and offset relative to the beginning of the suck for genioglossus (a, b) and mylohyoid (c, d) for sucks and sucks involving a swallow in anterior (blue) and posterior (yellow) portions of the muscle. Lines indicate statistically significant differences with large effects sizes. No differences were observed in genioglossus, whereas onset timing followed an anteroposterior wave in mylohyoid (c), and offset was later in posterior electrodes during a swallow than during a suck (d).

Fig. 4

Mean length changes (solid line) ± one standard error (shaded region) in the anterior (a) and posterior (b) bellies of mylohyoid during sucking. Each line represents one individual; green: muscle is on; gray: muscle is off; IMD: Intermarker distance, standardized to be 0 at the time of muscle onset during a behavior. Note that the excursion of movement illustrated here is less than the typical excursion due to variation in when the minimum and maximum distances occurred across cycles within an individual.

Fig. 5

Example raw (unstandardized by onset timing) data from one pig for anterior mylohyoid EMG and IMD data (a), posterior mylohyoid EMG and IMD data (b), and thyrohyoid EMG data (c) for 1 s. Black lines indicate the beginning of a suck cycle, gray bars indicate the duration of a swallow, highlighted by thyrohyoid firing (gray) to demonstrate changes in EMG activity during posterior mylohyoid. Anterior mylohyoid does not change EMG activity during swallowing, and is primarily concentric during sucking (a), whereas posterior mylohyoid has changes in EMG activity during swallowing, but remains isometric during all activity (b). IMD; intermarker distance.