Coordinative organization of lingual propulsion during the normal adult swallow

Abstract

Lingual propulsion during swallowing is characterized by the sequential elevation of the anterior, middle, and dorsal regions of the tongue. Although lingual discoordination underlies many swallowing disorders, the coordinative organization of lingual propulsion during the typical and disordered swallow is poorly understood. The purpose of this investigation was to quantitatively describe the coordinative organization of lingual propulsion during the normal adult swallow. Tongue movement data were obtained from the X-Ray Microbeam Database at the University of Wisconsin. Movement of four pellets placed on specific tongue regions were tracked in 36 healthy adult participants while they swallowed 10 cc of water across five discrete trials. The propulsive action of the tongue during bolus transport was quantified using a cross-correlation analysis. Lingual transit time (LTT), which was defined as the interval (lag time) between the movements of the anterior- and posterior-most tongue regions, was determined to be approximately 168 ms. The average time interval (lag) between the movements of the posterior tongue regions was significantly shorter than the intervals between more anterior tongue regions. The results also suggest that during bolus transport movement patterns of the anterior tongue regions are distinct from those of the posterior tongue regions. Future work is needed to determine if the absence of the observed coordinative organization of lingual propulsion is indicative of oral stage dysphagia.

Figure 1

(Top) Example of the tongue pellet movement trajectories during a single swallow trial plotted in a two-dimensional coordinate system. (Only vertical movement data were analyzed in this investigation.) (Bottom) Extracted vertical time histories for each pellet during a single swallow trial. The movement peak for each pellet indicates the timing at the point of maximum constriction when the tongue approximates the palate. Zero crossings in the velocity trace associated with the onset of T1 movement and offset of T4 movement are denoted as filled circles. All pellet movement data between the zero-crossings markers (shaded region) were analyzed for each swallow trial. The vertical position is referenced relative the maxillary occlusal plane as described in the Methods section.

Figure 2

Figure 2a. (Top - A) Vertical displacement trajectories for T3 and T4 pellets during a discrete swallow trial. Note the shape similarity of the movement traces and the small time interval (lag) between the peak displacement of T3 and T4. The vertical position is referenced relative the maxillary occlusal plane as described in the Methods section. (Bottom - B) The cross-correlation functions for signals T3 and T4. The peak coefficient and lag value were extracted from each cross-correlation function. The corresponding peak correlation coefficient is represented in the vertical axis. Note the high degree of movement similarity that was visually observed in panel A is represented as a coefficient value (vertical axis). The resultant lag value, represented on the horizontal axis, is also derived from the cross-correlation function. Figure 2b. (Top - A) Vertical displacement trajectories for T1 and T4 pellets during a discrete swallow trial. Note how the movement traces are relatively distinct, that is, their shape is less similar. Note also the relatively large time interval (lag) between the peak displacement of T1 and T4 in comparison to the lag of T3+T4 as displayed in Figure 2a. The vertical position is referenced relative the maxillary occlusal plane as described in the Methods section. (Bottom - B) The cross-correlation functions for signals T1 and T4. The peak coefficient and lag values were extracted from each cross-correlation. Note how the relatively low degree of spatial similarity (vertical axis) and the corresponding lag value (horizontal axis) are in contrast to the example in 2a which resulted in a much higher degree of spatial similarity and shorter lag time.

Figure 3

Lingual transit time as defined by the interval (lag) between the motions of T2 and T4. The vertical position is referenced relative the maxillary occlusal plane as described in the Methods section.

Figure 4

Average peak coefficient for all pellet pairs across all subjects. All data were transformed into Fisher’s z values and statistically analyzed. The values were then transformed using the inverse of Fisher’s z function and are reported in the figure. Standard error of the mean bars [average SD/√n] represent across-subject variation.

Figure 5

Average lag value for all pellet pairs across all subjects. Standard error of the mean bars [average SD/√n] represent across-subject variation.

Figure 6

Relative timing of the propulsive wave across tongue pellet regions. The gray lines indicate the average timing onset of movement for each pellet. It is assumed that the onset for T1 is at time zero, T2 onset = 142 ms, T3 onset = 198 ms, and T4 onset = 224 ms.

Figure 7

(Top) Example of tongue pellet positions before swallow. Note that T1 is elevated to the palate to secure the bolus in the oral cavity. (Bottom) Movement trajectories for each tongue pellet during a single swallow. Note how the displacement of T1 in the y-dimension is minimal relative to the displacement of T2, T3, and T4.