Kinematic strategies for hyoid movement in rapid sequential swallowing

Kinematic strategies for hyoid movement in rapid sequential swallowing

Chi-Fishman, Gloria

Past studies revealed that rapid sequential swallows differed significantly from commanded discrete swallows in tongue-palate contact pattern, submental muscle response characteristics, and duration of videofluoroscopic deglutitive events in healthy individuals (Chi-Fishman & Sonies, 2000; Chi-Fishman, Stone, & McCall, 1998). Specifically, rapid sequential swallows were characterized by (a) temporal-spatial overlaps of linguopalatal contact stages, (b) a repetitive “activation and partial deactivation” pattern in surface EMG waveform, and (c) significantly shortened oral transit, pharyngeal response, upper esophageal sphincter opening, and total swallow durations. However, the control strategies that underlie these characteristics have not been elucidated.

In studying movement attributes and motor control strategies, one cannot examine only the variable of duration and infer that lengthened durations exclusively indicate slower movement (cf. Rademaker, Pauloski, Colangelo, & Logemann, 1998; Robbins, Hamilton, Lof, & Kempster, 1992; Sonies, Parent, Morrish, & Baum, 1988). Other kinematic elements– amplitude and velocity-are equally important, and the accomplishment of movement targets characteristically requires changes in the interrelations among the kinematic parameters. Variations in the interplay of these parameters can produce different kinematic outcomes. For example, if duration is held constant, an increase in peak velocity will lead to an increase in movement amplitude; if velocity remains unchanged, a decrease in amplitude will cause the movement to be completed in less time (Milner, 1986). By studying these kinematic variations, one gains insights into how movement variables are adjusted or scaled according to task requirements and whether the underlying strategies of the motor control mechanism change or remain invariant across tasks.

It has been shown that in rapid movements (e.g., typing on a keyboard, reduplicating selected consonant sounds), the amount of force used for the task is directly related to peak velocity and that the latter is strongly coupled with movement amplitude (see Cooke, 1980 and Milner, 1986 for reviews). Examining the relations among position, velocity, and torque during simple alternate arm movements, Cooke (1982) found that at a fixed amplitude, but changing velocities, the faster the movement the greater the stiffness of the musculature. In their study of simple lingual and laryngeal kinematics during speech, Munhall, Ostry, and Parush (1985) computed the ratio of maximal velocity to movement amplitude as a derived measure of mass-normalized stiffness and found this ratio to increase systematically with decreases in movement duration.

The relationships between force and muscle stiffness are understandably complex. Simple equations that accurately detect linearity in kinematic relations for selected types of motor acts (e.g., isometric tasks) may not be adequate for other movement types (e.g., dynamic tasks). Swallowing is a complex, dynamic motor behavior with both voluntary and involuntary components. Whether the same kinematic relations and variations observed in voluntary limb and speech movements would apply to movements of structures involved in pharyngeal swallowing had not been determined. Any movement, simple or complex, voluntary or reflexive, that results in a change of position of a given structure is the product of anisometric contraction of muscles and has distinct kinematic properties.

Structural and physiological competency of the hyolaryngeal motor complex is crucial to safe swallowing. This region, consisting of the hyoid bone, suprahyoid and infrahyoid musculature, and anatomical elements of the larynx, is the principal sensorimotor agent for airway protection and upper esophageal sphincter opening during deglutition (Cook et al., 1989; Jacob, Kahrilas, Logemann, Shah, & Ha, 1989). Current gold standards for videofluoroscopic study of swallowing use the onset of hyolaryngeal movement as an index for the start of pharyngeal swallow (Dodds, Stewart, & Logemann, 1990; Logemann, 1993; Robbins et al., 1992). As the point of attachment for muscular and nonmuscular tissue of the floor of the mouth, tongue, and larynx, the hyoid bone is highly mobile (Hiatt & Gartner, 1987; Zemlin, 1998), and its movement characteristics and temporal coordination with other events during swallowing provide important information in the understanding of deglutitive physiology and in clinical diagnostics (Logemann, 1998; Perlman, Vandaele, & Otterbacher, 1995; Wintzen, Badrising, Roos, Vielvoye, & Liauw, 1994).

The present study was designed to examine the interrelations among the kinematic variables (i.e., duration, amplitude, and velocity) for hyoid motion and to determine the strategies used for accomplishing discrete liquid swallows versus sequential swallows as a part of rapid continuous drinking. The main hypothesis tested was that increased hyoid movement velocity was a major characteristic of rapid sequential swallowing.

Method

Subjects

Thirty healthy men (15) and women (15) were studied in three stratified age groups: young (Range = 20– 39, M = 27.92, SD = 4.55 years; n = 12, 6 males and 6 females), mid-aged (Range = 40-59, M = 50.78, SD = 5.60 years; n = 11, 5 males and 6 females), and elderly (Range = 60-79, M = 66.85, SD = 4.67 years; n = 7, 4 males and 3 females). Subjects had no complaints or history of swallowing difficulties and no past or current medical conditions or medication usage that might affect oral sensorimotor function, deglutition, or cognition. All subjects passed a swallowing screening and an oral motor screening. This study was approved by the Institutional Review Board of the National Institutes of Health.

Instrumentation

An Advanced Technology Laboratories Ultramark 9 Ultrasound System (Bothell, WA) was used with a 3.5– 6.0 mHz wide aperture annular array transducer to collect real-time, midsagittal images of swallowing at 900 sector angle. Focal depth was set to 7-11 cm, depending on the size of the subject’s tongue and head. Focal zones were set to 4-6 cm for optimal visualization of the hyoid shadow, floor-of-the-mouth (FOM) muscles, and tongue surface. The ultrasound signals were routed through a Horita II Time Code Generator (Mission Viejo, CA, Model TRG-50PC) and a Horita Multiple I/O Video Distribution Amp (Model VDA-50) at 1/30-s speed to a Sony U-matic videocassette recorder (Tokyo, Japan, Model VO-5850).

A transducer holder assembly (Figure 1, a) was custom-made to stabilize the scan head and eliminate manual handling. This assembly consisted of an aluminum and Delrin (high-quality plastic) block with two control knobs for azimuthal rotation and attitudinal angling. At its base the holder assembly was connected to a grooved horizontal boom, the opposite end of which was attached to the head of a heavy duty tripod via a cylindrical aluminum adapter and a tightening knob. These arrangements provided several degrees of freedom for up-down, left-right, and front-back adjustments as well as angling, permitting individualized transducer positioning and stabilization.

With the subject seated comfortably in a dental chair and the head rest properly adjusted, the subject’s head was secured to the head rest with a soft cloth head band (5.6 x 48 cm). The transducer was then placed under the chin, with its marked centers at the front and on the left side aligned, respectively, to the center of the subject’s upper incisors, and to the 1/3-point of the subject’s jaw length (measured with calipers) from the mental symphysis. To ensure a full view of the hyoid shadow in the acquired midsagittal images, the transducer was tilted from 15 deg to 36.5 deg (M = 24.8, SD = 5.8) posterior to vertical across subjects.

Head and transducer stabilization was necessary for experimental control. This setup did not prohibit but presumably limited jaw movement. Unlike in mastication where jaw movement is essential, during a pharyngeal swallow the jaw is relatively fixed such that contraction of the suprahyoid muscles results in hyoid elevation (Hiatt & Gartner, 1987). Nonetheless, it is possible that the transducer placement altered normal jaw and hyoid coupling. The extent of such alteration was suspected to be minimal.

Swallowing Tasks

Swallowing tasks included discrete swallows of 5 cc, 10 cc, 20 cc, 30 cc and cup-drinking of 120 cc of thin, juice-like, lemon-colored liquid at 7-cP viscosity. Two trials of each task were carried out, and the task order was randomized. All discrete boluses were calibrated and presented via syringes. For drinking, a graduated cup with part of its rim cut off was used; this enabled tilting of the cup while the subject’s head remained upright and stabilized.

For the discrete swallowing tasks, subjects were reminded to begin immediately upon the swallow command, to complete each given task in a single swallow, and to relax the tongue to the floor of the mouth immediately after the swallow. For the sequential swallowing task, subjects were instructed to “drink the whole amount as fast as you can without pausing between swallows.” By design, volume per swallow and total number of swallows during drinking were not controlled. Estimation of average bolus volume was not performed.

Data Analysis

Offline digitization of the videotaped swallows was accomplished via a Scion LG-3 Grayscale Scientific PCI Frame Grabber with the Scion Image software (Frederick, MD) on a PowerMac system. On submental midsagittal ultrasound, the hyoid bone characteristically casts a distinct shadow. Near the base of the scan, the anterior border of this darkened region intersects with the FOM muscles that are also clearly distinguishable because of stronger echoes than the surrounding medium (see Figure 1, b). As shown in Figure 1, during an ultrasound-depicted swallow, the hyoid shadow moves from its starting position in a direction toward the front of the tongue (Figure 1, c-e; hereafter referred to as the forward movement; similar to the anterior-superior hyoid motion seen during swallowing on videofluorography), reaches maximal displacement and remains in place for a short period (Figure 1, f), and moves back toward its starting position (Figure 1, g-h; hereafter referred to as the backward movement). This hyoid excursion is accompanied by readily visible swallow-related FOM muscle contraction and relaxation (Figure 1, c-h). These image characteristics permitted systematic tracking of the spatial and temporal changes in hyoid movement throughout a task response on the digitized scans. Positional changes, as points with X and Y Cartesian coordinates (white dots in Figure 1), were measured frame-by-frame by visual identification of the intersection of the anterior border of the black hyoid shadow and the superior border of the imaged FOM muscles. Each frame was a 640 x 480 matrix of pixels scaled to the unit of centimeters at 39 pixels per cm based on the known depth (indicated by numeric markers with ticks in Figure 1) of the ultrasound scans. The reference point where X and Y were both zero was at the upper left corner of each frame (Figure 1, b). All measurements were made with software-determined basic contrast enhancement (histogram stretching) using NIH Image Version 1.61 with a custom macro (Rasband, 1996).

Our 30 subjects produced a total of 240 discrete task responses, four of which were disqualified because of double swallows. The data set for sequential task responses included 53 first swallows (Seq1st) and 265 qualified subsequent/sequential swallows (Seq). To qualify, each Seq swallow must (a) have a between– swallow interval of

From the tracked changes in event timing and X andY coordinates, 12 dependent variables were derived, including the following:

Maximal amplitude (cm): maximal displacement (Figure 1, f) in two-dimensional space in the forward movement trajectory, relative to the hyoid position at the start of its swallow-related motion (Figure 1, c); the distance between the starting and the ending positions of forward hyoid movement, calculated from the measured sets of X and Y coordinates as the square root of the sum of squares.

End-start amplitude difference (cm): distance in the X dimension between the ending and the starting hyoid positions for a given swallow (i.e., ending X coordinate in Figure 1, h minus starting X coordinate in Figure 1, c).

Total distance (cm): sum of frame-by-frame displacements from start to end of a swallow (Figure 1, c-h), including the distance traversed in both the forward and backward movement trajectories.

Forward peak velocity (cm/s): peak tangential velocity in the forward movement trajectory while the hyoid was en route to maximal displacement.

Backward peak velocity (cm/s): peak tangential velocity in the backward movement trajectory while the hyoid was retracting from maximal displacement.

Start-to-max duration (s): interval from the onset of swallow-related forward hyoid movement to the first moment of maximal displacement (Figure 1, c-f).

At-max duration (s): interval from the first to the last moments of hyoid remaining at maximal displacement.

Max-to-end duration (s): interval from the last moment of maximal displacement to the first moment of maximal hyoid retraction at the end of a swallow (Figure 1, f-h).

Total duration (s): interval from the start of swallow-related forward hyoid movement to the first moment of maximal retraction (i.e., sum of start-to-max, at-max, and max-to-end durations; Figure 1, c-h).

Time to forward peak velocity (s): interval from start of swallow-related hyoid motion to time of forward peak velocity.

Time to backward peak velocity (s): interval from start of swallow-related hyoid motion to time of backward peak velocity.

Stiffness index: ratio of forward peak velocity to maximal amplitude.

This study was of a doubly multivariate repeated measures design. Observations were averaged across trials or repetitions by task for each subject. With Subject as the experimental unit and Task, Age Group, and Gender as factors, main effects were tested using the SAS Proc Mixed model with Bonferroni-Holm adjustment of a for multiple repeated measures analyses of variance (SAS Institute Inc., 2001). Where significant main effects were found, post hoc contrasts were conducted via individual repeated measures ANOVA with Tukey-Kramer adjustment of p values to correct for multiple comparisons.

Additionally, correlation analyses were performed by task using the linear regression approach to determine and contrast the relationships between forward peak velocity and maximal amplitude as well as between the ratio of these two variables (stiffness index) and start– to-max duration. Furthermore, descriptive analysis was conducted on the displacement waveforms by subject and task, contrasting the differences between discrete and rapid sequential swallows and stratifying the individual profiles into common patterns based on observations in three areas: maximal amplitude, ending amplitude, and total distance.

Although stringent criteria were followed while tracking hyoid shadow displacement, a subjective component was inherent in the determination of coordinate changes. Thus, an intermeasurer reliability test was performed on the calculated frame-by-frame displacements of two measurers from 33 discrete and 27 sequential swallows (10.6% of total) of five randomly selected subjects. The overall correlation coefficient (Pearson r) for 892 time-matched pairs of displacement values was 0.799 [F(1, 890) = 1572, p

Results

Task Effects

Task had significant main effects on all measures tested except forward peak velocity. Interactions were not significant in all but two cases-task by age for max– to-end duration and task by gender for total distance (see Age Effects and Gender Effects sections). Table 1 lists the means and standard deviations by task for the individual dependent variables with their corresponding p values and Bonferroni-Holm adjusted a for the main effects.

Post hoc comparisons revealed that rapid sequential swallows, regardless of order, had significantly reduced maximal amplitude (maximal displacement), total distance, at-max and total durations, and time to backward peak velocity compared with discrete swallows of any volume. Seq (but not Seq1st) swallows also had significantly lower backward peak velocity than all discrete swallows. In stiffness index, on the contrary, Seq1st/Seq swallows had significantly greater values than any discrete task responses. Although Seq1st/Seq swallows were consistently shorter than discrete swallows in other timing measures, only the following contrasts were significant after key-Kramer adjustments ofp: Seq1st/Seq

Comparisons between Seq1st and Seq swallows showed significant difference in only two measures. Specifically, Seq swallows had greater maximal amplitude (p = .0219) and max-to-end duration (p = .0082) than Seq1st swallows.

Seq1st/Seq swallows did not contribute to the significant main task effect for end-start amplitude difference. Post hoc comparisons showed that in contrast to 5-cc swallows, larger volume swallows (20 cc and 30 cc) ended with the hyoid shadow at a place significantly short of its starting position (i.e., not returning all the way; hence a positive end-start amplitude difference score); the same was true for the contrast between 10 cc and 30 cc (see Table 1). For Seq swallows, in general, the hyoid bone also did not return fully to its starting position. However, the end-start amplitude difference was not significantly different from that for any discrete swallows. Examination of the raw data of individual subjects revealed that over 50% had a high, positive end– start amplitude difference score for their Seq swallows, unlike their 5-cc swallows where the hyoid shadow ended in a considerably more retracted position than that at the start of movement (hence a negative difference score).

In addition to end-start amplitude difference, significant contrasts were found between selected discrete swallowing tasks in maximal amplitude and start-to– max duration. Specifically, larger-volume swallows (20 cc and 30 cc) had greater maximal amplitude than smaller-volume swallows (5 cc and 10 cc), and 5-cc swallows were longer in start-to-max duration than 30-cc swallows (see Table 1).

As illustrated in Figure 2, regression analyses of the relationship between forward peak velocity and maximal amplitude by task with subject as the experimental unit revealed modest correlations for 5-cc, 10– cc, and 20-cc swallows (ranging from .45 for 20 cc to .70 for 5 cc). Correlations were weak, however, for 30-cc swallows (r = .38) and even weaker for Seq1st/Seq task responses (r = .33/.30, respectively). The slopes differed significantly from zero for all discrete but not Seq1st/ Seq swallows. The runs tests showed no significant departure from linearity in all cases.

Figure 3 presents scatter plots with linear regression lines and 95% confidence intervals for the ratio of forward peak velocity to maximal amplitude as a function of start-to-max duration. In all cases, the runs tests showed no significant departure from linearity. A moderate to moderately strong inverse relationship (i.e., the shorter the duration the greater the ratio) was evident for all discrete swallows (r ranging from .41 for 5 cc to .81 for 20 cc) and Seq1st swallows (r = .68) with significantly non-zero slopes. For Seq swallows, this relationship was essentially nonexistent (r = .04), and the slope was not significantly non-zero (p = .8199).

Four basic patterns of differences between Seq and discrete task responses (Figure 4) were revealed by descriptive analysis of the displacement profiles (changes in XY displacement over time) of individual subjects. In Pattern 1 (observed in 10/30 subjects), Seq swallows, relative to discrete swallows, were characterized by lower maximal amplitude, higher ending amplitude, and shorter total distance traversed. Pattern 2 (observed in 10/30 subjects) depicted overall reductions in maximal amplitude, ending amplitude, and total distance for Seq swallows, in contrast to discrete swallows. In Pattern 3 (observed in 6/30 subjects), Seq swallows had considerably higher ending amplitude and shorter total distance than discrete swallows, but an essentially unchanged average maximal amplitude. Pattern 4, relatively less common (observed in 4/30 subjects) but more complex in waveform, was characterized by lower maximal amplitude but essentially unchanged ending amplitude and total distance for Seq swallows. Further examination showed that in Pattern 4, maximal amplitude often occurred at the end of a Seq swallow, and total distance was increased in Y but reduced in X, thus essentially unchanged in XY.

Our subjects used an average of 8 swallows (M SD = 8.05 2.42, Range = 4-16) to consume 120 cc of liquid during the rapid drinking task. Typically, the first several sequential swallows would meet the criterion for between-cycle interval and the last one to three would be discrete, clearing swallows. About 64% of the rapid drinking series ended with one discrete clearing swallow. No apparent differences were observed in mean total number of swallows and mean number of discrete ending swallows by age or gender.

All subjects indicated during postexperiment interviews that they swallowed “faster” for the drinking task than they did for the other tasks.

Age Effects

The main effect of age was not significant for any variables as assessed by the Bonferroni-Holm method. Visual inspection of data, however, showed a systematic increase with age in the means for maximal amplitude (1.37 +/- 0.47, 1.51 +/- 0.54, 1.67 +/- 0.65), total distance (3.16 +/- 1.06, 3.43 +/- 1.12, 3.83 +/- 1.27), and start-to-max duration (0.43 +/- 0.16, 0.54 +/- 0.19, 0.60 +/- 0.21) and a systematic decrease with age in mean stiffness index (5.89 +/- 1.73, 5.37 +/- 1.47, 4.84 +/- 1.50).

Post hoc test was performed on the significant interaction between task and age for max-to-end duration. Results attributed this significant interaction to the “Seq > Seq1st” contrast for the oldest age group only (0.68 +/– 0.13 vs. 0.49 +/- 0.20, p = .0231).

Gender Effects

The main effects of gender were significant for maximal amplitude [F(1, 24) = 16.60, p = .0004, adjusted a = .0042], total distance [F(1, 24) = 11.80, p = .0022, adjusted a = .0045], and forward peak velocity [F(1, 24) = 9.53, p = .0050, adjusted a = .0050]. Post hoc comparisons showed that males had significantly higher mean scores for these parameters than did females: 1.70 +/- 0.60 versus 1.28 +/- 0.41 for maximal amplitude, 3.90 +/- 1.21 versus 2.92 +/- 0.86 for total distance, and 8.24 +/- 2.64 versus 6.68 +/- 2.04 for forward peak velocity. Data inspection also revealed consistently higher mean scores for males than for females in backward peak velocity (7.55 +/- 2.32 vs. 6.02 +/- 2.37), time to backward peak velocity (0.85 +/- 0.24 vs. 0.75 +/- 0.19), and total duration (1.11 +/- 0.32 vs. 0.99 +/- 0.30), though statistical significance was not reached after Tukey-Kramer adjustment of p.

Post hoc test was performed on the significant interaction between task and gender for total distance. Results attributed this significant interaction to the “male > female” contrasts for swallows of 5 cc (4.30 +/– 1.15 vs. 3.01 +/- 0.72), 10 cc (4.34 +/- 0.99 vs. 2.84 +/- 0.63), and 20 cc (4.59 +/- 1.07 vs. 3.28 +/- 0.91), but not Seq1st (2.75 +/- 0.63 vs. 2.29 +/- 0.62), Seq (2.94 +/- 0.49 vs. 2.55 +/– 0.64), or 30 cc (4.51 +/- 1.24 vs. 3.61 +/- 0.96) after Tukey– Kramer adjustment of p.

Discussion

This study found conclusive evidence for rejecting the hypothesis of increased velocity as the main kinematic strategy for hyoid motion during rapid sequential swallowing. As in past investigations (Chi-Fishman & Sonies, 2000; Chi-Fishman et al., 1998), rapid sequential swallows had significantly shorter durations than discrete swallows of any volume. However, detailed kinematic analyses of the present study revealed that shortened hyoid movement durations were not an index of faster movement pace. As evidenced, task effect on average peak velocity in the forward movement trajectory was not significant. Average peak velocity in the backward trajectory was significantly lower for sequential than for all discrete swallows. The main kinematic strategy identified was a significant reduction in maximal amplitude (magnitude of displacement) and total distance traversed. That is, for the healthy individuals sampled in this study, the perception of a “faster” swallow was based on the strategy of completing the task in shorter time by reducing the range of movement and not by increasing movement speed. The evidence that amplitude was reduced for sequential swallows suggests flexibility in the functional range of deglutitive hyoid motion. In healthy adults, safe swallowing apparently can be accomplished during rapid drink-swallow cycles without that extent of maximal hyoid displacement characteristic of discrete swallows. This further supports the notion that the pharyngeal phase of deglutition, conventionally believed to be immutable, can respond to sensory and proprioceptive modulations based on the demands of the task at hand.

Kinematic differences between discrete and sequential swallows were further illustrated by correlation analyses of the relationship between forward peak velocity and maximal amplitude and how the ratio of these two variables changed as a function of time to maximal amplitude. In both analyses, discrete swallows in general showed moderate correlations, whereas correlations for sequential swallows were weak or nonexistent. The contrast, again, appeared to be based on whether velocity was the kinematic parameter manipulated for task accommodation.

The velocity-amplitude correlation has been substantiated for a variety of movements involving voluntary anisometric muscle contractions in, for example, the limb, speech, and eye motor systems (see Ostry, Keller, & Parush, 1983 for review). In fact, rapid reduplicating limb and speech motions are characteristically accomplished with increased velocity that changes the slope of the length-tension curves of agonist and antagonist muscles, and the mechanism for increasing movement speed at the level of muscle mechanics is an increase in the stiffness of the musculature (Cooke, 1980; Ostry et al., 1983). Within this paradigm, increased muscle stiffness is equivalent to an increase in the ratio of “peak velocity to maximal amplitude” (Cooke, 1980).

In the present study, the finding that sequential swallows, without increasing velocity, had significantly greater average stiffness indices than discrete swallows of any volume presented a paradox. Mathematically, an increase in the “peak velocity to maximal amplitude” ratio can be achieved in one of two ways: by increasing velocity while holding amplitude constant or by decreasing amplitude while keeping velocity unchanged. The latter turned out to be our case. Thus, conceptually, our result seemed to implicate stiffness adjustment as a mechanism for producing task-induced hyoid amplitude scaling. The accuracy of this implication remains undetermined, as a generalized reduction in contraction force in the suprahyoid musculature during sequential swallowing could also produce a decrease in maximal amplitude. A derived kinematic index of stiffness may not be operationally appropriate for the dynamic act of swallowing.

The displacement profiles of our individual subjects, originally stratified into common patterns according to maximal amplitude, ending amplitude, and total distance, revealed three distinct strategies for sequential swallowing. These strategies appeared to involve varying degrees of tonic and phasic muscle activities and varying temporal-spatial patterns of muscle activation. Specifically, rapid sequential swallows in both Patterns 1 and 3 exhibited a characteristic, persistently elevated ending amplitude (“higher” hyoid position at end of sequential swallows as compared to that for discrete swallows), suggesting increased levels of tonic or sustained muscle activity throughout the task series. Past submental surface EMG during rapid sequential swallowing showed a similar pattern that corresponded to a cyclical “rise and partial fall” movement characteristic of the hyolaryngeal region on simultaneous videofluorography (Chi-Fishman & Sonies, 2000). Heightened and sustained muscle activity is likely to contribute to increased muscle stiffness, less reciprocity, and greater coactivation of antagonist muscles, resulting in reduced maximal amplitude. In contrast, in Pattern 2, relatively little tonic activity was exhibited throughout the sequential task series, suggesting a greater degree of reciprocity in the activation of antagonist muscles. Pattern 4, characterized by multiple peaks, could be due to distinct muscle force vectors being out of phase in their timing, suggesting differences in muscle geometry and relative timing of distinct muscle groups to be the potential contributing factors. Hyoid anatomy is known to be quite variable across human specimens (Zemlin, 1998). The anatomy of our Pattern 4 subjects could be distinct.

To elucidate the mechanisms responsible for the control of hyoid movements during rapid sequential swallowing, future studies are needed to directly examine the mechanical properties of suprahyoid and infrahyoid muscles in relation to force output, the contributions of their respective tonic and phasic activities to displacement scaling, and the interplays between subgroups of suprahyoid muscles that can serve as agonists and antagonists during contraction (e.g., mylohyoid, geniohyoid, and anterior belly of the digastric vs. stylohyoid and posterior digastric belly). Critical examinations of some of the fundamental neurophysiological factors are equally important to a better understanding of the mechanisms for task-induced deglutitive hyolaryngeal motor control, including properties of the motor units, characteristics of their driving neural signals (e.g., firing rate, recruitment order and size, activation frequency and pattern), and modulation by afferent feedback from the periphery.

Rademaker et al. (1998) reported increased videofluoroscopic hyoid movement duration with age in healthy women. The same age-induced trend was observed in the present study for not only hyoid movement duration but also displacements. However, the main effect of age did not reach statistical significance after stringent Bonferroni-Holm corrections of a for multiple tests.

Leonard, Kendall, McKenzie, Goncalves, and Walker (2000) reported greater videofluoroscopic hyoid displacement in males than in females. In the present study, gender-based differences were found significant in not only maximal amplitude but also total distance and forward peak velocity. Male-female differences in hyolaryngeal anatomy and suprahyoid muscle contractile force are the likely factors contributing to these findings.

By design, this study did not control for the amount of fluid intake per swallow during rapid continuous drinking. Because rapid continuous drinking typically ended in one to three discrete clearing swallows, computing an average volume based on the total amount consumed and the total number of swallows tallied would be inaccurate. Because volume is three-dimensional, we also elected not to estimate volume from 2D midsagittal ultrasound images. Therefore, the contribution of bolus volume to the differences found between sequential and discrete swallows could not be directly addressed. However, for 8 of the 11 variables subjected to post hoc comparisons-that is, all but maximal amplitude, end-start amplitude difference, and start-to-max duration-contrasts between pairs of discrete swallowing tasks were not significant, whereas sequential-discrete comparisons were significantly different. It appears that the majority of the measures in this study were not confounded by the factor of bolus volume. Nonetheless, for optimal experimental control, future investigations in this area may consider a protocol that induces sequential swallowing via mechanical oral infusion of liquid at graded rates (cf. Issa & Porostocky, 1994).

Conclusions

Sequential swallowing differs significantly from discrete swallows in hyoid movement kinematics and strategy. When the instruction was to drink as rapidly as one can, amplitude down-scaling was the predominant strategy employed by the healthy subjects of this study to achieve shortened movement duration without increasing peak velocity. This finding suggests a greater flexibility in the functional range of hyoid motion. Future studies are needed to better understand the mechanics of the individual participating muscles and the neurophysiological details of the responsible mechanisms.

Acknowledgments

The authors thank Mr. David Chow for developing an NIH-Image macro to expedite displacement tracking, Miss Julie Lei and Mr. Antony Hsu for assistance with image processing and data reduction, Drs. Betty Wang and Robert Wesley for statistical support, and Mr. Michael Harris-Love for technical consultation on muscle physiology.

Copyright American Speech-Language-Hearing Association Jun 2002

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