Biomechanical basis for lingual muscular deformation during
swallowing
Vitaly J.
Napadow1,
Qun
Chen2,
Van J.
Wedeen3, and
Richard J.
Gilbert1
1 Department of Mechanical Engineering,
Massachusetts Institute of Technology, Cambridge 02139; and
2 Department of Radiology, Beth Israel Deaconess
Medical Center, and 3 NMR Center
and Department of Radiology, Massachusetts General Hospital,
Harvard Medical School, Boston, Massachusetts 02215
 |
ABSTRACT |
Our goal was to
quantify intramural mechanics in the tongue through an assessment of
local strain during the physiological phases of swallowing. Subjects
were imaged with an ultrafast gradient echo magnetic resonance imaging
(MRI) pulse sequence after the application of supersaturated magnetized
bands in the x and
y directions. Local strain was defined
through deformation of discrete triangular elements defined by these
bands and was depicted graphically either as color-coded
two-dimensional strain maps or as three-dimensional octahedra whose
axes correspond to the principal strains for each element. During early
accommodation, the anterior tongue showed positive strain (expansive)
in the anterior-posterior direction (x), whereas the middle tongue
showed negative strain (contractile) in the superior-inferior direction
(y). During late accommodation, the anterior
tongue displayed increased positive
x-direction and y-direction strain, whereas the
posterior tongue displayed increased negative
y-direction strain. These findings
were consistent with contraction of the anterior-located intrinsic
muscles and the posterior-located genioglossus and hyoglossus muscles.
During propulsion, posterior displacement of the tongue was principally associated with positive strain directed in the
x and
y directions. These findings were
consistent with posterior passive stretch in the midline due to
contraction of the laterally inserted styloglossus muscle, as well as
contraction of the posterior located transversus muscle. We conclude
that MRI of lingual deformation during swallowing resolves the
synergistic contractions of the intrinsic and extrinsic muscle groups.
tongue physiology; deglutition; muscle mechanics
 |
INTRODUCTION |
DURING NORMAL SWALLOWING, the tongue undergoes a
stereotypical sequence of muscular deformations. The ingested bolus is
initially contained in a groove-like depression in the middle dorsal
surface of the tongue (early accommodation). This depression is then
translated in a posterior direction until the bolus comes to rest at
the posterior edge of the tongue (late accommodation). Finally, the oral stage of the swallow is concluded by the rapid clearance of the
bolus retrograde into the oropharynx (propulsion)
(5). The extent of muscular tissue deformation during
swallowing may vary under normal conditions as a function of bolus
volume (1) or viscosity (9), or it may be modified by
pathological effects on muscle contractility and/or neuromuscular
regulation (5).
Because of the complexity of lingual anatomy and its material
attributes, the relationship between tongue structure and mechanical function is not well understood. The anterior tongue consists of a
central region of orthogonally oriented intrinsic fibers (transversus
and verticalis) surrounded by a sheath-like tract of longitudinally
oriented intrinsic fibers (longitudinalis). The transversus and
longitudinalis muscles extend to the posterior tongue (6). The
posterior tongue contains a central region of fibers originating at the
mental spine of the mandible and projecting in a fan-like manner in the
superior, lateral, and posterior directions (corresponding to the
genioglossus). There are two major laterally inserted fiber
populations, the first directed posterior and inferior (corresponding
to the hyoglossus) and the second directed posterior and superior
(corresponding to the styloglossus). Furthermore, owing to its highly
aqueous content, the tongue tissue is effectively incompressible, and therefore it maintains the ability to deform without altering tissue
volume. In view of these factors, the assessment of the intramural
mechanics of the tongue during physiological motion on the basis of
surface properties alone is problematic (2, 3, 4, 10). We have
previously studied the intramural mechanics underlying lingual tissue
deformation through the assessment of regional strain by magnetic
resonance imaging during relatively simple motions, such as protrusion
and bending (10). In the current study, we have extended this magnetic
resonance technique to derive three-dimensional maps of intrinsic and
extrinsic muscular strain for the more complex deformations associated
with swallowing.
 |
MATERIALS AND METHODS |
Subjects (n = 8) were chosen for study
who possessed no history or current abnormalities of speech or
swallowing. These studies were approved by the Institutional Review
Board for Human Research of Beth Israel Deaconess Medical Center. Dry
(saliva only) swallows were elicited from the subjects, and magnetic
resonance imaging was performed for each swallow. The timing of image
acquisition was determined in such a manner as to visualize the various
phases of oral stage deglutition.
Magnetic resonance imaging.
Magnetic resonance imaging was performed with a 1.5 Tesla Siemens Vision MRI system, equipped with an anterior neck coil
that used an ultrafast asymmetric gradient echo pulse sequence
(TurboFLASH). The imaging parameters were as follows: repetition
time/echo time, 2.25/0.8 ms; matrix size, 80 × 128;
slice thickness, 10 mm; and effective spatial resolution, 1.33 × 1.33 mm, as previously described (8). The imaging pulse
sequence was preceded by saturation radiofrequency tagging pulses
(spacing 7 mm) that deform with and track actual tissue deformation.
Owing to the fact that image intensity was proportionate to the amount
of longitudinal magnetization before the imaging pulse sequence, the
tissue affected by the tagging pulses appeared as dark lines in
relation to the adjacent tissue. In a two-dimensional (2-D) image of
undeformed tissue, magnetic tags appeared as a rectilinear grid (7-mm
spacing between taglines), and, as such, deformation of the tagging
grid corresponded to local deformation of the actual tissue. For a
given subject, the experimental protocol was as follows: 1) application
of magnetic tags to the resting undeformed tongue muscle tissue, which,
through an audible click, prompted the subject to swallow; 2) variable delay of a set time interval (300-800 ms, in increments of 100 ms); and 3) imaging of the tagged, deformed tissue.
Strain quantification in the deformed tagged image.
Deformation was quantified in image postprocessing with
measures of nonlinear strain, a unitless measure of localized
deformation suited to quantifying large deformations. To resolve the
idealized material continuum of the tongue, discrete triangular
deforming elements were defined by digitizing nodes at tagline
intersections. Thus each triangular element was composed of two
independently deforming line elements whose length and angular
orientation related the axial and shear strain measured from the actual
deforming tongue tissue.
Although this tagging technique is inherently 2-D, the out-of-plane
axial strain was calculated by knowing the 2-D strain condition,
assuming that tongue muscle is incompressible (hence isochoric) and
that out-of-plane shear strains are negligible
|
(1)
|
where
E11,
E22, and
E33 are the principal strains.
Because Exz and
Eyz are assumed nil
|
(2)
|
These
assumptions are reasonable because the tongue tissue is highly aqueous
(water can be assumed incompressible), the swallow time scale does not
allow significant influx and efflux of blood or other fluids into the
tissue, and swallow kinematics are generally symmetrical about the
midsagittal plane.
Directional axial or shear strains were represented individually as a
color-coded "map," smoothed by bicubic approximating splines,
overlaying the original tagged image. The entire strain tensor was
alternately represented by a spatial array of octahedra, with each
octahedra centered on a tagging element's centroid. The major and
minor axes of these octahedra were oriented according to the directions
of the tensorial eigenvectors and scaled to the linear directional
axial stretch measured in the given tagging element. In addition, the
relative size of an octahedron was based on a scaling factor,
f, defined by a function of the strain
tensor's independent eigenvalues
(
1 and
2)
|
(3)
|
Thus
the relative size of an octahedron relates an overall measure of strain
inherent in the corresponding tongue tissue element.
Data analysis.
To obtain mean directional strain data, four regions in the midsagittal
slice of the tongue (anterior, midsuperior, posterior, and inferior;
Fig. 1) were sampled in the
x, y,
and z directions. Data were analyzed
for each region for three phases of oral-stage deglutition: early
accommodation, late accommodation, and propulsion. P values were computed for a one-sided
t-test, which tested whether or not a
sample mean was significantly greater than or less than zero. The means
and standard deviations for the one-sided
t-test were computed for each
condition.

View larger version (12K):
[in this window]
[in a new window]
|
Fig. 1.
Regional analysis of tongue mechanics. Segmentation of midsagittal
imaging slice was into 4 functional regions. Region
1: intrinsic musculature, including transversus,
verticalis, and longitudinalis. Region
2: anterior genioglossus and posterior intrinsic
fibers. Region 3: posterior fibers of
genioglossus muscle. Region 4:
inferior genioglossus and geniohyoid fibers. Coordinate axes
x, y,
and z correspond to anterior-posterior
(x), inferior-superior
(y), and medial-lateral
(z) directions.
|
|
On the basis of previous determinations of tissue myoarchitecture and
function in the midsagittal plane, the anterior tongue region
(region 1) encompasses the tongue's
intrinsic musculature (transversus, verticalis, and longitudinalis
muscles). The middle superior tongue region (region
2) encompasses the anterior fibers of the
genioglossus muscle and a portion of the intrinsic muscles. The
posterior tongue region (region 3)
encompasses predominantly the posterior fibers of the genioglossus
muscle. Although regions 2 and
3 subdivide the genioglossus muscle,
there is precedent for heterogeneous, localized activity in this
muscle, as has been previously suggested by
electromyography studies (7). The inferior tongue region
(region 4) encompasses the inferior
fibers of the genioglossus muscle, as well as the geniohyoid muscle.
These regions were also chosen to help clarify the multidimensional
(both time and space) strain data. The coordinate axes
x, y,
and z correspond to anterior-posterior
(x), inferior-superior
(y), and medial-lateral (z) directions.
 |
RESULTS |
Direction-dependent strain fields were acquired for the midsagittal
slice of the tongue with the use of a tissue-tagging nuclear magnetic
resonance technique. Normal subjects were studied during three phases
of dry swallows: early accommodation, late accommodation, and
propulsion. Strain data were visualized either as 2-D strain maps
(axial strain in the x,
y, and
z directions) for representative subjects, or as octahedra representing the complete strain tensor (directional strain in principal directions) for each deforming element
(Figs. 2-4). In addition, intersubject axial strain means for each
of four functional regions of the tongue were also displayed (Table
1).
In early accommodation, the subject contained the bolus in the middle
portion of the tongue's dorsal surface (Fig.
2). The anterior tongue showed a
characteristic pattern of positive (expansive) x-direction strain (peak strain
0.521), whereas the middle tongue showed negative (contractile)
y-direction strain (peak strain
0.319), along with positive x-
and z-direction strain (peak strains 0.477 and 0.803, respectively). The posterior and inferior regions of
the tongue demonstrated x-direction
expansion (peaking at 0.208 and 0.477, respectively). Intersubject mean
data corroborated these deformation patterns
(P < 0.01; Table 1).

View larger version (71K):
[in this window]
[in a new window]
|
Fig. 2.
Lingual strain during early accommodation. Direction-dependent strain
fields were acquired for midsagittal slice of tongue with use of
tissue-tagging nuclear magnetic resonance imaging and discrete element
analysis. A grid of saturation magnetic resonance imaging tags was
applied to resting tissue to create a set of deforming elements. Strain
data were visualized either as two-dimensional (2-D) strain maps (axial
strain in x,
y, and
z directions) or as octahedra
representing complete strain tensor (directional strain in principal
directions) for each deforming element.
A: deformed grid associated with
tongue movement. B: triangular finite
element mesh associated with tongue movement.
C: three-dimensional strain tensor
depicted as octahedra corresponding to each element.
D-F:
2-D strain maps depicting axial strain in
x
(D),
y
(E), and
z
(F) directions. Bolus containment is
associated with negative y-direction
strain consistent with a synergistic contraction of anterior
genioglossus and hyoglossus, with concomitant
x- and
z-direction expansion.
|
|
During late accommodation (Fig. 3), with
the subject holding the bolus in a posterior depression, the anterior
tongue displayed positive y-direction
strain (peak strain 0.151). The posterior tongue displayed significant
negative y-direction
strain (peak strain
0.302) with commensurate
expansion along the x and
z directions (peaking at 0.358 and
1.845, respectively). Intersubject mean data also corroborated these
deformation patterns (P < 0.01;
Table 2). Thus bolus accommodation (early
and late) principally represents a combination of contraction of the
intrinsic core muscles in the anterior tongue (with commensurate
anterior or superior expansion) and inferiorly-directed contraction of
the extrinsic muscles (genioglossus and hyoglossus) in the middle and
posterior regions of the tongue.

View larger version (82K):
[in this window]
[in a new window]
|
Fig. 3.
Lingual strain during late accommodation. Direction-dependent strain
fields (A-F) are as described in Fig. 2.
Combination of y-direction contraction
in posterior tongue and expansion in anterior tongue results in
shifting of bolus to posterior dorsal surface of tongue, consistent
principally with contraction of posterior genioglossus and concomitant
x- and
z-direction expansion.
|
|
During the propulsive phase of the swallow (Fig.
4), the bolus is propelled retrograde into
the oropharynx by posterior displacement and deformation of tongue
tissue. During this phase, the strain results in the posterior
genioglossus presented expansive x-
and y-direction strain (peaking at
0.469 and 0.684, respectively) and contractile
z-direction strain (peaking at
0.374). These results were also seen as
statistically significant deformation patterns in intersubject mean
strain calculations (P < 0.001; Table 3). This result was consistent with
the existence of postero-superior-directed passive stretch in the
midline, and suggests concurrent contraction of the laterally inserted
styloglossus (not visualized in the current study), as well as
contraction of the z-directed muscle fibers characteristic of the intrinsic transversus muscle.

View larger version (61K):
[in this window]
[in a new window]
|
Fig. 4.
Lingual strain during propulsion. Direction-dependent strain fields
(A-F) are as described in Fig. 2;
x- and
y-direction expansion in posterior
tongue was consistent with contraction of laterally inserted
styloglossus (with associated passive drag) and
z-direction contraction of posterior
located transversus fibers.
|
|
 |
DISCUSSION |
The tongue is a muscular organ that is instrumental in the
manipulation, configuration, and delivery of the ingested bolus from
the oral cavity to the pharynx during swallowing. These functions are
carried out through a series of characteristic deformations, which are
designed to first control (early and late accommodation) and then
rapidly propel the bolus (propulsion). To determine the intramural
dynamics of the lingual musculature associated with these deformations,
we have used tagging magnetic resonance imaging to quantify local
muscle deformation (i.e., strain) in relation to overall tissue shape.
Strain, which was the measured result of our analysis, is a unitless
measure of normalized deformation. Positive strain signifies expansion,
whereas negative strain signifies tissue contraction. Through this
analysis, we have elaborated a series of spatially resolved strain maps
corresponding to regional muscular activity during the functional
phases of swallowing.
Early accommodation was characterized by the containment of the bolus
in a grooved depression at the middle portion of the tongue's dorsal
surface. This grooved depression appeared to have been created by a
contraction of the anterior genioglossus in combination with the
hyoglossus, verticalis (intrinsic), and transversus (intrinsic)
muscles. Verticalis contraction was seen as a region of negative
y-direction strain in the anterior
tongue (Fig. 2D), resulting in
x-direction expansion of the tongue
tip toward the incisors. Transversus contraction was suggested on the
basis of subtle z-direction negative
strain (Fig. 2E). There was,
however, strong evidence of negative
y-direction strain directly below the
bolus, producing a depression of the containing groove. This tissue
contraction could be the direct result of genioglossus contraction or
could have been caused through passive drag by contraction of the
hyoglossus, which inserts into the midportion of the tongue body
laterally from below (hence not visualized in the midsagittal slice).
Genioglossus contraction in the swallow has been demonstrated by
previous EMG studies (7), whereas synergistic involvement of the
hyoglossus could be inferred from the strain tensor visualization map
(Fig. 2C). This strain map demonstrated that the contractile eigenvectors (visualized as the short
axes of octahedra: the direction of greatest contractile strain when
z-direction strain is positive) were
oriented postero-inferiorly. Because the midsagittal slice is directly
medial to the lateral insertions of the hyoglossus, this strain pattern
was consistent with either genioglossus or hyoglossus contraction,
occurring independently or in concert. These contractions were
associated with x- and
z-direction expansion in this region,
elongating the grooved depression and improving bolus containment. The
x-direction expansion in the posterior
tongue aided in closing off the pharynx.
Late accommodation was characterized by a shifting of the bolus toward
the posterior dorsal surface of the tongue, in effect "priming the
lingual pump" before eventual propulsion into the oropharynx. The
soft palate was shifted superiorly, thus closing off the nasopharynx.
The most prominent finding during this phase was an increase of
negative y-direction strain (i.e.,
inferior-directed contraction) in the posterior region of the tongue,
which contained the bolus. This contraction is responsible both for the
creation of enhanced posterior depression and for extension of the
bolus depression in the x and
z directions (due to tissue
incompressibility). As noted above, although strain was directly imaged
within the genioglossus, contraction of either the hyoglossus or the
genioglossus could also have contributed to this pattern. Conceivably,
the degree to which these muscles contribute to the accommodating depression in the posterior tongue may also vary as a function of bolus
volume or viscosity or as a function of pathological regulation of
tongue contractility. Translation of the contractile region from the
anterior to the posterior genioglossus (early to late accommodation)
transferred the bolus retrograde via the grooved depression, preparing
the bolus for propulsion.
Bolus propulsion was characterized by the retrograde motion of the
tongue toward the pharyngeal wall, thus expelling the cradled bolus
from the oral cavity. The most prominent effect was on the posterior
tongue, with significant expansion of the tissue in the
x and
y directions and concomitant
z-direction contraction. Contraction
of intrinsic transversus muscle fibers in the posterior tongue most
likely produced this pattern, because tissue expansion in the
x and
y directions (due to incompressibility
of the tongue tissue) was seen. Octahedra in the posterior tongue had
their principal eigenvector (octahedral long axis), or the direction of
greatest expansion, oriented in a postero-superior direction. This
observation suggests that the styloglossus may have also been
contracted. Sole contraction of the styloglossus (in a postero-superior direction) could not produce expansive strain above its insertion point, in the midportion of the tongue's lateral surfaces because the
tongue is constrained from below. Styloglossus contraction should
stretch only the tongue tissue located between its insertion point and
the tongue's inferior attachment. Because we observed postero-superior
expansion in the posterior tongue all the way to the dorsal surface, a
synergistic mechanism involving the posterior transversus and
styloglossus may be in effect.
Our data were consistent with a biomechanical model in which the
intrinsic and extrinsic fibers function synergistically rather than as
independent actuators. In this regard, the unique myoarchitecture of
the tongue allows the organ to function efficiently as a muscular hydrostat (8, 11), a term whose properties include tissue incompressibility derived from a highly aqueous composition and the
ability to elicit tissue deformation while simultaneously providing
skeletal support for that tissue. The former is evidenced by
contracting lingual myofibers, which induce tissue compression along
fiber directions and tissue expansion along directions orthogonal to
the fibers (due to tissue incompressibility). In both accommodation and
propulsion, physiological function may have been performed though a
synergistic combination of tissue compression and expansion. In fact,
tissue incompressibility necessitates the simultaneous existence of
both compression and expansion for a given tissue element, whereas the
tongue's interdigitating myofibers ensure that compression/expansion
coupling synergistically produces the intended function. Conceivably,
deglutitive function in patients with oral phase dysphagia may be
impaired through a pathological reorganization of the underlying
myoarchitecture and the concomitant alteration of compression/expansion distribution.
In summary, we have used magnetic resonance imaging techniques to study
intramural muscle mechanics for the tongue during normal swallowing.
Our results provide evidence for a synergistic mechanical model
involving the intrinsic and extrinsic muscles during physiological
tissue deformation and suggest a basis for examining structure-function
relationships in this tissue during normal and pathological conditions.
 |
FOOTNOTES |
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: R. J. Gilbert, Dept. of Mechanical Engineering, Massachusetts Institute of
Technology, 77 Massachusetts Ave., Cambridge, MA 02139 (E-mail:
rgilbert{at}mit.edu).
Received 22 February 1999; accepted in final form 23 June 1999.
 |
REFERENCES |
1.
Dantas, R. O.,
M. K. Kern,
B. T. Massey,
W. J. Dodds,
P. J. Kahrilas,
J. G. Brasseur,
I. J. Cook,
and
I. M. Lang.
Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing.
Am. J. Physiol.
258 (Gastrointest. Liver Physiol. 21):
G675-G681,
1990[Abstract/Free Full Text].
2.
Dodds, W. J.,
E. T. Stewart,
and
J. A. Logemann.
Physiology and radiology of the normal oral and pharyngeal phases of swallowing.
AJR Am. J. Roentgenol.
154:
953-963,
1990[Medline].
3.
Gilbert, R. J.,
S. Daftary,
T. A. Campbell,
and
R. M. Weisskoff.
Patterns of lingual deformation associated with bolus containment and propulsion during deglutition as determined by echoplanar magnetic resonance imaging.
J. Mag. Reson. Imaging
8:
554-560,
1998.[Medline]
4.
Kahrilas, P. J.,
S. Lin,
J. A. Logemann,
G. A. Ergun,
and
F. Facchini.
Deglutitive tongue action: volume accommodation and bolus propulsion.
Gastroenterology
104:
152-162,
1993[Medline].
5.
Miller, A. J.
Deglutition.
Physiol. Rev.
62:
129-184,
1982[Free Full Text].
6.
Miyawaki, K.
A study of the musculature of the human tongue.
Ann. Bull. Res. Inst. Logoped. Phoniat.
8:
23-50,
1974.
7.
Miyawaki, K.,
H. Hirose,
T. Ushijima,
and
M. Sawashima.
A preliminary report on the electromyographic study of the activity of lingual muscles.
Ann. Bull. Res. Inst. Logoped. Phoniat.
9:
91-106,
1975.
8.
Napadow, V. J.,
Q. Chen,
V. J. Wedeen,
and
R. J. Gilbert.
Intramural mechanics of the human tongue in association with physiological deformations.
J. Biomech.
32:
1-12,
1999[Medline].
9.
Pouderoux, P.,
and
P. Kahrilas.
Deglutitive tongue force modulation by volition, volume, and viscosity in humans.
Gastroenterology
108:
1418-1426,
1995[Medline].
10.
Shawker, T. H.,
B. C. Sonies,
and
M. Stone.
Sonography of speech and swallowing.
In: Ultrasound Annual, edited by R. C. Sanders,
and M. C. Hill. New York: Raven, 1984, p. 237-260.
11.
Smith, K. K.,
and
W. M. Kier.
Trunks, tongues, and tentacles: moving with skeletons of muscle.
Am. Sci.
77:
29-35,
1989.
Am J Physiol Gastroint Liver Physiol 277(3):G695-G701
0002-9513/99 $5.00
Copyright © 1999 the American Physiological Society