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Role of Vertical Larynx Movement and Cervical Lordosis in F0 Control

Kiyoshi Honda, Hiroyuki Hirai, Shinobu Masaki and Yasuhiro Shimada
Language and Speech 1999 42: 401
DOI: 10.1177/00238309990420040301
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401

LAN GUAGE AND SPEECH, 1999, 42 (4), 4 01 41 1

R ole of Vertical Larynx Movement

and Cervical Lordosis in F0 Control*
a

KIYOSHI HONDA,

SHINOBU MASAKI,

HIROYUKI HIRAI,

YASUHIRO SHIMADA

a ATR

Human Information Processing Research Laboratories,

Kyoto, Japan
b Sanyo Electric, Co., Hypermedia Research Center, Osaka, Japan
c Takanohara Central Hospital, Nara, Japan
KEY WORDS

ABSTRACT

The role of vertical larynx movement in vocal frequency (F0) change has
attracted the attention of many researchers. Recently, Hirai, Honda,
extrinsic laryngeal
Fujimoto, and Shimada (1994) proposed a mechanism of F0 control by
muscles
vertical larynx movement based on the measurement of magnetic resonance
images (MRI). In F0 changes, the larynx moves vertically along the cervical
magnetic resonance
spine, which displays anterior convexity (lordosis) at the level of the larynx.
imaging (MRI)
Therefore, the vertical larynx movement results in the rotation of the cricoid
cartilage and vocal fold tension changes. The present study reexamines the
vertical larynx
above mechanism based on a qualitative analysis of midsagittal MRI data
movement
using three male subjects with evident cervical lordosis. Tracings of the jaw,
hyoid bone, laryngeal cartilage, and cervical spine were compared in high
voice fundamental
and low F0 ranges. In the high F0 range, the hyoid bone moved horizonfrequency (F0)
tally while the larynx height remained relatively constant. In the low F0
range, the entire larynx moved vertically, and the cricoid cartilage rotated
along the cervical lordosis. These results indicate that the vertical movement of the larynx comprises
an effective F0 lowering mechanism, and suggest that the human morphologies of low larynx position
and spinal curvature contribute to voluntary use of the vocal function.
cervical lordosis

INTRODUCTION

It is well-established that in sustained phonation larynx height tends to be associated with

the voice fundamental frequency (F0). Roughly speaking, the larynx moves up and down
as F0 rises and falls. This suggests that vertical movement of the larynx is a critical
component of F0 control mechanisms. In the literature, however, this empirical observation
has lacked plausible physiological explanation. Due to the anatomical complexity of the
neck region, the linkage between vertical larynx movement and vocal fold tension is not
self-explanatory. Therefore, in this study, functional characteristics of the cervical structures
are investigated in search of physiological mechanisms of extralaryngeal F0 control.
* Note: A version of this paper was presented at the International Conference on Voice Physiology
and Biomechanics May 2831, 1997 in Evanston, Illinois.
Address for correspondence: Kiyoshi Honda, ATR Human Information Processing Research
Laboratories, 2 2 Hikaridai, Seika-cho, Soraku-gun, Kyoto 619-0288 Japan. Fax: + 81 -77495-1008; e-mail: < honda@hip.atr.co.jp>
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Vertical larynx movement and F0

The phenomenon of vertical larynx movement in F0 changes has been noted using
X-ray observations of the larynx during phonation: Moeller and Fischer (1904) recorded
changes in the positions and orientations of the laryngeal cartilages associated with pitch
changes; Curry (1937) observed progressive upward movements of the hyoid bone and
larynx in pitch raising; Chiba and Kajiyama (1941) also showed that a higher larynx position
was associated with a higher pitch produced with different phonation types. A number of
researchers have attempted to explore the causal mechanisms: Kenyon (1927), Sonninen
(1956, 1968), and Zenker (1964) proposed biomechanical explanations for the role of the
extrinsic muscles in tilting the thyroid cartilage and proposed possible pathways of force
between the larynx and the surrounding structures. Later, EMG studies revealed that the
sternohyoid muscle, one of the strap muscles in front of the neck, contributes towards F0
lowering possibly by pulling the larynx downward (Faaborg-Anderson & Sonninen, 1960;
Ohala & Hirose, 1970; Simada & Hirose, 1970). However, how vertical larynx movement
by the action of this muscle results in changes in vocal fold tension has never been clarif ied.
To our knowledge, the most effective action of the larynx contributing to changes in
vocal fold tension is the rotation of the cricothyroid joint (Arnold, 1961; Fink, 1975; Negus,
1935; Tschiassny, 1944). With this mechanism the cricothyroid muscle effectively stretches
the vocal folds and increases their tension. On the other hand, the muscles involved in the
vertical movements of the larynx do not exert a direct force causing the cricothyroid joint
rotation. If all components of the larynx move up and down in tandem, there is no biomechanical effect on the internal configuration of the larynx. Therefore, the role of vertical
larynx movement in F0 control has been a mystery.
Since the measurement of larynx position is technically difficult, there are not many
studies investigating vertical larynx movements in speech or singing. Previous measurements of larynx position have employed various techniques using optical (Ewan & Krones,
1974; Kakita & Hiki, 1976), mechanical (Gandour & Maddieson, 1976), and X-ray devices
(Lindqvist, Sawashima, & Hirose, 1973; Shipp, 1975). Lateral X-ray cinematography
provides a good view of the neck region, but it is often inadequate for the purpose of
measuring laryngeal movements due to the poor contrast of the cartilages or the shadow
cast by the shoulders. Magnetic resonance imaging (MRI) is a relatively new technique for
visualizing the forms of speech organs (Baer, Gore, Gracco, & Nye, 1991). Although this
technique is limited to static imaging of the vocal tract during the sustained production of
vowels and some consonants, the successive display of various speech gestures can reveal
the pseudodynamic movements of speech organs. From such successive image sequences,
the vertical movement of the laryngeal cartilages can be readily inferred. This vertical
motion of the larynx takes place along the cervical spine, which shows lordosis (anterior
convexity of the spine) at the level of the larynx. A close examination of the laryngeal
images indicates that the cricoid cartilage rotates as it moves up and down along the cervical
lordosis. Given this observation as a hint, Hirai, Honda, Fujimoto, and Shimada (1994)
measured the geometry of the laryngeal cartilages and cervical spine during vowel
production on a descending musical scale. Their main finding was a mechanism for rotating
the cricoid cartilage by means of the vertical larynx movement and cervical lordosis.
The aim of the present study is to reexamine the earlier work by Hirai et al. (1994)
in the context of recently acquired MRI data. Although the previous study gave solid
evidence of the role of vertical larynx movement in F0 control, some observations were
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403

inconsistent: the degree of cervical lordosis varied among subjects. This was probably due
to the flexibility of the spinal column in the young and the supine posture required during
MRI data collection. The spinal column is flexible at birth, and it gradually develops
relatively fixed curves (Crelin, 1973). The sigmoid shape of the spinal column in the
lateral view is a result of adaptation to gravity in the upright posture (Asmussen, 1960),
and it tends to diminish in the supine posture (Okajima & Taniguchi, 1959). The cervical
curvature is secondary or compensatory to the primary thoracic curvature (Davis &
Coupland, 1967). It is likely therefore that the young subjects used in the previous MRI
experiment had straight cervical spines in the supine posture.
In this study, MRI recordings of the head and neck region were obtained for three
middle-aged male subjects during the performance of the same task as used in the previous
experiment. Qualitative differences in laryngeal movements were examined in relation to
the curvature of the cervical spine.
METHOD

MRI experiments were performed to record the positions of the articulators and the larynx
during vowel production with different F0 values. The MRI scanner was a Shimadzu
SMT-100GUX (1.0 [T ]) with a neck receiver coil. The three male subjects (three of the
authors), aged from 40 to 45, took a supine posture in the MRI scanner, and produced 12
repetitions of sustained vowel /a / according to a descending musical major scale spanning
one and a half octaves from 262 Hz to 87 Hz. The subjects listened to a guide tone for each
target F0, and then initiated the vowel. For each vowel production, a midsagittal image
was recorded using a standard spin-echo method. The scan time for each image was five
seconds. Since the subjects had experience as MRI subjects, they maintained a steady
posture of the speech organs during these scans. Cushions behind the neck and head provided
for head stability during the experiment. One subject (KH) did not use a head cushion
because of the small size of the receiver coil (approximately 23 cm in the inner front-back
diameter).
The obtained images were displayed on a computer screen with 8-bit gray-scale
resolution. Manual tracings were performed by the first author to extract the visible outlines
of the tongue, mandibular symphysis, hyoid bone, thyroid cartilage, cricoid cartilage, and
cervical spine. Although the cartilages were not clearly demarcated in all of the images,
certain landmark points were always recognizable. Therefore, the outline of each cartilage
was traced from one of the clear images, and then the tracings were fitted on other images
by rotation and translation. This procedure was also used for outlining the mandibular
symphysis and the body of the hyoid bone.
Figure 1 shows an example of the images with tracings for one speaker (KH). The
tracings in this figure show the outlines of rigid structures such as the jaw, hyoid bone (H),
thyroid cartilage (T), and cricoid cartilage (C). The dashed line indicates the orientation of
the cricoid cartilage. The left image is the data for the highest tone (262 Hz) and the right
image is that for the lowest tone (87 Hz). In both figures, the dashed line marks the inferior
border of the cricoid cartilage, which serves as a good indicator of the rotation of this
cartilage. The three marking points were located on the nose and the posterior nasal spine
to indicate the degree of head movements. All of the tracings were grouped into two dataDownloaded from las.sagepub.com at University of York on August 18, 2014

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Vertical larynx movement and F0

Figure 1
Examples of MR images for the highest and lowest tones.

sets, one for the upper half of the F0 range (262 Hz to 165 Hz) and one for the lower half
(147 Hz to 87 Hz). These sets of superimposed images were analyzed for the degree of
movements and angular changes.
RESULTS

Figure 2 shows tracings for the three subjects (KH, SM, and YS) in two groups for six
high tones and six low tones. In the figure, all three subjects show cervical lordosis
within the range of laryngeal movement, though the form of curvature varies to some
extent among the subjects. The arrows in the figure indicate the direction of movement
towards a lower F0. As F0 decreases, the jaw opens, and the hyoid bone tends to move
backward and then downward. The laryngeal cartilages move downward monotonically
in the low F0 range. The movement patterns of these traced structures are consistent across
the subjects. Generally, the extent of movement is smaller in the high F0 range than in the
low F0 range.
Subject KH in Figure 2(a) shows no curvature in the whole extent of the cervical spine
(C2 C7). Anterior convexity is only seen at the bottom of the cervical spine (between C7
and T1). The supine posture without a head cushion seems to be a factor in straightening
the cervical spine. In the high F0 range, the jaw and hyoid bone move slightly backward
as F0 falls, and the vertical larynx movement is relatively small. For low tones, the jaw and
hyoid bone move slightly downward, and the larynx demonstrates a large downward
movement. The cricoid cartilage rotates as it descends, which appears to be facilitated by
the change in the degree of cervical lordosis.
Subject SM in Figure 2 (b) shows gradual arch-like lordosis of the cervical spine at
the level of the larynx (between C5 & C7). In the high F0 range, the hyoid bone moves
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Figure 2
Movements of the jaw, hyoid bone, laryngeal cartilages, and cervical spine in a high F0 range (left)
and low F0 range (right).
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Vertical larynx movement and F0

TABLE 1

The angular change of the cricoid cartilage

High F0 range

Low F0 range

Total range

(262Hz 165Hz)

(147Hz 87 Hz)

(262Hz 87 Hz)

KH

4.12

7.45

12.77

SM

2.73

4.90

8.62

YS

3.90

5.69

9.93

Subject

backward as F0 falls, while the laryngeal cartilages maintain a constant position. In the
low F0 range, the jaw, hyoid bone, and larynx show a large downward displacement. The
rotation of the cricoid cartilage along the cervical spine is also evident.
Subject YS in Figure 2 (c) also shows cervical lordosis at the level of the larynx
(between C5 & C7). In the high F0 range, a backward movement of the hyoid bone and a
downward movement of the larynx is observed. Head movement is also observed near the
highest F0 level. In the low F0 range, all of the structures of the jaw, hyoid bone, and
laryngeal cartilages show a large downward movement. The cricoid cartilage rotates as it
moves along the lordosis. The cervical spine also shows a small change in the degree of
convexity.
Table 1 indicates the degree of cricoid cartilage rotation in the high and low F0 ranges.
Each value in the table corresponds to the angle between the dashed lines in Figure 2. For
all three subjects, the rotation of the cricoid cartilage is larger in the low F0 range than in
the high F0 range. Note, however, that the values in the table do not necessarily indicate
the angle of cricothyroid joint rotation because the thyroid cartilage can also rotate
independently.
The above MRI data consistently demonstrate that the cricoid cartilage rotates as it
descends along the lordosis of the cervical spine. The posterior plate of the cricoid cartilage
maintains a parallel relationship with the arch of the cervical lordosis. The dashed line
marking the inferior border of the cricoid cartilage keeps a perpendicular orientation to
the outline of the cervical spine. In addition, the cervical spine shows a subtle change in
form: the cervical lordosis is less obvious in the high F0 range, while it is more pronounced
in the low F0 range. This change suggests an active manipulation of the cervical spine to
facilitate the rotation of the cricoid cartilage to raise F0.
Besides the above two observations, the positions of the tongue and jaw demonstrate
a signif icant change. In all of the data, the tongue-jaw complex shifts downward and
backward as F0 decreases. The MRI tracings for the whole range of F0 show that the tongue
position changes according to the movement of the hyoid bone. The tongue movement
results in an expansion of the oral cavity, which is accompanied by the lengthening of the
pharyngeal cavity due to larynx lowering. Since vocal tract constriction for the vowel /a /
moves closer to the glottis as the larynx moves downward, it seems at least for this vowel
that the vocal tract maintains a proportional shape for the vowel, with different lengths of
the vocal tract.
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407

Figure 3
Horizontal and vertical components of the extralaryngeal F0 control mechanisms.

DISCUSSION

A few possible mechanisms of the extralaryngeal control of F0 can be derived from the
above results. Figure 3 depicts two major components. In the high F0 range, as shown in
Figure 3(a), horizontal movement of the hyoid bone can be consistently observed. The
forward movement of the hyoid bone is produced by the action of the suprahyoid articulatory muscles such as the genioglossus and geniohyoid muscles (Honda, 1983), and
facilitates rotation of the thyroid cartilage for raising F0. The vertical larynx movement is
relatively small in this F0 range. In the low F0 range, in Figure 3(b), a large vertical
movement of the hyoid-larynx complex is observed along the cervical spine. The larynx
lowering is mainly due to contraction of the infrahyoid extrinsic laryngeal muscles. This
action induces rotation of the cricoid cartilage along the cervical lordosis. As a result, larynx
lowering contributes to vocal fold shortening and relaxation.
The horizontal movement of the hyoid bone and its effect on F0 have been discussed
with respect to causal mechanisms of intrinsic vowel F0. The tendency for the vowel
height to be associated with F0 is found in all languages observed to date (Whalen & Levitt,
1995), and it seems to reflect a certain biomechanical interaction between the larynx and
supralaryngeal articulators. In vowel production, the posterior fibers of the genioglossus
elevate the tongue dorsum, and they also pull the hyoid bone forward. As the hyoid bone
advances, the thyroid cartilage receives a passive force from the hyoid bone and rotates at
the cricothyroid joint in a direction to stretch the vocal folds. Therefore, the biomechanical
coupling of the tongue and larynx via the hyoid bone serves as a plausible causal mechanism
of intrinsic vowel F0 (Honda, 1983). However, whether the thyroid cartilage rotates due to
hyoid bone movement lacks empirical support. In this study, the images of the thyroid
cartilage were obscure, and any changes in its angle were not detectable. Note that besides
the above explanation there are many other accounts of the causal mechanisms of intrinsic
vowel F0 (Ohala, 1973; Sapir, 1989; see Honda, 1995, for review).
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Vertical larynx movement and F0

The observation of the vertical movement of the larynx and its effect on the cricoid
cartilage is consistent with the main result of the previous study by Hirai et al. (1994). Since
the cricoid cartilage moves up and down with its posterior plate facing the anterior convexity
of the cervical spine, vertical movements of the larynx naturally result in the rotation of
the cricothyroid joint. This linkage is effected by the tension of the connective tissues and
muscles along the pharynx, which maintain the laryngeal cartilages held on the cervical
spine. The present study shows that the vertical larynx movement is larger in the low F0
range than in the high F0 range. Therefore, this action offers the most effective F0 lowering
mechanism in the range where the action of the cricothyroid muscle is no longer available.
The results also suggest that, in the low F0 range, vocal fold length is adjusted mainly by
the rotation of the cricoid cartilage, not of the thyroid cartilage. Hirai et al. (1994) reported
one exceptional case, however: the cricoid cartilage moved down almost in parallel along
the straight cervical spine and the thyroid cartilage rotated backward as F0 decreased. This
fact implies that the orientation of the thyroid cartilage may be independently controlled
by an as yet unknown mechanism.
The importance of vertical movement of the larynx in vocal performance has been
extensively studied by Sonninen (1956). He examined the effect of the sternothyroid muscle
on the cricothyroid joint at various head positions of human cadavers. When this muscle
was pulled downward manually, the larynx moved downward and the space between the
thyroid and cricoid cartilage expanded. This suggests that larynx lowering is a causal
factor for rotating the cricothyroid joint in a direction that shortens the vocal folds. The
change in the cricothyroid angle was most obvious when the cadaver head was bent
backward with a cushion behind the shoulders, and it was less obvious when the head was
flexed forward. These observations are consistent with the F0 lowering mechanism proposed
in this study, and provide evidence that the effect of vertical larynx movement on the vocal
fold length is dependent on the degree of cervical lordosis.
The role of the sternothyroid muscle in the adjustment of vocal fold length has also
been questioned (e.g., Niimi, Horiguchi, & Kobayashi, 1991). Since this muscle attaches
to the thyroid cartilage and runs in front of the cricothyroid joint, it can cause lengthening,
rather than shortening, of the vocal folds by rotating the thyroid cartilage forward. Obviously
this anatomically-based account contradicts Sonninens observations. Considering that the
sternothyroid muscle also produces larynx lowering jointly with the sternohyoid muscle,
it is reasonable to assume that the combined action of these infrahyoid muscles for F0
lowering can overcompensate for the potential action of the sternothyroid muscle alone
for vocal fold lengthening. Many EMG studies have shown that the activity of the
sternohyoid muscles is associated with F0 lowering in speech utterances (see Hall, 1994,
for review), with a few studies including the data for both of the infrahyoid muscles
(Atkinson, 1978; Erickson, 1993; Simada & Hirose, 1970). It seems therefore that the
main role of these muscles in F0 lowering, if not their exclusive role, is the active use of
the mechanism proposed in this study.
The MRI data also indicate a curious change in the form of the cervical spine. Near
the highest F0, the cervical spine at the level of the cricoid cartilage changes its curvature
and this resulted in a slight regional kyphosis (anterior concavity of the spinal column).
Backward bending of the cervical spine behind the cricoid cartilage seems to facilitate
backward rotation of the posterior plate of the cricoid cartilage. Contrarily, in the low F0
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409

range, the enhanced cervical lordosis helps rotate the cricoid cartilage and shorten the vocal
folds. Consequently, regional lordosis and kyphosis of the cervical spine contribute to a
fine adjustment of F0. This implies that the deep cervical muscles are used in achieving a
wide range of vocal performance. There are approximately twenty pairs of muscles involved
in the extension, flexion, and rotation of the neck, and some of these muscles are thought
to contribute to this change. The regional kyphosis may also contribute to varying the
voice quality as well as F0. Other factors being equal, this change in the form of the cervical
spine is reflected by a widening of the pharyngeal cavity above the laryngeal vestibule. This
configuration of the vocal tract is used by singers to produce a certain musical voice
quality (Honda, Hirai, Estill, & Tohkura, 1995).
To summarize, overall F0 control seems to arise from the coordination of mechanisms
that involve both intrinsic and extrinsic laryngeal factors. The two mechanisms for raising
and lowering F0 discussed in this study must be functionally linked to the actions of the
intrinsic laryngeal muscles (i.e., the cricothyroid and thyroarytenoid muscles) in the normal
process of speech production. The dissociation of the linkage (e.g., high larynx position
with shorter vocal folds for low F0) may contribute to different dimensions of voice
control such as voice quality.
CONCLUSION

Physiological studies of F0 control mechanisms have focused on a relatively small number

of factors such as the action of the intrinsic laryngeal muscles and the effect of the subglottal
pressure. As is generally the case in human behavior, however, vocal control may reflect
numerous physiological mechanisms that are available for use. The present study showed
evidence that movements of the laryngeal framework and cervical spine comprise an
important factor of F0 control mechanisms. Such extralaryngeal mechanisms of F0 control
are characterized by a large articulatory variability (Honda, 1985). This implies that F0 is
not an independent parameter of the voice source but an element shared by vowel sounds.
The mechanism of F0 lowering by larynx lowering stems from the unique morphology
of human cervical organs, which have arisen from the major changes of the body in human
evolution. There are two morphological factors underlying the mechanisms discussed: one
is the curvature of the spinal column, and the other is the descent of the human larynx. The
enlargement of the brain case and human upright bipedalism are major causal factors of
the sigmoid curvature of the spinal column. The larynx descent is another outcome of
these changes of the human body, and it parallels the formation of the right-angled vocal
tract in humans (DuBrul, 1958; Fink, 1975). Due to all of these changes, the position of
the human larynx reaches the point of maximum lordosis of the cervical spine. Therefore,
it is highly likely from a morphological point of view that gross changes in the human
body play a significant role in increasing the capacity of the vocal function.
Received: November 11, 1997; revised manuscript received: February 1, 1999;
accepted: March 29, 1999

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