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DOI: 10.1177/00238309990420040301

1999 42: 401Language and SpeechKiyoshi Honda, Hiroyuki Hirai, Shinobu Masaki and Yasuhiro Shimada

Role of Vertical Larynx Movement and Cervical Lordosis in F0 Control

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401

Role of Vertical Larynx Movement

and Cervical Lordosis in F0 Control*

KIYOSHI HONDA,a

HIROYUKI HIRAI,b

SHINOBU MASAKI,aYASUHIRO SHIMADA

c

aATR Human Information Processing Research Laboratories,Kyoto, Japan

b Sanyo Electric, Co., Hypermedia Research Center, Osaka, Japan

c Takanohara Central Hospital, Nara, Japan

INTRODUCTION

It is well-established that in sustained phonation larynx height tends to be associated withthe voice fundamental frequency (F0). Roughly speaking, the larynx moves up and downas F0 rises and falls. This suggests that vertical movement of the larynx is a criticalcomponent of F0 control mechanisms. In the literature, however, this empirical observationhas lacked plausible physiological explanation. Due to the anatomical complexity of theneck region, the linkage between vertical larynx movement and vocal fold tension is notself-explanatory. Therefore, in this study, functional characteristics of the cervical structuresare investigated in search of physiological mechanisms of extralaryngeal F0 control.

* Note: A version of this paper was presented at the International Conference on Voice Physiologyand Biomechanics May 2831, 1997 in Evanston, Illinois.

Address for correspondence: Kiyoshi Honda, ATR Human Information Processing ResearchLaboratories, 22 Hikaridai, Seika-cho, Soraku-gun, Kyoto 619-0288 Japan. Fax: +81-774-95-1008; e-mail:

LANGUAGE AND SPEECH, 1999, 42 (4), 401 411

ABSTRACTThe role of vertical larynx movement in vocal frequency (F0) change hasattracted the attention of many researchers. Recently, Hirai, Honda,Fujimoto, and Shimada (1994) proposed a mechanism of F0 control byvertical larynx movement based on the measurement of magnetic resonanceimages (MRI). In F0 changes, the larynx moves vertically along the cervicalspine, which displays anterior convexity (lordosis) at the level of the larynx.Therefore, the vertical larynx movement results in the rotation of the cricoidcartilage and vocal fold tension changes. The present study reexamines theabove mechanism based on a qualitative analysis of midsagittal MRI datausing three male subjects with evident cervical lordosis. Tracings of the jaw,hyoid bone, laryngeal cartilage, and cervical spine were compared in highand low F0 ranges. In the high F0 range, the hyoid bone moved horizon-tally while the larynx height remained relatively constant. In the low F0range, the entire larynx moved vertically, and the cricoid cartilage rotated

along the cervical lordosis. These results indicate that the vertical movement of the larynx comprisesan effective F0 lowering mechanism, and suggest that the human morphologies of low larynx positionand spinal curvature contribute to voluntary use of the vocal function.

KEY WORDScervical lordosis

extrinsic laryngealmuscles

magnetic resonanceimaging (MRI)

vertical larynx

movement

voice fundamentalfrequency (F0)

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402 Vertical larynx movement and F0

The phenomenon of vertical larynx movement in F0 changes has been noted usingX-ray observations of the larynx during phonation: Moeller and Fischer (1904) recordedchanges in the positions and orientations of the laryngeal cartilages associated with pitchchanges; Curry (1937) observed progressive upward movements of the hyoid bone andlarynx in pitch raising; Chiba and Kajiyama (1941) also showed that a higher larynx positionwas associated with a higher pitch produced with different phonation types. A number ofresearchers have attempted to explore the causal mechanisms: Kenyon (1927), Sonninen(1956, 1968), and Zenker (1964) proposed biomechanical explanations for the role of theextrinsic muscles in tilting the thyroid cartilage and proposed possible pathways of forcebetween the larynx and the surrounding structures. Later, EMG studies revealed that thesternohyoid muscle, one of the strap muscles in front of the neck, contributes towards F0lowering 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 stretchesthe vocal folds and increases their tension. On the other hand, the muscles involved in thevertical movements of the larynx do not exert a direct force causing the cricothyroid jointrotation. If all components of the larynx move up and down in tandem, there is no biome-chanical 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 measure-ments 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 cinematographyprovides a good view of the neck region, but it is often inadequate for the purpose ofmeasuring 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 forvisualizing the forms of speech organs (Baer, Gore, Gracco, & Nye, 1991). Although thistechnique is limited to static imaging of the vocal tract during the sustained production ofvowels and some consonants, the successive display of various speech gestures can revealthe pseudodynamic movements of speech organs. From such successive image sequences,the vertical movement of the laryngeal cartilages can be readily inferred. This verticalmotion of the larynx takes place along the cervical spine, which shows lordosis (anteriorconvexity of the spine) at the level of the larynx. A close examination of the laryngealimages indicates that the cricoid cartilage rotates as it moves up and down along the cervicallordosis. Given this observation as a hint, Hirai, Honda, Fujimoto, and Shimada (1994)measured the geometry of the laryngeal cartilages and cervical spine during vowelproduction on a descending musical scale. Their main finding was a mechanism for rotatingthe 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 solidevidence of the role of vertical larynx movement in F0 control, some observations were



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403K. Honda, H. Hirai, S. Masaki, and Y. Shimada

inconsistent: the degree of cervical lordosis varied among subjects. This was probably dueto the flexibility of the spinal column in the young and the supine posture required duringMRI data collection. The spinal column is flexible at birth, and it gradually developsrelatively fixed curves (Crelin, 1973). The sigmoid shape of the spinal column in thelateral 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 cervicalcurvature is secondary or compensatory to the primary thoracic curvature (Davis &Coupland, 1967). It is likely therefore that the young subjects used in the previous MRIexperiment had straight cervical spines in the supine posture.

In this study, MRI recordings of the head and neck region were obtained for threemiddle-aged male subjects during the performance of the same task as used in the previousexperiment. Qualitative differences in laryngeal movements were examined in relation tothe curvature of the cervical spine.

METHOD

MRI experiments were performed to record the positions of the articulators and the larynxduring vowel production with different F0 values. The MRI scanner was a ShimadzuSMT-100GUX (1.0 [T]) with a neck receiver coil. The three male subjects (three of theauthors), aged from 40 to 45, took a supine posture in the MRI scanner, and produced 12repetitions 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 eachtarget F0, and then initiated the vowel. For each vowel production, a midsagittal imagewas recorded using a standard spin-echo method. The scan time for each image was fiveseconds. Since the subjects had experience as MRI subjects, they maintained a steadyposture of the speech organs during these scans. Cushions behind the neck and head providedfor head stability during the experiment. One subject (KH) did not use a head cushionbecause of the small size of the receiver coil (approximately 23 cm in the inner front-backdiameter).

The obtained images were displayed on a computer screen with 8-bit gray-scaleresolution. Manual tracings were performed by the first author to extract the visible outlinesof the tongue, mandibular symphysis, hyoid bone, thyroid cartilage, cricoid cartilage, andcervical spine. Although the cartilages were not clearly demarcated in all of the images,certain landmark points were always recognizable. Therefore, the outline of each cartilagewas traced from one of the clear images, and then the tracings were fitted on other imagesby rotation and translation. This procedure was also used for outlining the mandibularsymphysis and the body of the hyoid bone.

Figure 1 shows an example of the images with tracings for one speaker (KH). Thetracings in this f igure 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 ofthe cricoid cartilage. The left image is the data for the highest tone (262 Hz) and the rightimage is that for the lowest tone (87 Hz). In both figures, the dashed line marks the inferiorborder of the cricoid cartilage, which serves as a good indicator of the rotation of thiscartilage. The three marking points were located on the nose and the posterior nasal spineto indicate the degree of head movements. All of the tracings were grouped into two data-



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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 sixhigh tones and six low tones. In the f igure, all three subjects show cervical lordosiswithin the range of laryngeal movement, though the form of curvature varies to someextent 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 movebackward and then downward. The laryngeal cartilages move downward monotonicallyin the low F0 range. The movement patterns of these traced structures are consistent acrossthe subjects. Generally, the extent of movement is smaller in the high F0 range than in thelow 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 C7and 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 backwardas F0 falls, and the vertical larynx movement is relatively small. For low tones, the jaw andhyoid bone move slightly downward, and the larynx demonstrates a large downwardmovement. The cricoid cartilage rotates as it descends, which appears to be facilitated bythe change in the degree of cervical lordosis.

Subject SM in Figure 2 (b) shows gradual arch-like lordosis of the cervical spine atthe level of the larynx (between C5 & C7). In the high F0 range, the hyoid bone moves

Figure 1

Examples of MR images for the highest and lowest tones.

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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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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. Therotation 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 adownward movement of the larynx is observed. Head movement is also observed near thehighest F0 level. In the low F0 range, all of the structures of the jaw, hyoid bone, andlaryngeal cartilages show a large downward movement. The cricoid cartilage rotates as itmoves 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. Forall three subjects, the rotation of the cricoid cartilage is larger in the low F0 range than inthe high F0 range. Note, however, that the values in the table do not necessarily indicatethe angle of cricothyroid joint rotation because the thyroid cartilage can also rotateindependently.

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 cartilagemaintains a parallel relationship with the arch of the cervical lordosis. The dashed linemarking the inferior border of the cricoid cartilage keeps a perpendicular orientation tothe outline of the cervical spine. In addition, the cervical spine shows a subtle change inform: the cervical lordosis is less obvious in the high F0 range, while it is more pronouncedin the low F0 range. This change suggests an active manipulation of the cervical spine tofacilitate the rotation of the cricoid cartilage to raise F0.

Besides the above two observations, the positions of the tongue and jaw demonstrate

a significant change. In all of the data, the tongue-jaw complex shifts downward andbackward as F0 decreases. The MRI tracings for the whole range of F0 show that the tongueposition changes according to the movement of the hyoid bone. The tongue movementresults in an expansion of the oral cavity, which is accompanied by the lengthening of thepharyngeal 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 vowelthat the vocal tract maintains a proportional shape for the vowel, with different lengths ofthe vocal tract.

TABLE 1

The angular change of the cricoid cartilage

High F0 range Low F0 range Total range

Subject (262Hz165Hz) (147Hz87Hz) (262Hz87Hz)

KH 4.12 7.45 12.77

SM 2.73 4.90 8.62

YS 3.90 5.69 9.93



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DISCUSSION

A few possible mechanisms of the extralaryngeal control of F0 can be derived from theabove results. Figure 3 depicts two major components. In the high F0 range, as shown inFigure 3(a), horizontal movement of the hyoid bone can be consistently observed. Theforward movement of the hyoid bone is produced by the action of the suprahyoid articu-latory muscles such as the genioglossus and geniohyoid muscles (Honda, 1983), andfacilitates rotation of the thyroid cartilage for raising F0. The vertical larynx movement isrelatively small in this F0 range. In the low F0 range, in Figure 3(b), a large verticalmovement of the hyoid-larynx complex is observed along the cervical spine. The larynxlowering 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, larynxlowering contributes to vocal fold shortening and relaxation.

The horizontal movement of the hyoid bone and its effect on F0 have been discussedwith respect to causal mechanisms of intrinsic vowel F0. The tendency for the vowelheight 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 andsupralaryngeal articulators. In vowel production, the posterior fibers of the genioglossuselevate 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 atthe cricothyroid joint in a direction to stretch the vocal folds. Therefore, the biomechanicalcoupling of the tongue and larynx via the hyoid bone serves as a plausible causal mechanismof intrinsic vowel F0 (Honda, 1983). However, whether the thyroid cartilage rotates due tohyoid bone movement lacks empirical support. In this study, the images of the thyroidcartilage were obscure, and any changes in its angle were not detectable. Note that besidesthe above explanation there are many other accounts of the causal mechanisms of intrinsicvowel F0 (Ohala, 1973; Sapir, 1989; see Honda, 1995, for review).

Figure 3

Horizontal and vertical components of the extralaryngeal F0 control mechanisms.



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The observation of the vertical movement of the larynx and its effect on the cricoidcartilage is consistent with the main result of the previous study by Hirai et al. (1994). Sincethe cricoid cartilage moves up and down with its posterior plate facing the anterior convexityof the cervical spine, vertical movements of the larynx naturally result in the rotation ofthe cricothyroid joint. This linkage is effected by the tension of the connective tissues andmuscles along the pharynx, which maintain the laryngeal cartilages held on the cervicalspine. The present study shows that the vertical larynx movement is larger in the low F0range than in the high F0 range. Therefore, this action offers the most effective F0 loweringmechanism 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 bythe rotation of the cricoid cartilage, not of the thyroid cartilage. Hirai et al. (1994) reportedone exceptional case, however: the cricoid cartilage moved down almost in parallel alongthe 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 controlledby an as yet unknown mechanism.

The importance of vertical movement of the larynx in vocal performance has beenextensively studied by Sonninen (1956). He examined the effect of the sternothyroid muscleon the cricothyroid joint at various head positions of human cadavers. When this musclewas pulled downward manually, the larynx moved downward and the space between thethyroid and cricoid cartilage expanded. This suggests that larynx lowering is a causalfactor 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 bentbackward with a cushion behind the shoulders, and it was less obvious when the head wasflexed forward. These observations are consistent with the F0 lowering mechanism proposedin this study, and provide evidence that the effect of vertical larynx movement on the vocalfold length is dependent on the degree of cervical lordosis.

The role of the sternothyroid muscle in the adjustment of vocal fold length has alsobeen questioned (e.g., Niimi, Horiguchi, & Kobayashi, 1991). Since this muscle attachesto 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. Obviouslythis anatomically-based account contradicts Sonninens observations. Considering that thesternothyroid muscle also produces larynx lowering jointly with the sternohyoid muscle,it is reasonable to assume that the combined action of these infrahyoid muscles for F0lowering can overcompensate for the potential action of the sternothyroid muscle alonefor vocal fold lengthening. Many EMG studies have shown that the activity of thesternohyoid 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 themain role of these muscles in F0 lowering, if not their exclusive role, is the active use ofthe mechanism proposed in this study.

The MRI data also indicate a curious change in the form of the cervical spine. Nearthe highest F0, the cervical spine at the level of the cricoid cartilage changes its curvatureand 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 facilitatebackward rotation of the posterior plate of the cricoid cartilage. Contrarily, in the low F0



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range, the enhanced cervical lordosis helps rotate the cricoid cartilage and shorten the vocalfolds. Consequently, regional lordosis and kyphosis of the cervical spine contribute to afine adjustment of F0. This implies that the deep cervical muscles are used in achieving awide range of vocal performance. There are approximately twenty pairs of muscles involvedin the extension, flexion, and rotation of the neck, and some of these muscles are thoughtto contribute to this change. The regional kyphosis may also contribute to varying thevoice quality as well as F0. Other factors being equal, this change in the form of the cervicalspine is reflected by a widening of the pharyngeal cavity above the laryngeal vestibule. Thisconfiguration of the vocal tract is used by singers to produce a certain musical voicequality (Honda, Hirai, Estill, & Tohkura, 1995).

To summarize, overall F0 control seems to arise from the coordination of mechanismsthat involve both intrinsic and extrinsic laryngeal factors. The two mechanisms for raisingand 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 normalprocess of speech production. The dissociation of the linkage (e.g., high larynx positionwith shorter vocal folds for low F0) may contribute to different dimensions of voicecontrol 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 subglottalpressure. As is generally the case in human behavior, however, vocal control may reflectnumerous physiological mechanisms that are available for use. The present study showedevidence that movements of the laryngeal framework and cervical spine comprise animportant factor of F0 control mechanisms. Such extralaryngeal mechanisms of F0 controlare characterized by a large articulatory variability (Honda, 1985). This implies that F0 isnot 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 humanevolution. There are two morphological factors underlying the mechanisms discussed: oneis the curvature of the spinal column, and the other is the descent of the human larynx. Theenlargement of the brain case and human upright bipedalism are major causal factors ofthe sigmoid curvature of the spinal column. The larynx descent is another outcome ofthese changes of the human body, and it parallels the formation of the right-angled vocaltract in humans (DuBrul, 1958; Fink, 1975). Due to all of these changes, the position ofthe 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 humanbody 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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