Functional and descriptive anatomy of the bottlenosed dolphin nasolaryngeal system with special reference to the musculature associated with sound production

From: ANIMAL SONAR SYSTEMS Edited by Rene-Guy Busnel and James F. FISh (Plenum Publishing Corporation, 1980)

FUNCTIONAL AND DESCRIPTIVE ANATOMY OF THE BOTTLENOSED DOLPHIN NASOLARYNGEAL SYSTEM WITH. SPECIAL REFERENCE TO THE MUSCULATURE ASSOCIATED I,JITH SOUND PRODUCTION

R. F. Green, S. H. Ridgway, and W. E. Evans t

Naval Ocean Systems Center San Diego, Ca. 92132 U.S.A.

t f.lubbs-Sea World Research Institute San Diego, Ca. 92109 U.S.A.

INTRODUCTION

The nasolaryngeal system of the bottlenosed dolphin (Tursiops truncatus) is complex and highly specialized for respiration and sound production. The exact source and mechanism of sound production by do~phins is not understood. Electromyographic studies are essential for understanding the functional anatomy and mechanisms of sound production. Dissections and measurements have been made for the purpose of identifying extE~rnal landmarks and other details necessary for inserting electrodes in the muscles of the nasolaryngeal arE;a. Based upon these anatomic investigations, some functions of this musculature have been suggested, and the first electromyographic studies of dolphin acoustic mechanisms have been initiated.

Previous Studies

The biological community generally accepts the production of sound by the vast majority of living amniote vertebrates as beyond

w' question. Many assume that our understanding of how this vast array of acoustic e:missions are produced is at a high state of development. This is far from true. With the exception of humans, our knowledge of the mechanics vf sound production in vertebrates, especially cetaceans, is based on indirect evidence and speCUlation (Kelemen, 1963; Gaunt and Wells, 1973; Kinne, 1975).

The mechanisms of sound production in most vertebrates are essentially modifications of the respiratory system and are in

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200 R. F. GREEN ET AL.

reality an overlaid function. This factor more than any other has contributed to compounding the problem of understanding the mechanisms of sound production in marine mammals. We have not only inherent complexities of the terrestrial mammalian nasolaryngeal system but the added problems caused by modifications of the system to permit a) breathing air while inhabiting an aquatic environment, b) prolonged breath holding, c) diving to reasonably deep depth with resulting pressure problems, and d) the ingestion of food without taking water into the lungs. Despite years of discussions, special seminars, experiments, morphological descriptions and several studies of functional anatomy, uncertainty still exists, and the details of production of the vast variety of sounds found in the repertoire of cetaceans is still an unsolved mystery. Exact sites, muscular or mechanical processes, aerodynamics (flow, pressure,etc) and acoustical properties of the anatomic structures involved are insufficiently known even in the bottlenosed dolphin (Tursiops truncatus), the most intensively studied of all the species.

In birds, and more recently in studies of rodents and chiropterans(Hersh, 1966; Roberts, 1973, 1975a, 1975b; Gaunt et aI., 1976) additional insight has been gained by using inhalation of -light gases (HeO ), measurement of air flow and pressures, and electrical potentials of muscles thought to be involved in sound production in birds(Gaunt and Gaunt, 1977). We are now in the process of applying these t,ools to the study of sound production mechanisms in Tursiops. The data from these studies combined with the information already available from analytical measurements near presumptive sound production sites (Evans, 1973; Diercks et al., 1971; Romanenko, 1974), x-ray cinematography (Gurevich, 1973; Norris et al., 1971) and production of sound in light air (He02) and atmosphere (Evans and Rieger,1977, in preparation), should provide the base for an accurate description for the total system.

There is no need for an additional detailed description of the nasal sac system or the structure of the delphinid larynx; these have been more than adequately provided by Lawrence and Schevill (1956), Purves (1967), Mead (1972), and Schenkkan (1973). This report is a documentation of the total nasolaryngeal system with special reference to the musculature in relationship to external features for use as a stereotaxic guide in electromyographic and ultrasonic scanning studies.

Interest in how dolphins and other cetaceans produce sound goes back more than 100 years. Murie(l871), interpreted" a double raised smooth membranous fold" in the lower part of the larynx in Risso's dolphin (Grampus griseus), to represent the vocal cords and therefore to be the site of sound production. Dubois (1886), did not find vocal cords in any of the cetaceans he examined. He did agree, however, with Watson and Young (1879) who worked on beluga

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ANATOMY OF THE BOTTLENOSED DOLPHIN 201

whales, I:md Turner (1872), who studied fin whales. These workers assumed that the rear extensions of the arytenoid cartilages lie so close together that they would vibrate as air passed over them thus taking over the function of vocal cords. Lawrence and Schevill (1956) suggested the sounds were laryngeal in origin. As recently as 1967 Purves concluded that the mechanism of sound production in Phocoena phocoena is similar to sound production in man except that the aryepiglottal folds are called into play instead of the thyroarytenoid (vocal) folds. Evans and Prescott (1962) suggested a dual sound source; the larynx for whistles and the nasal plugs and associated sacs for pulses. Norris (1964, 1969) favors the nasal sac system as the site of sound generation. Diercks et al. (1971) also suggested a sound production site in the region Of the nasal plugs. Nord s et a1. (l971), Mead (1972), Schenkkan (1973), Evans and Maderson (1973), and Dormer (1974) further support the role of the nasal sacs and particularly the edges of the nasal plugs as the site of sound generation, especially for the pulses used in echolocation.

Some of the above conclusions concerning the site of sound production were derived by interpretation of anatomy while others were supported by a variety of experimental evidence. Roberts (1975a) has demonstrated that a comprehensive study of the anatomy of the rodent larynx, although informative, did not add much insight into a complete understanding of the function of this organ in the production of either audible or ultrasonic sounds. In further studies Roberts(1975b), using ablation of sections of the hypoglossal nerve, demonstrated the involvement of the intrinsic musculature of the larynx in the production of ultrasonic emissions. He also demonstrated that the muscles supplied by the hypoglossal nerves were not involved in the production of ultrasound. The use of this technique on delphinids, necessitating sacrifice of the animals, is impractical from an economic standpoint. Activity of specific muscles suspected of contributing to sound production can be measured using electromyographic (EMG) techniques. Studies of this nature also present some definite advantages over the nerve ablation method in that specific muscles can be studied. As far as can be determined

.. from the literature no one has approached the problem by EMG studies. Since the mu.scles must ultimately produce most of the force to activate the mechanisms by which sounds are produced, we view it as essential to find out how they are functioning during the production of sounds.

Of several anatomic studies on the larynx and nasal sac systems, little has been reported that would be useful for EMG studies. The contents of this report developed out of a need for more detailed anatomic information with reference to external landmarks. Our intent is to supplement studies done by others so as to obtain the necessary information to do EMG's.


MATERIALS AND METHODS

The bottlenosed dolphin, Tursiops truncatus (Figure 1), has been extensively investigated, and its echolocation capability is well documented (Evans, 1973; Altes, 1974). Since this is the species on which we plan to do EMG studies, all of the dissections, measurements, and illustrations were of this species.

Dolphins are valuable animals, and specimens for anatomic dissection are often hard to come by. The specimens for this study all came from animals that died of natural causes in the wild, in ocenariums or in our own laboratory.

The laryngeal dissections used as many as seven different dolphins. This explains why the various views of the laryngeal cartilages, muscles, etc. are not of the same size. The larynx was taken at postmortem examination and preserved in 10% formalin. The transverse, frontal and oblique sections are freehand sections and vary in thickness as indicated.

We were able to obtain the head of a Tursiops truncatus that had' been perfused with 10% formalin shortly after death. The head was sectioned into more than 30 transverse sections 1 cm thick.

Figure 1. Left lateral view of the bottlenosed dolphin, Tursiops truncatus.

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The sections ranged from 8-11 mm in average thickness and varied no more than 2 mm from side to side (Figure 30). The tissues exterior to the cranial cavity were found to be well fixed, but the brain-was in such poor condition that the brain sections were discarded and therefore not included in illustrations of the sections. In some ill.ustrations the details of cartilages, muscles and bone have been outlined.

RESULTS AND DISCUSSION

The Larynx

The larynx (Figure 2 and 3) is so specialized it is considered to be an organ useful in characterizing the cetacea. It is intranarial, projecting upward from the floor of the pharynx with its anterior end held firmly within the internal nares by a sphincter composed of palato-pharyngeal muscle (Negus, 1931). In odontocete cetaceans the opening of the external nares (blowhole) has migrated to a position on top of the head so that when the animal surfaces the opening into the nasal passage is the first part of the head to be exposed. The elongated intranarial larynx functions to keep the nasal air passages continuous with the glottis while the porpoise dashes through the water open mouthed after its prey (Huxley, 1888).

Laryngeal cartilases. With the exception of the so called "aryteno-epiglottal beak"; (Figure 2 and 3) the cetacean larynx 1S

similar in general structure to other mammalian larynges, being composed of a cartilag.enous framework held together by a number of muscles.

The thyroid cartilage (Figures 4,6,12,15,16,17,18,19,20,21,22, 25,26,27,and-zs) is made up of right and left laminae fused at their ventral margins without forming even the slightest laryngeal prominence. Each lamina has two well developed processes; the anteriorly directed cranial cornua and the posteriorly directed caudal cornua, the latter being the better developed. The thyroid cartilage forms the main body of the larynx. Most of the extrensic muscles, which function to move the complete larynx, are attached to this cartilage.

The caudal cornua of the thyroid cartilage articulate with the posterior-superior lateral margins of the cricoid cartilage by small oval synovial joints. Anteriorly the thyroid cartilage also articulates with the epiglottal cartilage. This articulation is by a fibrous joint that allows limited movement. Additional movement is suggested, however, by a slight bending of the cartilage which is especially thin just posterior to this joint.

204 R. F. GREEN ET AL

Figure 2. Left dorso-lateral view of the laryngeal beak of a bottlenosed dolphin.

Figure 3. A midsagittal section through the head of a bottlenosed dolphin. A- the nasal area, B- the laryngeal area.

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Figure 4. All laryngeal cartilages in approximate articulated position. 2- arytenoid cartilage, 6- cricoid cartilage, 8- cuneiform cartilage, 10- epiglottal cartilage, 12- thyroid cartilage, 14, 1st tracheal cartilage.

In Tursiops the cricoid cartilage (Figures 4,5,7,12,18,19,20, 21,22,24,25,~~and 27) is no~)mplete ring as is found in some cetaceans, but it is open ventrally, forming two rather long posteriorly projecting lateral cornua. These cornua almost fill the posterior lateral notch in each thyroid lamina.In addition to the joints formed between the cricoid and thyroid cartilages, there are much larger synovial joints along the anterior lateral margins of the body of the cricoid cartilage where the cricoid articulates with the arytenoid cartilages.

The de1phinid epiglottal cartilage (Figures 4,5,8,12,13,14,15, 16,17,22,23,2l~,25,26,and 27) is much longer than the epiglottal cartilage in Dlost mammals and has deepened medially to form a trough with thin lat€~ra1 margins projecting posteriad to wrap around the anterior borde,rs of the cuneiform and arytenoid cartilages, thereby forming the "laryngeal beak".

The arytenoid cartilages (Figures 4,5,9,12,17,18,19,22,24,25, and 26) articulate by well formed oval-shaped synovial joints with

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Figure 5. Laryngeal cartilages in approximate articulate position except thyroid cartilage removed. 2- arytenoid cartilage, 4·- corniculate cartilage, 6- cricoid cartilage, 8- cuneiform cartilage, 10- epiglottal cartilage, 14- 1st tracheal cartilage, 28- articular facet to thyroid cartilage.

the anterior lateral margins of the cricoid cartilage. Each has a well developed laterally projecting muscular process, but no vocal processes are evident. The arytenoid cartilages also articulate with the cuneiform cartilages.

The cuneiform cartilages (Figures 4,5,9,12,13,14,15.16,17,18, 19,20,22,23~24,25,26,and 27), form elongated blade-like processes Q

that face each other medially to lie in the trough formed by the epiglottal cartilage. As indicated above, the cuneiform cartilages articulate with the arytenoids. Two or more small cartilages, probably representing the corniculate cartilages, attach to the end of each cuneiform cartilage and also to the posterior two-fifths of the ventral edge of the arytenoid.

The arytenoid, the cuneiform, and the corniculate cartilages as described above have been referred to in various ways in the literature on cetacean larynges. Benham (1901) called the structure formed by these cartilages the arytenoid. D'Arcy-Thompson (1890) called the blade-like cartilages the super-arytenoids. Howes (1879)

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6 j * 4 , e •• Figure 6. Lateral (top) and ventral (bottom) views of the thyroid cartilage. 19- anterior notch, 20- posterior notch, 21- cranial cornu. 22- caudal cornu, 23- lamina.

was the first to call the blades the cuneiform cartilages. Howes was supported by Cleland (1884), Purves (J.967) , and Dormer (1974).

Extrinsic laryngeal muscles. All the extrinsic muscles are paired except for the hyoepiglottal muscle which is single. To simplify description only the muscles on the left side are described.

The hyoepiglottal muscle ( Figures 10,11,14,15,22,24,25,26, and 27) originates from the mid-dorsal basihyal segment of the hyoid bone, and inserts o~ the inferior one-half of the anterior edge of the epiglottal cartilage. This muscle probably functions to pull the epiglottal cartilage forward so as to enlarge the size of the anterior passageway in the laryngeal beak.

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R. F. GREEN ET AL.

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Figure 7. Left lateral (left) and dorsal (right) views of the cricoid cartilage. 23- lamina, 24- spine, 25- posterior dorsal cornu, 26-' posterior ventral cornu, 27- articular surface to arytenoid cartilage, 28- articular facet to thyroid cartilage.

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Figure 8. Lateral (left), anterior (middle), and posterior (right) views of the epiglottal cartilage. 29- lip, 30- trough.

ANATOMY OF THE BOTTLE NOSED DOLPHIN

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Figure 9. Ventral (top), lateral (middle), and dorsal (bottom) views of the arytenoid, cuneiform and corniculate cartilages.

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2- arytenoid cartilage, 4- corniculate cartilage, 8- cuneiform cartilage, 31- muscular process, 32- articular surface to cricoid cartilage.

The sternothyroid muscle (Figure 28) originates on the anterior margin of the sternum, and inserts on the lateral surface of the thyroid cartilage just superior to and anterior to the insertion 0:: the cricothyroid muscle. The sternothyroid probably functions to pull the complete laryngeal apparatus posteriad.

The EbYrohyoid muscle (Figure 28) originates on the lateral surface of the thyroid cartilage just anterior and ventral to the insertion of the sternohyoid muscle. Its insertion is at the posterior margin of the basihyal and thyrohyal segments of the hyoid bone. It probably functions to pull the laryngeal apparatus anteriad, thus more firmly lodging the tip of the laryngeal beak in the internal nares.

The larynx is suspended from the base of the cranium by a highly complex series of muscles, the thyropalatine, the occipito-


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Figure lO.Left lateral view of the larynx. 1- Cricoarytenoid-dorsal muscle, 5- cricothyroid-oblique muscle, 6- cricoid cartilage, 7- cricothyroid-straight muscle, 9- hyoepiglottal muscle, 11- interarytenoid muscle, 14- 1st tracheal cartilage.

thyroid and the thyropharyngeal. These muscles attach to the dorsal margin and anteromedial surface of the thyroid carti ,and then pass dorsad and anteriad to att,a,ch to the floor of the cranium. The most anterior of these muscles is the thyropalatine,( a posterior part of the palatopharyngeal muscle), which attaches to the medial surface of the thyroid lamina and the thyroid ligament. The middle muscle, the occipitothyroid, attaches to the dorsal margin of the cr.mial cornu of the thyroid cartilage. The most posterior muscle, the thyropharyngeal, attaches to the dorsal margin of the posterior cornu of the thyroid cartilage. The anterior fibers of the palatopharyngeal muscle together with the pterygopharyngeal muscle form the sphinct,er that partially fills the lower part of the internal nares and holds the laryngeal beak in place.

Intrinsic laryngeal Muscles. The cricothyroid muscle, (Figures 10,12,18,19,20,21,22, and 27) has its origin to the lateral posterior surface of the lateral cornu of the cricoid cartilage.Its insertion is to the thyroid cartilage along the inferior margin of the caudal cornu, to the posterior notch and to the lateral surface of the lanlina just below the posterior notch. This muscle has two distinct

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ANATOMY OF THE BOTTLENOSED DOLPHIN

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Figure 11. Lateral view of the larynx with thyroid cartilage and cricothyroid muscles removed. 1- cricoarytenoid-dorsal muscle, 3- cricoarytenoid- lateral muscle, 6- cricoid cartilage, 9-hyoepiglottal muscle, 11- interarytenoid muscle, 14- 1st tracheal cartilage, 15- thyroarytenoid muscle.

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parts in the dolphin, a dorsal oblique cricothyroid and a ventral straight cricothyroid.

The cricoarytenoid muscle, ( Figures 10,11,12,18,19,20,21,22, 24,25, and 26) has its origin over the dorsal surface of the cricoid cartilage extending laterad to the medial surface of the caudal cornu of the thyroid cartilage. The muscle is in two distinct parts, the dorsal cricoarytenoid and the lateral cricoarytenoid. Because of its attachment to the caudal cornu, Hosokawa (1950) ca1ls this muscle the ceratocricoarytenoideus. Both parts of the muscle insert on the dorsal muscular process of the arytenoid cartilage. They probably function to rotate the arytenoids lateral and posteriodorsad. This action increases inter-arytenoid space between the edges of the arytenoids and thus the inter-cuneiform space between the anterior edges of the cuneiform cartilages.

The thyroarytenoid muscle ( Figures 11,12,17,18,19,22,24,25, 26, and 27)lies on the medial surface of the thyroid cartilage and

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Figure 12. Dorsal view of laryngo~pharyngeal area showing location of transverse sections T3-Tll. XXX: indicates where the cricoid crest can be palpated.

has its origin on the dorsal midline and medial surfaces. The fibers pass dorsad to insert on the ventral surface of the muscular process of the arytenoid cartilage. The anterior fibers pass laterad, over the posterior angle of the epiglottal cartilage, but do not appear to attach to the epiglottis in such a way as to act upon it. The thyroarytenoid probably functions to pull the arytenoid and cuneiform cartilages ventrad and mesad to decrease the angle between their medial surfaces. If the arytenoid and cuneiform cartilages are already approximated the thyroarytenoid muscles probably function to pull the arytenoids and cuneiforms deeper into the epiglottal trough.

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Figure 13- Anterior section of section T3. 8- cuneiform cartilage, 9- hyoepig1otta1 muscle, 10- epiglottal cartilage.

Figure 14- Anterior surface of section T4. 8- cuneiform cartilage, 9- hyoepig1ottal muscle, 10- epiglottal cartilage.


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Figure 15. Anterior surface of section T5. 8- cuneiform cartilage, 9- hyoepiglottal muscle, 10- epiglottal cartilage, 11- thyroid cartilage.

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Figure 16- Anterior surface of section T6. 8- cuneiform cartilage, 9- epiglottal cartilage, 12- thyroid cartilage, 15- thyroarytenoid muscle, 17- thyrohyoid muscle.


Figure 17., Anterior surface of section T7. 2- arytenoid cartilage, 8- cuneiform cartilage, 10- epiglottal cartilage, 11- interarytenoid muscle, 12- thyroid cartilage, 15- thyroarytenoid muscle, 17- thyrohyoid muscle.

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Figure 18. Anterior surface of section T8. 1- cricoarytenoid- dorsal muscle, 2- arytenoid cartilage, 3- cricoarytenoid- lateral muscle, 5- cricothyroid- oblique muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 11- interarytenoid muscle, 12- thyroid cartilage, 15- thyroarytenoid muscle.


Figure 19. Anterior surface of section T9. 1- cricoarytenoiddorsal muscle, 2- arytenoid cartilage, 3- cricoarytenoid- lateral muscle, 4- corniculate cart , 5- cricothyroid-oblique muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 12- thyroid cartilage, 15- thyroarytenoid muscle.

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Figure 20. Anterior surface of section TlO. 1- cricoarytenoiddorsal muscle, 3- cricoarytenoid- lateral muscle, 4- corniculate cartilage, 5- cricothyroid-oblique muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 12- thyroid cartilage.

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ANATOMY OF THE BOTTLE NOSED DOLPHIN 217

Figure 21. Anterior surface of se'ction Tll. 1- cricoarytenoiddorsal muscle, 3- cricoarytenoid-' lateral musc Ie, 5- cricothyroidoblique mus.cle, 6- cricoid cartilage, 7- cricothyroid- straight muscle, 12- thyroid cartilage.

The interarytenoid muscle (Figures 10,11,12,17, and 18), joins the dorsal margins of the cuneiform and to a lesser degree the arytenoid cartilages. Some of the posterior fibers pass below and join into the anterior edge of the dorsal cricoarytenoid muscle. This muscle apparently functions to assist the cricoarytenoid muscles in increasing the interarytenoid and intercuneiform spaces.

EMG Studies On Laryngeal Muscles

Since none of the laryngeal muscles can be recorded by the use of surface electrodes because of the thick overlying blubber and subcutaneous muscle, electrodes must be inserted directly into the muscle to be studied. The bottlenosed dolphins available for these studies were young adults 125-150 kg in weight and 2.3-2.5 m in length. The measurements given below relate to animals in that size range.

There are two approaches that can be used to insert an electrode into the hyoepiglottal muscle. To begin the first approach ( A in Figure 29;:-palpate the posterior edge of the hyoid bone along the midline. The electrode is inserted about 2.0 cm behind the posterior edge of the hyoid bone and directed anteriorly at about 50-55° so as to pass between the hyoid and the epiglottal cartilage. The muscle is between 4.5 and 5.0 cms deep and has a transverse width of about 1.5 cm.


FRONTAL

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Figure 22- Left lateral view of the larynx indicating where transverse beak (TB) sections 1-7 and frontal (F) sections 8-11 were made.

The hyoepig10tta1 muscle can also be reached through the throat. The electrode would then be directed as illustrated at B in Figure 29, and the recording wires may be run out the subject's mouth.

To place an electrode into the sternothyroid muscle it was oriented using the baseline as illustrated in Figure 28, moving 3.5 cm to the left (animals left) of the midline to insert into the left sternothyroid muscle or 3.5 cm to the right of the midventral line to insert into the right sternothyroid muscle. The electrode should be inserted at 900 to the body surface and placed 4.5 cm deep (A-Figure 28).

The palata-pharyngeal muscle, the muscle that helps to hold the larynx in place, and may also serve to differentially close off the internal nares, can be recorded by inserting an electrode as illustrated at C, Figure 29.


Figure 23. Dorsal surfaces of TB (transverse beak) sections 1-7. 8- cuneifornl cartilage, 9- hyoepiglottal muscle, 10- epiglottal cartilage.

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Figure 24" Dorsal surface of section F8. 1- cricoarytenoid-dorsal muscle, 2-- arytenoid cartilage, 3- cricoarytenoid-lateral muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 9- hyoepiglottal muscle, 10- epiglottal cartilage, 15- thyroarytenoid muscle.

The electrode can be inserted into the cricothyroid muscle in much the same way as into the sternothyroid muscle, by using the line illustrated in Figure 28. Moving 2.5 cm lateral to the midventral line insertion can be made either to the left or right cricothyroid muscle. The electrode should be inserted at 900 to the body surface and placed 3.5-4 cm deep ( C- Figure 28).


Figure 25. Dorsal surface of section F9. 1- cricoarytenoid-dorsal muscle, 2- ,21rytenoid cartilage, 3- cricoarytenoid-lateral muscle, 6- cricoid .cartilage, 8- cuneiform cartilage, 9- hyoepiglottal muscle, 10- epiglottal cartilage, 12- thyroid cartilage, 14- 1st tracheal cartilage.

To insert the electrode into the thyrohyoid muscle the posterior hyoid is palpated on the midline. Then move posteriad 2-2.5 cm along the midline and then from 2-2.5 cm laterad. The electrode should be inserted at 900 to the body surface. The

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26. Dorsal surface of section FlO. 1- cricoarytenoid-dorsal muscle, 2- arytenoid carti ,3- cricoarytenoid-lateral muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 9- hyoepiglottal muscle, 10- epiglottal cartilage, 12- thyroid cartilage, 14- 1st tracheal cartilage, 15- thyroarytenoid muscle.

muscle is 3.5-4.0 cm deep and is backed up by the thyroid cartilage and the base of the epiglottal cartilage (B- Figure 28).

The !.hyropalatine, the muscles lie lateral to the

~~~~~~~~ and the thyropharyngeal can probably be


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Figure 27. Dorsal surface of section Fll. 4- corniculate cartilage, 5- cricothyroid-oblique muscle, 6- cricoid cartilage, 8- cuneiform cartilage, 9-· hyoepiglottal muscle, 10- epiglottal cartilage, 12- thyroid cartilage, 14- 1st tracheal cartilage, 15- thyroarytenoid muscle.

recorded by placing electrodes through the wall of the pharynx. If these muscles have an active role in sound production (other than suspending the larynx), we would speculate that they work together, therefore recordings from these muscles could be taken anywhere along the complete length of the larynx.


Figure 28. Ventral view of hyo-sternal area (the white line passes along the anterior edge of the flippers). 5- cricothyroid, 12- thyrc,id cartilage, 13- sternothyroid muscle, 17- thyrohyoid muscle, 18- panniculus carnosus muscle, 33- basihyal segment of hyoid bone, 34- thyrohyal segment of hyoid bone, 35-blubber, 36- thyroid gland. A- placement of sternothyroid muscle electrode, B- placement of thyrohyoid muscle electrode, C- placement of cricothyroid muscle electrode.

The cricoarytenoid muscles are located lateral and posterior to the cricoid crest and can be approached by palpating the anterior margin of the crest just posterior to the base of the laryngeal beak. Electrodes can be inserted into either the left or right cricoarytenoid .muscle 2 cm posterior to and 1 cm left or right of the crest. There is a sheet of esophageal muscle about 0.5 cm thick which passes between the pharyngeal wall and the cricoarytenoid muscle. The electrode must be inserted through this muscle layer to reach the cricoarytenoid.

The thyroarytenoid muscle is located approximately 2.3 cm lateral and ventral to the cricoid crest. The electrode should be

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Figure 29. Hid-sagittal section of a dolphin head. 50- blowhole, 51'- nasal plug, 52- melon, 55- premaxillary sacs, 65- nasal plug muscle, A- placement of hyoepiglottal muscle electrode, B- alternate placement of hyoepiglottal muscle electrode, C- placement of palatopharyngeal sphincter electrode, D- placement of interarytenoid muscle elecrode.

inserted at a point 2 cm posterior to the posterior edge of the epiglottal cartilage where the muscle is approximately 1 cm thick.

The interarytenoid muscle passes just anterior to the crieoid crest. The muscle extends approximately 1.5 cm to the left and 1.5 cm to the right of the midline and is approximately 2.0 wide from front tc back) and 1. 0 cm thick a long the mid line. The electrode is directed at an angle parallel to the dorsal edge of the cuneiform cartilages for insertion into this muscle (D-Figure29).

The Nasal System

The nasal system (Figure 3), includes the bony nasal passage; the spiracular cavity; and the plugs, sacs, membranes and muscles associated with the blowhole region, Due to their structure and location, the internal nares with their plugs, sacs, and membranes are considered to be the structures most likely involved in sound production. Lawrence and Schevill (1956), Mead(l972), Schenkkan (1973), and Dormer (1974) have given detailed descriptions and illustrations of the nasal region in the bottlenosed dolphin.


Oi~CMl!5 Figure 30. Left side of head showing the approximate location of the cross sections through the nasal region. The numbers lateral to the blowhole are section numbers referred to in the following figures.

We were interested in the anatomy of this area specifically for purposes of understanding dolphin sound production through ultrasonic scanning and EMG studies of function, therefore, we will present only a general description here.

The !)ony ~ passage passes upward through the skull in an anteriorly curved, almost vertical plane (Figure 29). Within the cranium the passage is separated by the bony and cartilagenous septum into two sub-oval tubes. The upper part of the passageway is a single chamber and is called the spiracular cavity (Von Baer, 1926), It passes upward a short distance to a single opening,

the blowhole. The blowhole is more or less round when open, but is "e" shaped when closed.

The nasal sacs.The nasal sacs are extensively developed in the bottlenosed dolphin. Four pairs of sacs communicate either directly or indirectly with the spiracular cavity. The premaxillary sacs (Figures 29, 33, and 34) are the largest and lie on top of the premaxillary bones just anterior to the openings into the bony nasal passage. They open into the spiracular cavity. The vestibular sacs (Figures 32-37) are located just below the skin, projecting posteriolaterad from the spiracular cavity into which they open.


The nasofronta1 sacs (Murie,1871) are "U" shaped tubular sacs that pass around the spiracular cavity below the vestibular sacs.

The accessory ~ (Schenkkan, 1971) project laterally from the inferior vestibules; passages that connect the posterior nasofrontal sacs to the posterior spiracular cavity.

The ~asal ~ (Lawrence and Schevill, 1956) protrude from the anterior spiracular wall just dorsal to the premaxillary sacs. They fit tightly against the posterior wall of the spiracular cavity to form a seal. The distal margins of the plugs form into. lips that fit into the openings between the inferior vestibules and the posterior spiracular cavity.

Nasal musculature. The several layers of muscles associated with the sacs, plugs, and lips are also complexly developed. Huber (1934) was of the opinion that the rostral muscles were derived from the pars labialis of the maxillonasolabialis muscle and the layers of muscle around the blowhole to be derived from the pars nasalis of the maxillonasolabialis. Lawrence and Schevill (1956) and Mead (1972) concur with Huber's interpretation of these origins. Mead, however, suggests the division should be made between medial and lateral. layers of muscle rather than between anterior and posterior muscles. This would result in the lateral, rostral, and superficial nasal muscles being derived from the pars labialis, and the medial rostral and deep nasal musculature being derived from the pars nasalis of the maxillonasolabialis muscle.

The posteroexternus (Figure 40) is the most superficial of the nasal sac muscles. Its origin extends along the posterior 1/2 of the supraorbital process of the maxilla bone, the temporal crest of the frontal bone, and nuchal crest (occipito-frontal suture). The muscle is generally quite thin and tendinous, with anterodorsad directed fibers passing over the vestibular sac to attach to the dense connective tissue in the posterior and lateral wall of the nasal passage. These anterior fibers are loosely attached over the dorsal surface of the vestibular sacs. The posterior fibers are directed anteriomediad to insert just above the anterior fibers.

This description of the posteroexternus is much the same as that given by Lawrence and Schevill (1956). It does not agree with Mead (1972), who describes the insertion of this muscle as being to the vertex .and contralateral muscle. Lawrence and Schevill also illustrate this muscle to show its origin over most of the nuchal crest thus completely covering the anteroexternus muscle below it. Mead, howev,er, illustrates the posteroexternus with its origin over the lower nuchal crest, with anteroexternus muscle exposed posteriorly. We have found the muscle to be as illustrated by Lawrence and Schevill about 80 percent of the time. About 20 percent


of the specimens that we dissected conform to Mead's description. On occasion one side of the specimen will appear as described by Mead while the other side will be structured like that described by Lawrence and Schevill.

This muscle probably functions to pull back on the posterior. wall and laterad on the lateral wall of the spiracular cavity. It could also function as a compressor of underlying structures and to restrict vertical expansion of the vestibular sac, as suggested by Mead (1972). Such a compressor function could also help in the conservation of water and heat that would ordinarily be lost with expired air <Coulombe ~ ~., 1965).

The intermedius muscle originates under the posteroexternus along th~ posterior 1/2 of the supraorbital process as well as from the fascia over the anteroexternus and posteroexternus muscles. It is more easily identified at its insertion end where the fibers pass loosely into the dense connective tissue mass dorsal to the nasal plugs. Mead (1972) also found the more dorsal fibers to be associated with the anterior dorsal surface of the vestibular sac This we found to be true in about 50 percent of the animals we dissected. It is also the case on one side of the head, but not on the other. This muscle is sometimes missing from both sides of the head. This muscle possibly functions to pull the nasal plugs down against the internal nares, but does not seem to be of great importance, as indicated by the generally weak insertion and variability.

The anteroexternus muscle (Figures 32 and 33) is a wide expansive muscle which takes its origin from the anterior supraorbital process posterior to the temporal and nuchal crests. The anterior margin of the muscle folds back over itself giving the appearance of a sepHrate muscle. The posterior dorsal margin occupies the angle between the anterior nuchal crest and the lateral margin of the vertex. The anterior fibers insert into the dense connective tissue beneath the anterior lip of the blowhole and into the lateral anterior wall of the spiracular cavity. The posterior fibers insert on the posterior and lateral wall of the· spiracular cavity as well as on the dorsal edge of the blowhole ligament. This muscle passes both below and above the vestibular sac, completely surrounding it.

Anteriorly, the anteroexternus is difficult to separate from the anterointernus muscle. The anterior fibers lie just posterior to the posterior extension of the lateral rostral muscle. Posteriorly, the muscle can be separated more easily from the posterointernus muscle, as the fibers run in different directions.

This description of the anteroexternus muscle is much like the description of the same muscle as redefined by Mead. Lawrence and Schevill refer only to the anterior fibers as the anteroexternus.

,----'----!'--rl--------------------------------I i I

ANATOMY OF THE BOTTLENOSEO DOLPHIN 229

We found these anterior fibers to be distinctly separate in a few instances, but in most cases the anterior and posterior parts were not separable.

The anterior fibers of the muscle probably function to pull down on the nasal plug causing it to seal over the internal nares. These anterior fibers may, as suggested by Lawrence and Schevill, draw the vestibular sac forward and laterad. The posterior part of the muscle, as described by Mead, probably functions to draw the posterior lip backwards, qpening the blowhole. Since the vestibular sacs are completely surrounded by this muscle it very likely functions to maintain the size and position of these sacs as well as compressing the sacs.

The posteriorinternus muscle (Figure 40) lies deep to the posterior three-quarters of the anteroexternus muscle as defined by Mead. Its origin is to the frontal bone, above the eye; to the dorsal medial margin of the supraorbital process, then dorsad to lie in the angle between the nuchal crest and the vertex. Its fibers pass anteriad and dorsad under the vestibular sacs to insert on the posterior and lateral wall of the nasal passage as well as to the lateral margins of the nasofrontal sacs. As Mead suggests, this muscle probably functions to pull the posterior wall forward, putting pressure on the blowhole ligament that in turn puts pressure on the lips of the nasal plugs causing the plugs to more effectively close the external bony passages.

The anterointernus muscle (Figures 32, 33, 35) is the deepest and most massive of the nasal muscles. The anterior part .of this muscle as described by Mead includes what Lawrence and Schevill called the profundus muscle. In our dissections, we most often found the two parts of the muscle to be closely joined even though there was occasionally a distinct boundry between them. Anteriorly the fibers insert to the connective tissue mass anterior to the spiracular cavity and over the nasal plugs. The median and posterior fibers insert into the lateral wall of the nasal passage and to the nasofrontal sac.

This muscle is probably the most powerful of the nasal muscles and must therefore playa significant: role in the function of the blowhole region. By drawing the anterior wall of the spiracular sac posteriad and by compressing the nasal plug mass it would playa significant role in closing the nasal passage. Purves (1967) suggested that the contraction of this muscle would compress the premaxillary sacs and function in the recycling of air.

The rostra:L muscle (Figure 31) consists of an elongated mass located on the fateral margins of the rostrum. Its or~g~n is from the dorsal surfa.ce of the maxilla. The muscle is divisible into

'----~------------~I------------------"------------------r_--------------! i ! \

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lateral and medial parts with the lateral fibers inserting into the lip and connective tissue lateral to the melon. The medial fibers project dorsally and medially to insert into the melon and lateral margin of the nasal plug. The medial fibers probably function to alter the shape of the melon and may function in sound production by action on the nasal plug. The muscle may also function in concert with sound production if the various theories of acoustic beam forming by the dolphin melon are correct (Wood, 1964).

The ~ is an elongated mass of fibers having their origin on the premaxillary bones anterior to the premaxillary sacs. The fibers insert into the dense connective tissue and fat of the nasal plugs. There appear to be more muscle fibers in the right side than in the left side of this muscle. This is probably due in part to the fact that the right plug is as much as 2 to 2-1/2 times as large as the left plug. This muscle most likely functions to pull the nasal plugs forward and may be involved in sound production.

The intrinsic muscles of the nasofrontal sacs almost completely surround the nasofronta1 sacs. The muscles originate from the dense connective tissue on the anterior wall of the vertex. Some fibers pass laterad below the lateral arc of the nasofrontal sacs to merge with the nasal plug muscle. Other fibers are associated with the inferior vestibule passages. There are an almost unlimited number of actions these fibers might have upon the sacs and passages they are associated with.

Mead (1972) has described the diagonal membrane muscle, originating on the anterolateral vertex deep to the intrinsic muscle and inserting in the attached margin of the diagonal membrane. Mead prefaced his description by stating that due to the complexity of this this region the muscle has escaped the attention of earlier workers. We have been very careful in searching for this muscle during our last 4 dissections of the Tursiops nasal region. We have been successful in locating fibers which fit Meads description but the muscle is very diffuse and not well developed.

EMG studies on nasal musculature. To place electrodes in the various layers of -nasal musculature the sagittal section illustrated in Figure 29, and the cross sections illustrated in Figures 31-39 can be scaled up to fit an individual experimental animal. This is most easily done by measuring the width of the animal's head at the posterior canthus of the eyes. Measurements can then be taken directly from adjusted illustrations so as to know where and how deep to place the electrodes. The anterior surface of section 13 is used as a baseline since it can be easily referenced from external landmarks.

Through dissection and morphometric evaluation we have determined external landmarks and stereotaxic coordinates necessary for

--l


Figure 31. Anterior surface of section 19; 6 cm anterior to baseline (section 13). 52- melon, 66- lateral rostral muscle, 67- medial rostral muscle.

Figure 32. Anterior surface of section 16; 3 cm anterior to baseline (section 13). 54- pterygoid sinus, 65- nasal plug muscle, 70- medial roe;tral muscle, 74- anterior externus muscle.

231


Figure 33. Anterior surface of section 15; 2 em anterior to baseline (section 13). 52- melon, 57- premaxillary sac, 70- anterior externus muscle, 74- anterior internus muscle.

Figure 34. Anterior surface of section 14; 1 em anterior to baseline (section 13). 49- nasal passage, 55- mandible, 56- eye, 57- premaxillary sac, 61- vestibular sac, 75- palata-pharyngeal sphincter.

..

ANATOMY OF THE BOTTLE NOSED DOLPHIN 233

Figure 35. Anterior surface of baseline (section 13). This section passes 1/2 cm anterior to the back of the blowhole and 1/2 cm anterior to the posterior canthus of the eyes. 49- nasal passage, 50- blowhole, 51- nasal plug, 58·- nasofrontal sac, 61- vestibular sac, 70- anterior externus muscle, 71- posterior externus muscle, 74- anterior internus muscle .

Figure 36- Posterior surface of section 13. This surface is 1 cm posterior to the anterior surface of section 13. 48- cranial cavity, 49- nasal passage, 51- nasal plug, 61- vestibular sac.

I


75

Figure 37. Anterior surface of section 12; 1 cm posterior to baseline (section 13). 48- cranial cavity, 51- nasal plug, 61- vestibular sac, 75- palato-pharyngeal sphincter.

Figure 38. posterior surface of section 12; 2 cm posterior to the anterior surface of baseline (section 13). 48- cranial cavity, 51- nasal plug, 58- nasofrontal sac, 62-diagonal membrane.

----I-I . i

\


Figure 39. Anterior surface of section 11' 2 cm posterior to baseline (section 13). 48- cranial cavity:

:----71

73

Figure 40. Anterior surface of section 10; 3 cm posterior to baseline (section 13). 48- cranial cavity, 61- vestibular sac, 71- posterior externus muscle, 73- posterior internus muscle.

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235


electrodes in muscles suspected to be involved in sound production (see Ridgway, et al., this volume).

ACKNOWLEDGMENTS

We thank Dr. A. S. Gaunt for his many helpful suggestions and encouragement.

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Functional and descriptive anatomy of the bottlenosed dolphin nasolaryngeal system with special reference to the musculature associated with sound production