Gross and histological structure of the pharyngeal constrictors in the rabbit.код для вставкиСкачать
Gross and Histological Structure of the Pharyngeal Constrictors in the Rabbit C. R. DUTTA AND J. V. BASMAJIAN Department of Anatomy, Queen's University, Kingston, Ontario, Canada In a continuing study of the functional anatomy and electromyography of the pharynx, rabbits were chosen as subjects because there is a basic similarity of pharyngeal anatomy in various mammalian forms and because of the great convenience of experimenting with this species. However, it soon became apparent that no detailed information is available on the special anatomy of the pharynx in the rabbit and even the description given by Bensley and Craigie ('48) is not sufficient and complete. This resulted in the present study of the gross and histological structure of the pharyngeal constrictors of the rabbit without which further functional studies would have been hampered. Because our study revealed important facts which may be of general use, the essential findings are being reported in this paper. MATERIAL AND METHODS Ten adult rabbits each weighing about 3 kg were killed by intravenous chloroform and embalmed via the abdominal aorta. The preserving fluid contained antiseptics (carbolic acid and dettol), hardening fluids (alcohol and formalin), hygroscopic agents (glycerine and potassium acetate) and salts. Twenty-four hours after embalming, red latex was injected under pressure into the aorta to facilitate the detection of the arteries during dissection. Steps in dissection With the subject supine, neck extended and fore-limbs widely abducted and drawn downwards, a median vertical incision was made in the front of the neck and another horizontal incision was made along the lower border of the mandible up to the mastoid process on each side. The resulting pair of triangular skin flaps were turned backward and laterally along with platysma and the two depressor conchae (anterior and posterior) and the external jugular vein on each side (fig. 1). A very thin layer of deep fascia was removed to expose the deeper structures in the anterior triangle of the neck and the sternocleido-mastoid was retracted on each side. The submaxillary salivary gland was removed on the left side and retracted on the right side. The digastricus, made up of a single belly in the rabbit, was found on the medial aspect of medial pterygoid. A portion of digastricus was removed on one side to expose the superior and middle constrictors, the styloglossus, and the stylohyoideus minor. The mylohyoid muscles were seen between the two digastrici forming the floor of the mouth. The infrahyoid muscles, such as sternohyoid and sternothyroid, were removed from one side to expose the origin of the inferior constrictor, cricothyroid and thyrohyoid muscles, thyroid and cricoid cartilages, thyroid gland and trachea. One lobe of the thyroid gland was removed from one side to expose the contents of the carotid sheath, the ansa hypoglossi and the upper deep cervical lymph nodes; then the nodes were removed completely to expose the sympathetic trunk. The hypoglossal nerve was seen passing across the hyoglossus muscle. Both nerve and muscle were removed to expose the lingual artery on the surface of the middle constrictor. The stylohyoideus major muscle was cut away from the tip of the greater horn of the hyoid bone and retracted towards its origin (jugular process of the occipital bone) to expose the stylopharyngeus muscle with the glossopharyngeal nerve (figs. 1, 2). To expose the direction and insertion of the three constrictor muscles on the back of 127 128 C. R. DUTTA AND J. V. BASMAJIAN Fig. 1 Ventral view of dissection. Inset shows enlargement of contents of carotid sheath. the pharynx, a coronal section was made just behind the pharynx (fig. 2). Another median sagittal section of the pharynx was made to expose both the interior of the pharynx and the origin and direction of the inner longitudinal muscle coat of the pharynx (fig. 3). Histological studies In three rabbits, the total number of muscle fibers in each constrictor muscle was counted by teasing the fibers apart under a dissecting microscope ( X 40) and then counting them under a binocular phase contrast microscope ( X 100). The breadth of the muscle fibers were measured with the help of the stage and ocular micrometer. To determine the number of muscle fibers innervated by a single motor neuron, fresh specimens of constrictor muscles were taken from three rabbits and fixed in 5% formosaline for 24 hours. Then they were teased apart under the dissecting microscope. The teased specimens were immersed in 0.1% methylene blue for two minutes thus staining the nerve fibers and their endings. OBSERVATIONS The muscular coat of the pharynx is covered outside by loose areolar fascia and lined inside by a thick pharyngeal aponeurosis attached to the base of the skull and pterygoid process. The muscular coat comprises 6 paired voluntary striated muscles (though their function is essentially involuntary). The outer circular coat comprises three paired constrictors, namely, superior, middle and inferior. The inner longitudinal coat also comprises three paired muscles, namely, salpingo-, palato-, and stylo-pharyngeus (figs. 2, 3). The three constrictors are incomplete in front where the nose, mouth and larynx open into the pharynx. Superior constrictor As in the human being, superior constrictor is a fan shaped muscle with a narrow origin and a broad insertion (figs. 1, 2, 3). 129 PHARYNGEAL CONSTRICTORS O F RABBIT hetic trunk n. IX ntetnal carotid A. Corn. carotid A. Corn. carotid Sterno-thyroid m. Fig. 2 Dorsal view of dissection of pharyngeal constrictors and related muscles. Ha . UL Salpinqo-pharynqeus IE\\ PalaTophar ynqeus ‘“‘F S u p e r i o r constrictor Middle constr ickor - Inferior constrictor , Genioqlossus Geniohuoideus ’ :- - - 1 M ylohy 01deus Hyoid bone Palatine t o n s t l Fig. 3 \\’ Median sagittal section and dissection from interior of pharynx. Origin. It arises: ( a ) from the base of the external acoustic meatus by a thin band, ( b ) from the pterygoid hamulus and adjacent part of the posterior border of the medial pterygoid plate (pterygo-pharyngeus), (c) from the soft palate along with palato-pharyngeus, and ( d ) from the side of the tongue. Course and insertion. The upper fibers run dorsally, upward, and medially to be inserted into the pharyngeal tubercle of the occipital bone. The middle fibers run horizontally to be inserted into the pharyngeal raphe. The lower fibers run downward, backward and medially also to be inserted into the pharyngeal raphe. These 130 C , R. DUTTA AND J. fibers are overlapped by the middle constrictor. Middle constrictor (hyo-pharyngeus) It is also a fan shaped muscle with a narrow origin but broad insertion. Origin. It arises deep to hyoglossus from the greater and lesser horns of the hyoid bone and the angle between them. Course and insertion. All the fibers are inserted into the pharyngeal raphe. The upper fibers run obliquely upward, backward and medially; the middle fibers run horizontally; and the lower fibers run obliquely downward, backward and medidly to be inserted into pharyngeal raphe. The lower fibers are overlapped by the upper fibers of inferior constrictor. Inferior constrictor Unlike the human inferior constrictor, it is a quadrangular shaped muscle with a vertical height of 6-7 mm, a breadth of 7-8 mm, and a thickness (at its central part) of 1-2 mm. Origin. It arises : ( a ) from the oblique line of the thyroid cartilage behind the attachments of sternothyroid and thyrohyoid muscles (this part of the muscle being called thyro-pharyngeus) and (b) from the lateral aspect of the cricoid cartilage and fibrous arch covering the cricothyroideus (this part being known as crico-pharyngeus). Course and insertion. All the fibers run parallel with each other obliquely upward, backward, and medially to be inserted into the pharyngeal raphe. The lowest fibers blend with the longitudinal fibers of the esophagus. Relationships of constrictors Superior constrictor. The relations are : ( a ) dorsally-prevertebral fascia and muscles, and the pharyngeal venous plexus : ( b ) laterally-stylo-pharyngeus, medial pterygoid and middle constrictor muscles, glossopharyngeal and lingual nerves, symphatic trunk and carotid sheath; ( c ) internally-palato- and salpingo-pharyngeus, pharyngeal aponeurosis and tonsil; ( d ) superiorly-the sinus of Morgagni which is traversed by levator palati muscle and V. BASMAJIAN auditory (Eustachian) tube; (e) inferiorly (i.e., between superior and middle constrictors)-stylo-pharyngeus muscle and glossopharyngeal nerve. Middle constrictor. Its relations are : ( a ) dorsally-prevertebral fascia and muscles; (b) laterally-carotid sheath, pharyngeal plexus of nerves, covered near its origin by hyoglossus (separated by lingual artery) and covered at its lower part by inferior constrictor; (c) internally-superior constrictor, stylo- and palato-pharyngeus muscles and pharyngeal aponeurosis. Between the middle and inferior constrictor muscles no structure pierces the thyrohyoid membrane. Inferior constrictor. Its relations are : ( a ) dorsally- same as middle constrictor; (b) laterally-thyroid gland, carotid sheath, sternothyroid muscle and superior laryngeal vessels and nerve which pierce the muscle and thyroid cartilage on their lateral surface to enter the larynx; (c) internally-middle constrictor, stylo-pharyngeus muscle and fibrous coat; (d) inferiorly-the recurrent laryngeal nerve and the inferior laryngeal branch of the superior thyroid artery entering the larynx deep to it. Nerzie supply of constrictors The pharyngeal constrictors are supplied chiefly by the pharyngeal branch of the vagus through the pharyngeal plexus. The latter is formed on the surface of the middle constrictor by the pharyngeal branches of the vagus and glossopharyngeal nerves and the sympathetic trunk. From this plexus three main trunks arise and each trunk runs diagonally across the middle of individual constrictor muscles accompanied by a vessel (fig. 4). Fig. 4 Drawing of a nerve bundle ending on muscle fibers and accompanied by a vessel, as seen under low power phase contrast. 131 PHARYNGEAL CONSTRICTORS OF RABBIT TABLE 1 Histological characteristics of constrictor muscles in three rabbits Sup. constrictor Middle constrictor Inf. constrictor Length of muscle fibers 5-6 mm 6-7 mm 7-8 mm Breadth of muscle fibers 15-20 /A 15-20 /A 20-30 /A Arrangement of fibers Arranged in a complicated interlacing manner Arranged in a Arranged in a single sheet at single sheet at its upper and its edges but 3 4 lower edge but layers at its cenat its center tralpart. They they are arare all parallel with each other. ranged in 2-3 layers. The fibers There is considare almost parerable amount of allel with each fat between the other muscle fibers Color of muscle Pale Pale Red TABLE 2 Number of muscle fibers (by actual count) i n constrictor muscles of three rabbits Rabbit no. 1 2 3 Average Superior constrictor Middle constnctor 2860 4564 2212 3212 4332 4773 2550 3885 Histological findings The characteristics of the muscle fibers in three rabbits are summarized in table 1. It should also be noted that all the muscle fibers show good cross-striations. The total number of muscle fibers in these three rabbits are shown in table 2. T h e size of motor units. In the stained and teased tissue seen under the phasecontrast microscope, nerve trunks are accompanied by a vessel and cross the middles of the muscle fibers. As each crosses its muscle, it gives off branches to a series of fibers alternately on one side and then the other (fig. 4). Each branch ends on an end-plate that is situated near the middle of each muscle fiber. Under higher magnification ( X 500) with phase-contrast, individual nerve fibers are seen to innervate 4-6 muscle fibers in the inferior constrictor (fig. 5) and 2-4 muscle fibers in the middle and superior constrictors. Total number of motor units. This was calculated by dividing the number of muscle fibers by the average size of the motor Inferior constrictor 4491 6502 4312 5102 Nerve Fig. 5 Drawing of photograph showing the ending of nerve fibers on muscle fibers ( X ca. 500). unit. In this short series, the figure for the superior constrictor is about 1071, for middle constrictor, 1295, and for inferior constrictor, 1021. In other words, there are over 1000 motor units in each pharyngeal constrictor. 132 C . R. DUTTA AND J. V. BASMAJIAN DISCUSSION The above findings confirm that there is a marked basic similarity in the gross structure of the constrictor muscles of the pharynx in man and rabbit. This basic similarity is not surprising and is related to the following factors: ( a ) swallowing and respiration are the primitive functions of the pharynx in both man and rabbit and there is no essential differences in these functions in the two species; and (b) in both species the pharynx develops from the cephalic end of the foregut in about the same way. Possibly related to man's higher evolution or to his erect posture, there are a few noteworthy differences. In man, superior constrictor muscle extends its origin down to the mandible. This seems to be due to its important function of closing the nasopharynx during speech. The lower fibers of the inferior constrictor in man run horizontally to form the crico-esophageal sphincter. This muscle, according to Negus ('49) remains tonically contracted during ordinary respiration to prevent the entrance of air into the esophagus as a result of the inspiratory descent of the diaphragm and expansion of the thorax. This sphincter opens with closure of the larynx during swallowing by virtue of the attachment of the anterior wall of the esophagus to the back of the cricoid cartilage. In this study a direct count of the muscle fibers was made after teasing them apart under a dissecting microscope. There was a considerable range of results as shown in table 2. Nonetheless, averages of about 3200, 3900 and 5100 fibers for superior, middle and inferior constrictors, respectively, may be quite useful, especially since they were obtained by direct counting. Other observers, however, have made their counts (or rather, estimates) from cross sections of stained specimens. For example, van Harreveld ('47) estimated that there are 6282 fibers in the sartorius of the rabbit. Berlendis and De Caro ('55) gave 3600 fibers for the rabbit's stapedius and 4100 for tensor tympani. The motor end-plates are found to be located near the middles of the muscle fibers. This was also shown by Coers and Woolf ('59) in human skeletal muscle, by Gurkow and Bast ('58) in trapezius and sterno-mastoid of the hamster, and by Jarcho et al. ('52) in the gracilis of the rat. The size of the motor units in our study was determined by tracing the individual nerve fibers along their final distribution to the muscle fibers. Other observers have calculated the total number of muscle fibers in a muscle and the total number of nerve fibers in its motor nerve. Then, by dividing the former by the latter figure, they have calculated the size of the motor units. The latter method is rather questionable because we know that the motor nerve of a muscle contains many sensory and sympathetic fibers as well as motor fibers (fig. 6). Nonetheless, it is a method that does produce reasonable approximations. Tergast (1873) estimated that the motor units of the sheep extra-ocular muscles have 3-10 muscle fibers; Bors ('26) estimated 5-6 for human extra-ocular muscles. More particularly, Feinstein et al. ('55) reported 9 muscle fibers per motor unit in the human lateral rectus, 25 in platysma, 108 in the first lumbrical of the hand and 2000 in the medial head of gastrocnemius. Van Harreveld ('47) reported 100-125 muscle fibers per motor unit in the sartorius of the rabbit; Berlendis and De Car0 ('55), 27 in the stapedius and 30 in the tensor tympani of the rabbit; Wersdl ('581, 10 in the human tensor tympani; and Ruedi ('59), 2-3 muscle fibers per motor unit in the human laryngeal muscles. Generally it has been agreed that muscles controlling fine movements and adjustments (such as those attached to the ossicles of the ear and to the eyeball and the larynx) have the smallest number of muscle fibers per motor unit. This statement would now appear to include the pharyngeal constrictor muscles. On the other hand, large coarse-acting muscles, e.g., those in the limbs, have larger motor units. It will be noted that we have also calculated by a direct count of muscle fibers and a direct tracing of the terminal branches of motor nerve fibers the number of motor units in the pharyngeal constrictors. We find each contains just over 1000 motor units. By the less precise but still useful technique of estimation generally 133 PHARYNGEAL CONSTRICTORS OF RABBIT Aui'onomic Neruous 2 Sqs ?em - iVasodilator AC c \wMuscle I I I I I I fibre (Intrafusa21 SheZeta2 MuscZe I (tendons) CNS.3 ' 9 Sensory Nerve I I I I I I I I Pacinian I <@ Corpuscle ? I 9 Sensory Nerve Fig. 6 I I I I I [ ? I 1 1 I I (fascia) Naked Nerve Endings. (muscZe substanm / Scheme showing multiple innervation of skeletal muscIe (after Solandt, '42). employed, Feinstein et al. ('55) reported 3000 units in the human lateral rectus, and Berlendis and De Car0 ('55) reported 100-120 motor units in the stapedius and 125-190 motor units in the tensor tympani of the rabbit. It would appear to us that the total number of motor units has no intrinsic value in that this is simply a function of the size of the muscle and the size of the motor units in it. Strength of contraction is eventually dependent on the number of muscle fibers in an individual muscle and not on the number of motor units. Fine control, however, is dependent on the smallness of the motor units within the muscle. SUMMARY A study of the pharyngeal anatomy (gross and histological) was carried out in 10 adult rabbits. The gross structure of the constrictor muscles varies from that in the human being, especially in the superior and inferior constrictor. In three rabbits the muscle fibers were counted after teasing them apart and the nerve fibers were traced. The motor units in the inferior constrictor contain 4 to 6 muscle fibers each; those in the middle and superior constrictors contain two to 4 each. The smallness of the motor units in the pharyngeal constrictors places these muscles in the group of muscles that can produce very fine or delicate movements. In this short series, the average total number of muscle fibers were: for inferior constrictor, about 5100; for middle constrictor, about 3900; for superior constrictor, about 3200. 134 C . R. DUTTA AND J. V. BASMAJIAN LITERATURE CITED Berlendis, P. A,, and L. G. De Car0 1955 L’unitB motoria del muscolo stapedio. Boll. SOC.Med.-chir. Pavia, 69: 33-36. Bors, E. 1926 Ueber das Zahlenverhaltnis zwischen Nerven- und Muskelfasern. Anat. Anz., 60: 415416. Coers, C., and A. L. Woolf 1959 The Innervation of Muscle, a Biopsy Study. Charles C Thomas, Springfield, Ill. Craigie, E. H. 1948 B.ensIey’s Practical Anatomy of the Rabbit, ed. 8. University of Toronto Press, Toronto. Feinstein, B., B. Lindeghd, E. Nyman and G. Wohlfart 1955 Morphological studies of motor units in normal human muscles. Acta Anat., 23: 127-142. Gurkow, H. J., and T. H. Bast 1958 Innervation of striated skeletal muscle. Am. J. Phys. Med., 37: 269-277. Jarcho, L. W., C. Eyzaguirre, B. Bennan and J. L. Lilienthal 1952 Spread of excitation i n skeletal muscle: some factors contributing to the form of the electromyogram. Am. J. Physiol., 168: 44-57. Negus, V. E. 1949 The Comparative Anatomy and Physiology of the Larynx. William Heinemann, Ltd., London. Riiedi, L. 1959 Some observations on the histology and function of the larynx. Semon lecture, 1958, J. Laryngol. Otol., 73: 1-20. Solandt, D. Y. 1942 Atrophy in skeletal muscle. J. Am. Med. Assoc., 120: 511-513. Tergast, P. 1873 Ueber das Verhaltnis von Nerve und Muskel. Arch. Mikr. Anat., 9: 36-46. van Harreveld, A. 1947 On the force and size of the motor units in the rabbit’s sartorius muscle, Am. J. Physiol., 151: 96-106. Wersall, R. 1958 The tympanic muscles and their reflexes, Acta Oto-laryngologica, Supplementum 139.