A comparative morphologic study of the cardiac innervation in domestic animals II. The felineкод для вставкиСкачать
A Comparative Morphologic Study of the Cardiac Innervation in Domestic Animals 11. THE FELINE JOHN SCOTT McKIBBEN AND ROBERT GETTY Department of Veterinary Anatomy, Iowa State University, A m e s , Iozua ABSTRACT Detailed morphological studies of the cardiac innervation of the cat were reported. Sympathetic cardiac nerves arose from the thoracic, cervicothoracic, vertebral, and intermediate ganglia. Parasympathetic cardiac nerves arose from the vagi, both cranial and caudal to the origin of the recurrent laryngeal nerves, and from the right recurrent laryngeal nerve. Left cardiac nerves passed primarily to the caudal and right surfaces of the left chambers while right ones ramified on the right chambers and left portion of the left chambers. Left cardiac nerves are more prominent around the coronary sinus and atrioventricular node, while right ones contribute more to the area of the sinoatrial node. Both sympathetic and parasympathetic nerves were followed to each chamber. Interconnections through the cardiac plexus facilitated overlapping of nerve distributions. The cat, although having an early history as an animal for various laboratory investigations, has not enjoyed the attention of cardiologists which the dog has received. Anatomical descriptions of the cardiac innervation are limited. Bernhardt (1868), Boehm (1875), and Kazem Beck (1888) described the depressor nerve and its relationship to the heart. Mannu ('14) reported on the cardiac nerves of one cat. Perman ('24), Nonidez ('39), and Saccomanno ('43) contributed further information regarding the cardiac innervation of the cat. Only Anufriew ('28), however, has morphologically described the innervation of the feline heart in detail. Current veterinary anatomical textbooks do not include the morphological description of these cardiac nerves in the cat. The present investigation includes further morphological observations relevant to the proper understanding of cardiac function as well as for specialized procedures such as cardiac denervation studies. MATERIAL AND METHODS Ten adult cats were embalmed using the Iowa State University, Department of Veterinary Anatomy embalming formula. Direct morphologic dissection proceeded, exposing and tracing the cardiac nerves, as previously described (McKibben and Getty, '68). AM. J. ANAT., 122: 5 4 5 5 5 4 , RESULTS A. Thoracic ganglia and cardiac nerves Independent THORACIC GANGLIA were present along the thoracic sympathetic trunks bilaterally in each intercostal space from the third or fourth space caudally. They maintained a fairly uniform size of 2 mm craniocaudal, 1 mm dorsoventral, and 1 mm mediolateral. LEFT thoracic cardiac nerves arose from the third to fifth thoracic ganglia, joined the dorsal cervicothoracic cardiac nerve and entered the cardiac plexus. RIGHTthoracic cardiac nerves passing directly to the heart were not observed grossly; however, nerves arising from the third and fourth thoracic ganglia joined the right vagus nerve and potentially could reach the right atrium with the right caudal vagal cardiac nerves. B . Cervicothoracic ganglia and cardiac nerves On each side the CAUDAL CERVICAL and first two or three THORACIC GANGLIA combined to form the CERVICOTHORACIC GANGLION.This ganglion lies on the lateral surface of the longus colli muscle in the first intercostal space on the right side, and extends between the first and second intercostal spaces on the left side. Rami communicantes extend caudally at least to the third thoracic spinal nerve and cranially 545 Feline Approximate feline Left number weight 8 8 7 8 9 10 2 4 4 9 7 8 Average8 8 5 7 4 4 4 4 5 5 4 5 4 D-V 8 6 7 7 6 8 7 9 6 6 C-C 2 3 1 1 1 1 2 unidentified 4 3 2 3 1 1 Grossly Grossly unidentified Grossly unidentified unidentified unidentified Grossly Grossly unidentified Grossly unidentified Grossly Grossly unidentified Grossly Grossly unidentifies Grossly unidentified unidentified 0.50.50.5 Grossly unidentified unidentified Grossly Grossly Grossly unidentified n4-I. unidentified unidentified 1 Grossly C-Ti Unidentified M-L C-C unidentified 0.50.50.5 Grossly D-V Intermcdiate ganglion Riglit Grossly Grossly 1 1 1 1 1 1 1 1 2 1 1 1 M-L C-C Left unidentified 6 3 4 2 2 3 1 1 D-V Right Ansa subclavia 1 Left Right length length 10 10 15 12 15 5 8 8 7 10 10 19 25 30 18 20 15 15 12 10 20 23 17 13 20 30 13 20 13 15 10 20 20 28 23 35 45 20 30 20 25 20 30 30 ~- Cranial Caudal CranGal Caudal limb limb limb limb The width of th& cradial limbs aver'aged hne half millimeter: usually double caudal limbs averaged, together, 1 mm in width. 1 1 1 1 1 unidentified 2 1 1 1 2 Grossly 2 1 1 1 1 4 4 4 3 3 1 3 unidentified 3 1 1 2 2 M-L C-C Vertebral ganglion Grossly I>-V Left 2 2 1 2 2 2 2 2 M-L C-C C-C Craniocaudal. D-V Dorsoventral. M-L Mediolateral. 2 2 5 7 8 2 2 4 4 2 2 2 2 2 2 M-L Cervicothoracic ganglion Right 7 7 8 8 6 4 4 5 3 10 8 4 5 4 8 8 3 7 4 4 8 2 6 D-V 6 8 1 pounds C-C in TABLE 1 Feline: dimensions o f the ansa subclavia an,d of t h e ganglia o j origin f o r cardiac nzrves in millimeters 221-1 2 M 2 9 *3 E3 m r-1 I-1 82 rn 8 cl +, Left Right Left Right Left Right Left Right Left Right Left Right Left Right Left Right Left Right Side - -t+, ++ + + + ++ + + ++ + + ++- right coronary artery 1 + ++++ + + + ++- - I- ++ ++ Along the descending and circumflex branches of the left coronary artery on the left bid? 2 +++, Along the circuinflex branch of the left coronary artery caudally and on the right sides Between the cranial and caudal venae cavae 4 Between the caudal vena cava and le€t atrium 6 - ++ + ++ ++++ + ++ ++ +++ ++- + Cardiac plexus 6 -, not followed to this area; some may supply this area; moderate supply to the area; major supply to the area. 1 Main distribution includes the right aupcle, atrium, “d ventncle. ZMain distribution includes the left auricle left ventricle on the left side left interventricular septum and the left cranial portion of the right ventricle. 3 Main distribution includes the dorsum of ’the left auricle, ventrum of tlk left atrium, caudal and right sides of the left ventricle, right interatrial and interventncular septa and caudal right surface of the right ventricle. 4Main distribution includes the lateral right atrial wall towards the sinoatrial node and sometimes the extension across the coronary groove into the right longitudinal, sulcus. 5Main distribuhon may include the left atrium, right atrium, right side of the left ventricle, interatrial and interventricular septa on the right side, and the right caudal portion of the right ventricle. 6Main distribution to the dorsal atrial walls, great vessels, and intermingling of incoming branches which may then pass with major branches to the other five areas. Recurrent cardiac nerves Caudal vagal cardiac nerves Cranial vagal cardiac nerves Cranial cervical cardiac nerves Middle cervical cardiac nerves Vertebral cardiac nerves Intermediate cardiac nerves Cervicothoracic cardiac nerves Thoracic cardiac nerves Nerves TABLE 2 Distribution of cardiac nerves in the Feline 548 JOHN SCOTT McKIBBEN AND ROBERT GETTY at least to the sixth, seventh, and eighth cervical spinal nerves, grossly. The ganglia bilaterally were approximately the same size (table 1). Typically two or three cardiac nerves arose from the caudal portion of the LEFT cervicothoracic ganglion. A caudodorsal cervicothoracic cardiac nerue passed caudally along the dorsolateral border of the left subclavian artery and near this vessel’s origin joined a left caudoventral cervicothoracic nerve. The LEFT caudoventral cervicothoracic cardiac nerves followed the caudal limb of the ansa subclavia, then the left vagus towards the heart. The combined nerves passed over the left lateral surface of the aorta and rantified near the caudal border of the aortic arch. Here left cranial vagal cardiac nerves and left vertebral cardiac nerves also joined them. Principal branches passed caudoventrally, lateral to the pulmonary artew, and continued between the left auricle and pulmonary veins to the caudal portion of the coronary groove. They continued along the course of the circumflex branch of the left coronary artery to the right side of the left ventricle and into the right longitudinal sulcus. Branches Abbreviations 1 2 3c 3d 3e 3f 3g 3h Ramus communicans Sympathetic trunk Third thoracic ganglion Fourth thoracic ganglion Fifth thoracic ganglion Sixth thoracic ganglion Seventh thoracic ganglion Eighth thoracic ganglion 3j Ninth thoracic ganglion 4 Cervicothoracic ganglion 5 Ansa subclavia (caudal limb) 5’ Ansa subclavia (cranial limb) 7 Intermediate ganglion 8 Vertebral ganglion 10 Cranial cervical ganglion 11 Vagus nerve 12 Right recurrent laryngeal nerve 12’ Left recurrent laryngeal nerve 13 Thoracic cardiac nerve 14’ Caudodorsal cervicothoracic cardiac nerve 14” Caudoventral cervicothoracic cardiac nerve 16 Vertebral nerve 17 Intermediate cardiac nerve 18’ Caudal vertebral cardiac nerve 20 Cranial cervical nerve 21 Cranial vagal cardiac nerve 21’ Caudal vagal cardiac nerve 22 Recurrent cardiac nerve 24a Eighth cervical spinal nerve 24b Seventh cervical spinal nerve 24c Sixth cervical spinal nerve 24d Fifth cervical spinal nerve 24e Fourth cervical spinal nerve 24f Third cervical spinal nerve 25a First thoracic spinal nerve 25b Second thoracic spinal nerve 25c Third thoracic spinal nerve 25d Fourth thoracic spinal nerve 25e Fifth thoracic spinal nerve 25f Sixth thoracic spinal nerve 25g Seventh thoracic spinal nerve 25h Eighth thoracic spinal nerve 25j Ninth thoracic spinal nerve 26 Vascular nerve 28 Cardiac plexus Inferior (nodose) ganglion of the vagus nerve Aa First rib Ab Second rib Ac Third rib Ad Fourth rib Ae Fifth rib Af Sixth rib Ag Seventh rib Ah Eighth rib Aj Ninth rib B Longus colli muscle C Esophagus D Intercostal artery D’ Intercostal vein E Aorta F Brachiocephalic artery G Left subclavian artery G Right subclavian artery H Costocervical artery I Transverse colli artery (dorsal artery) Supreme intercostal artery (subcostal artery) J K Vertebral artery L Deep cervical artery M’ Costocervico-vertebral vein N’ Left common carotid artery N Right common carotid artery 0 Right vena azygos P Cranial vena cava Q Caudal vena cava R Right atrium R‘ Right auricle S’ Left auricle T Right ventricle U Left ventricle W Trachea X Bronchus Y Pulmonary artery Y Pulmonary vein Z Lung AA Ligamentum arteriosum BB Right coronary artery B B Descending branch of left coronary artery BB” Circumflex branch of left coronary artery CC Great cardiac vein FF Middle cardiac vein 29 FELINE CARDIAC INNERVATION Fig. 1 Feline: Left lateral view of the cardiac nerves and related ganglia. Fig. 2 Feline: Right lateral view of the cardiac nerves and related ganglia. 549 550 JOHN SCOTT McKIBBEN AND ROBERT GETTY Fig. 3 Feline: Dorsal view of the cardiac innervation. The sympathetic trunks and vagi are reflected laterally. passed to the dorsum of the left auricle, ventrum of the left atrium, caudal and right walls of the left ventricle, interatrial and interventricular septa from the right, and the caudal right portion of the right ventricle. Other branches of the left caudoventral cervicothoracic cardiac nerves passed to the aorta, pulmonary artery, left pulmonary veins and into the cardiac plexus. Some twigs continued through the FELINE CARDIAC INNERVATION cardiac plexus and between the aorta and pulmonary artery to join the trunk of combined right cardiac nerves. Together these nerves followed the right and left coronary arteries from near their origins to their ramifications on the right ventricle, left cranial portion of the left ventricle, and the cranial and ventral portions of the right and left auricles. RIGHT ceruicothoracic cardiac nerves passed with the caudal limb of the ansa subclavia to its junction with the right vagus nerve just caudal to the subclavian artery. Here they joined right vertebral, recurrent, and caudal vagal cardiac nerves, passed caudally on the ventral surface of the trachea, continued between the cranial vena cava and aorta and entered the cardiac plexus. The main continuation through the plexus was followed around the caudal surface of the aorta to the left side of the heart. On the left side it proceeded cranially around either side of the pulmonary artery, then along the right and left coronary arteries. Branches along these arteries passed to the right ventricular wall, cranial left portions of the left ventricle, interventricular septum and the cranial and ventral portions of the right and left auricles. Other right cervicothoracic cardiac nerves arising from the caudal limb of the ansa subclavia passed caudally with the right vagus nerve to the area of the right apical bronchus. Here, together with caudal vagal cardiac nerves, they left the vagus and proceeded between the right branch of the pulmonary artery and the cranial vena cava to ramify on the dorsolateral surface of the right atrium. Their course onto the right atrium was between the venae cavae or between the caudal vena cava and left atrium. Twigs may extend to the area of the coronary sinus. Occasionally, independent right cervicothoracic cardiac nerves passed directly from the right cervicothoracic ganglion to the area of the right apical bronchus. Here they joined caudal vagal cardiac nerves and passed to the right atrium. Twigs from right cervicothoracic cardiac nerves also passed to the cardiac plexus, right pulmonary artery and veins, and cranial and caudal vena cava. C . Cervical ganglia and cardiac nerves An inconstant INTERMEDIATE GANGLION of variable size (table 1) was noted on the 551 more caudal of the paired left caudal limbs of the ansa subclavia in three cats. Intermediate cardiac nerves arising from this ganglion passed with the left caudoventral cervicothoracic cardiac nerves to the heart. No homologous ganglion or nerves were noted grossly on the RIGHT side. Each VERTEBRAL GANGLION was located at the cranial ends of each ansa subclavia, directly craniomedial to the vertebral artery, and just dorsal to the vagus nerve. Each was approximately the same size (table 1 ) . Two to four vertebral cardiac nerves arose from the LEFT vertebral ganglion, joined into one trunk after passing caudally for a few millimeters, and continued caudally in close apposition to the left vagus nerve. Near the caudal border of the aortic arch it joined the other left cardiac nerves and passed to areas along the circumflex branch of the left coronary artery on the caudal and right sides of the heart, as previously described. Nerves from the left vertebral ganglion may join a nerve from the cranial cervical ganglion, and continue between the brachiocephalic and left subclavian arteries to reach the aorta. RIGHT vertebral cardiac nerves, generally three or four in number, joined the other right cardiac nerves and passed with them to the heart, as previously described under the right cervicothoracic cardiac nerves. No independent MIDDLE CERVICAL GANGLION was noted grossly in the cat. The CRANIAL CERVICAL GANGLION lay in close apposition to the nodose ganglion ventromedial to the tympanic bulla. It measured approximately 8 mm craniocaudal, 3 mm dorsoventral, and 2 mm mediolateral. No cranial cervical cardiac nerves were noted; however, on the left side a completely separable nerve arising from the cranial cervical ganglion, left cranial laryngeal nerve, and left vagus accompanied the vagosympathetic trunk caudally. It passed ventral to the left subclavian artery and between the left subclavian artery and brachiocephalic trunk and ramified on the aorta. D. Vagal cardiac nerues In addition to the vagal fibers passing in the previously described nerve, LEFT cranial vagal cardiac nerves arose from the 552 JOHN SCOTT McKIBBEN AND ROBERT GETTY intimately interwoven association of the left vagus with the sympathetic nerves at the junction of the aorta, pulmonary artery, and left bronchus. These nerves followed the sympathetic nerves from this side into the cardiac plexus, to the aorta and pulmonary artery, to the caudal and right aspects of the left ventricle, ventrum of the left atrium, interventricular and interatrial septa, and caudal portion of the right ventricle. Twigs may indirectly reach the left longitudinal sulcus and cranial coronary groove along the coronary arteries. A RIGHT cranial vagal cardiac nerve passed with other right cardiac nerves as described previously for the right cervicothoracic cardiac nerves. Two or three caudal vagal cardiac nerues arose from the LEFT vagus nerve about 5 nun caudal to the origin of the left recurrent laryngeal nerve from the vagus and passed cranioventrally between the pulmonary veins and left auricle into the coronary groove. The left auricle received twigs as the nerves passed it. They also ramified along the circumflex branch of the left coronary artery onto the caudal and right surfaces of the left ventricle, ventrum of the left atrium, interatrial and interventricular septa, and caudal wall of the right ventricle. Fine twigs sometimes also passed to the cardiac plexus, the left longitudinal sulcus, and along the right coronary artery. From the intimate association of the right vagus with the right sympathetic nerves, as the caudal limb of the ansa subclavia approximates the vagus, RIGHT caudal vagal cardiac nerves combined with sympathetic and right recurrent cardiac nerves and passed caudoventrally, ventral to the trachea. Their distribution included the right ventricle, left and cranial portions of the left Ventricle, and the cranial and ventral portions of the auricles. Two or three additional caudal vagal cardiac nerves arose These accompanied the right cervicothoracic cardiac nerves to the dorsolateral portion of the right atrium, the cardiac plexus, right pulmonary vessels, venae cavae and sometimes extended into the coronary groove in the area of the coronary sinus. heart grossly. Some ramified, however, on the caudal border of the aorta. One or two fine RIGHT recurrent cardiac nerves joined the sympathetic and vagal cardiac nerve trunk which originated near the caudal limb of the ansa subclavia. They passed together, as previously described, to the right ventricle, left caudal portion of the left ventricle, and the cranial and ventral portions of the auricles. DISCUSSION In the present morphologic investigation thoracic cardiac nerves were found to arise from the sympathetic trunk between the cervicothoracic ganglia and fourth or fifth thoracic ganglia on the right and left sides, respectively. Perman ('24) and investigators previous to him, did not report thoracic cardiac nerves in the cat. Anufriew ('28) noted their presence as far caudal as the second thoracic ganglion only on the left side. Saccomanno ('43), supporting gross findings with histologic observations, followed them bilaterally from the upper five or six thoracic sympathetic ganglia to the cardiac plexus. Thoracic cardiac nerves are variable in number and origin between specimens. Cervicothoracic cardiac nerves have been traced to the cardiac plexus from each side by Saccornanno ('43). Perman ('24) indicated that they passed to the atria, dorsal walls of both ventricles, and the lateral wall of the left ventricle from the left side. In agreement with Anufsiew ('28), the present authors found that left cervicothoracic cardiac nerves passed primarily to the dorsum of the left auricle, ventrum of the left atrium, caudal and right walls of the left ventricle, interatrial and interventricular septa from the right side, and the caudal right portion of the right ventricle. In addition, the present investigators found branches which continued through the cardiac plexus to join the combined trunk of right heart nerves. Both Perman ('24) and Anufriew ('28) found right cervicothoracic cardiac nerves passing to the ventral portion of the right ventricle and along the left longitudinal sulcus to both ventricles. In addition, Anufriew ('28) noted E. Recurrent cardiac nerves branches to the right auricles and atrium. Twigs arising from the LEFT recurrent The findings of the present authors are in laryngeal nerves were not followed to the agreement with Anufriew ('28). FELINE CARDIAC INNERVATION The inconstant intermediate ganglion and intermediate cardiac nerves in the cat were not reported previous to the present investigation. Their prominence varied considerably between specimens and they were similarly located only in one other species, the porcine. In accordance with Wrete ('59) the term intermediate ganglion is reserved for small inconstant ganglia situated in internodal rami between constant ganglia, as well as in communicating rami or in the main trunk or roots of spinal nerves. Though somewhat less than in the canine, the vertebral cardiac nerves contribute a large portion of the sympathetic cardiac innervation in the feline. Mannu ('14) and Saccomanno ('43) noted cardiac nerves from the vertebral ganglia but followed them only to the cardiac plexus. Perman ('24) noted their distribution from each side to the cranial portion of the right ventricle. Anufriew ('28) did not recognize these nerves. The present authors found that vertebral cardiac nerves passed to each of the major areas of distribution (table 2). Cervical cardiac nerves were not noted from the cranial cervical ganglion, nor was a middle cervical ganglion noted grossly. Vagal cardiac nerves, in agreement with Anufriew ('28), were followed to each of the major areas of distribution (table 2 ) . Both the atria and ventricles received fibers. Left recurrent cardiac nerves were not observed, though submacroscopic communications are suspected. Right recurrent cardiac nerves joined and were distributed with other right cardiac nerves. Though the origin, course, and distribution of cardiac nerves of the feline re- 553 semble those of the canine, generally, they combined on each side in the cat resulting in large trunks to specific areas. However, through communication with the cardiac plexus several areas could be supplied by a single trunk. ACKNOWLEDGMENT The appreciation of the authors is extended to Dr. D. J. Hillman for the photography. LITERATURE CITED Anufriew, W. N. 1928 Die Herznerven des Katze. Ztschr. f. Anat. u Entwg., 86: 639-654. Bernhardt, E. 1868 Anatomische und physiologische Untersuchungen uber den Nerve depressor bei der Katze. Dissertation Dorpat. Original not available; cited in Anufriew, W. N. 1928 Die Herznerven des Katze. Ztschr. f. Anat. u Entwg., 86: 639-654. Boehm, R. 1875 Untersuchungen uber den Nervus accelerator cordis der Katze. Arch. f. Exp. Path. u Pharm., 4 : 255-279. Kazem Beck, A. 1888 Beitrag zur Innervation des Herzens Arch. f. Anat. u Phys., 12: 325349. Mannu, A. 1914 Ricerche anatomocomperative sul simpatico cervicale nei mammiferi. Intern. Monatsschr. f. Anat. u Physiol., 30: 49-168. McKibben, J., and R. Getty 1968 A comparative morphologic study of the cardiac innervation in domestic animals. I. The canine. Am. J. Anat., 122: 533-544. Nonidez, J. F. 1939 Studies on the innervation of the heart. I. Distribution of the cardiac nerves, with special reference to the identification of the sympathetic and parasympathetic postganglionics. Am. J. Anat., 65: 361-401. Perman, E. 1924 Anatomische Untersuchung uber die Herznerven bei den hoheren Saugetieren und bei Menschen. Ztschr. f. Anat. u Entwg., 71: 382-457. Saccomanno, G. 1943 The components of the upper thoracic sympathetic nerves. J. Comp. Neur., 79: 355-379. Wrete, M. 1959 The anatomy of the sympathetic trunks in man. J. Anat., 93: 448-459.