JOURNAL OF MORPHOLOGY 207:165-172 (1991)
Topography and Nerve Supply of the Cucullaris (Trapezius) of Skates ROBERF L. BOOR11 AND DAVID G. SPERRY School of Life and Health Sciences, University of Delaware, Newark, Delaware 1971 6
ABSTRACT Dissections of Sudan black B stained specimens reveal that, of a complex of medial, intermediate, and lateral muscles of skates, presumed homologous to the cucullaris of sharks, only the lateral muscle is innervated by a branch or branches of the vagus and is inserted, in part, to the fused pharyngobranchials of the caudal visceral arches. The medial and intermediate muscles are supplied by separate branches of rostral spinal nerves and do not attach to the branchial skeleton. The lateral muscle therefore is the most likely homologue of the cucullaris (trapezius) of sharks and perhaps other fishes and tetrapods. The medial and intermediate muscles appear to be part of the axial musculature. The cucullaris (trapezius), among selachians, is a large superficial branchial muscle originating from the fascia covering the sides of the epaxial musculature and inserting on the pectoral girdle and last branchial arch. On the basis of its attachments, the cucullaris probably elevates and protracts the pectoral girdle and a part of the branchial skeleton. The cucullaris is innervated by a branch of the vagus termed the ramus accessorius (Marion, '05; Norris and Hughes, '20; Tanaka, '88). This ramus is generally, but not universally, believed t o contain special visceral motor neuronal components t o muscle derived from unsegmented hypomeric branchial mesoderm (Straus and Howell, '36; Romer and Parsons, '86; Kent, '87; Krammer et al., '87). The skeleton of rajoid elasmobranchs (skates),in contrast t o sharks, is highly modified, e.g., rostral vertebrae are fused to form a synarcium, a part of the pectoral girdle is fused with this synarcium to form a large rigid synarcual-pectoral girdle complex that encircles the body, and the number of independent branchial skeletal elements is reduced by fusion (Compagno, '77). The topography and attachments of a cucullaris muscle in skates, as a consequence of skeletal changes that significantly reduce mobility, can he expected to be modified but the muscle retained as a basic part of the elasmobranch body plan. Among rajoids, however, a homologue of cucullaris is uncertain. Marion ('05) de-
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1991 WILEY-LISS, INC.
scribes, on the basis of position and attachments, a complex of three muscles in Raja that resembles cucullaris of the dogfish shark and suggests that this complex is, wholly or in part, cucullaris (trapezius). Although attachments and functions may be modified, the cucullaris or its homologue in rajoids can be expected, as in selachians, to be innervated by a branch (or branches) of the vagus. However, the nerves supplying the three muscles of the presumed cucullaris complex in skates have not been described. The purpose of this study, therefore, using attachments and innervation as criteria, is to identify the homologue of the cucullaris in skates. With this information the central nucleus of origin of the motor components that supply this muscle can he identified by experimental methods. Knowledge of the cucullaris and its innervation in skates is important because elasmobranchs are considered generalized vertebrates and likely show primitive gnathostome patterns. This kind of information can be expected to lead to a better understanding of the evolution of the accessory nerve and the muscles it innervates among cartilaginous fishes, as well as in other vertebrates. Moreover, theories of vertebrate origins and relationships are based, to a large extent, on the branchial skeleton, musculature and nerves (Goodrich, '30; Northcutt and Gans, '831, and comparisons of different elasmobranchs (i.e., sharks and skates) will be useful for distinguishing possible morpho-
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types needed to test newly emerging theories regarding chordate cranial organization (Northcutt, '90). MATERIALS AND METHODS
Two clearnose skates, Raja eglanteria (males; 28.0 cm rostrum to vent lengths), and two little skates, Raja erinacea (females; 42.0 and 45.0 cm total lengths), caught by otter trawl in the Delaware Bay, were used in this study. A dry skeleton of one clearnose skate was prepared according t,o the procedure described by Hildebrand ('68). The remaining three specimens were anesthetized with ethyl m-aminobenzoate methanesulfonic acid salt (Aldrich), fixed by intracardial perfusion with 10%formal-saline, and stored in 10% neutral formalin. Of these, the clearnose skate was used €or gross dissection. The head and trunk to a level immediately caudal to the pectoral girdle of the two little skates were stained en toto with Sudan black B
(Rasmussen, '61) and used to reveal, by dissection, the nerve supply to relevant muscles. The blue/black stained myelinated axons and relatively unstained ganglion cells are easily seen with moderate magnifications ( x 10-16). RESULTS
Three muscles, termed medial, intermediate, and lateral (Marion, '05) are situated, in both Raja eglanteria and R. erinacea, between the dorsal synarcual process and the pectoral girdle. This complex of muscles, at the surface, is bounded medially by the dorsal longitudinal muscle mass and laterally by the most caudal dorsal superficial branchial constrictors (Fig. 1).Each of these three muscles differs in its attachments and innervation.
The medial muscle The medial muscle (Fig. 1A,B) is superficial and more-or-less separated from the un-
B Fig. 1. A: Topography of medial, intermediate, and lateral muscles of the clearnose skate (Ruju eglunteriu), dorsal view. B: Diagram of A. Scale bar = 2.00 cm.
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derlying and adjacent epaxial muscle by connective tissue septa. It arises from the caudal and medial surfaces of the dorsal synarcual process and its fibers pass caudally to insert on the middle one-third of the rostral and ventral border of the suprascapula (Fig. 2A,C,E).
T h e medial muscle is innervated by branches of the dorsal and ventral roots of segmental spinal nerves 10-16 (Fig. 3) that course peripherally, within the horizontal septum. The sensory components of these nerves spring directly from the dorsal root ganglia (Fig. 3A,B). The majority of the sensory fi-
LATERAL MUSCLE
F Fig. 2 A,B: Dorsolateral and lateral views, respectively, of a skeletal preparation of the clearnose skate at synarcual, branchial and pectoral levels C: Diagram of A (* = pharyngobranchials) D: Diagram of B E: Diagram
showing the attachments of medial and intermediate muscles F: Diagram showing the attachments of the lateral muscle Scale bar = 2 00 cm
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Fig. 3. A The spinal nerves at segmental dorsal root levels 13-15 of the little skate Raja erinacea, dorsal view. Rostra1 is toward the top of the figure. B: Diagram of a portion of A showing the origin of the sensory nerves (cross hatching) that innervate the medial muscle and skin. The nerves (oblique hatching) from the ventral roots supply the dorsal (epaxial) longitudinal muscle. C:
A dorsal root and its ganglion have been retracted to expose a motor nerve (arrow) emanating from a ventral root and joining a sensory nerve. D: Diagram of C showing the sensory (cross hatching) and motor (solid) components of a nerve that supplies the medial muscle. Scale bar = 1.00 mm.
bers are distributed to the skin, but a proportion enters the muscle on its medial aspect. The sensory nerves are joined, at the level of the ganglia, by small branches of the ventral roots (Fig. 3C,D) that accompany the former, enroute to the medial muscle. It proved possible to demonstrate the motor branches on segmental ventral root number 12 on one specimen and on ventral roots 15 and 16 on another specimen. The nerves that supply the medial muscle are separate from the large spinal nerve rami that course ventral to the horizontal septum to supply the fin musculature as well a s those rami emanating from the ventral roots (Fig. 3A,B) that cross the
ganglia and turn dorsally to supply the dorsal longitudinal muscle bundles medial t o the medial muscle. The intermediate muscle The origin of this muscle is by a deep, broad tendon from the ventral surface and lateral edge of the shelf of the synarcium, a t the level of the dorsal process. Its fibers pass dorsolaterally to insert on the rostrodorsal surface of the scapulocoracoid and, to a lesser extent, on the rostra1 edge of the lateral part of the suprascapula (Fig. ZA,C,E). The intermediate muscle is innervated primarily by branches of the ventral roots of spinal nerves
CUCULLARIS OF SKATES
10-12 (Fig. 4A,B), with a minor contribution from 13 and 14.These branches course caudally, ventral to the horizontal septum, and form a plexus from which fibers enter the dorsomedial surface of the muscle. No sensory fibers from the dorsal roots could be traced to this muscle.
The lateral muscle The lateral muscle consists of a smaller deep part and a larger superficial part. From a common origin on the lateral surface of the dorsal synarcual process, the fibers of the deep part pass ventrolaterally and caudally to insert on the lateral surface of the fused pharyngobranchials of the caudal visceral arches. The fibers of the superficial part pass ventrolaterally and caudally to insert on the rostroventral surface of the scapulocoracoid (Fig. 2B,D,F). Both parts of the lateral muscle are innervated by a branch (or branches) of the intestinal ramus of the vagus. These branches course caudodorsally to enter the medial surface of the muscle (Fig. 5). DISCUSSION
The lateral muscle, of the three muscles described by Marion ('05) and presumed to represent a trapezius complex in skates, is
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the most likely homologue of the cucullaris (trapezius) of sharks because 1) it is the only one of the complex innervated by a branch or branches (an accessory nerve) of the vagus and 2) it is the only one attached to an element of the branchial skeleton. The cucullaris of sharks is supplied by a n accessory nerve branching from the vagus (Alopias and Cynias: Edgeworth, '35; Mustelus: Tanaka, '88; Squalus acanthias: Norris and Hughes, 'go), although in some species branches of the first four spinal nerves also contribute to its innervation (Chlamydoselachus, Heptranchias, Heterodontus, Hexanchus, S. mitsukurzi: Edgeworth, '35). The presence of two heads to the lateral muscle of skates, with one head attached to the branchial skeleton and one head to the girdle, parallels the condition of the cucullaris of sharks where cranial and caudal parts are inserted onto the last branchial arch and scapula, respectively (Mustelus: Tanaka, '88). The cucullaris of other cartilaginous fishes, i.e., the Holocephali (chimaeras), like the lateral muscle of skates, is composed of superficial and deep parts inserting on the pectoral girdle and branchial skeleton, respectively (Edgeworth, '35). Each part of the holocephalian cucullaris is innervated by a separate branch of the vagus.
Fig. 4. A Ventral view showing branches of ventral roots 10-12 and their course to the intermediate musclc of the little skate. B: Diagram of A with nerve (solid) to the intermediate muscle indicated. Scale bar = 1.00mm.
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Fig. 5. A Ventral view showing the nerve to the lateral muscle of the little skate. B: Diagram ofA with nerve (solid) to the lateral muscle indicated. Scale bar = 1.00 mm.
Medial and intermediate muscles of the presumed cucullaris complex of skates, in contrast to the lateral muscle, are attached only to the vertebral column and pectoral girdle and each is innervated only by branches of the ventral roots of rostra1 spinal nerves. Muscles of similar topography and innervation are not described in sharks. While the position and nerve supply of the medial and intermediate muscles of skates do not preclude them from being parts of a larger cucullaris muscle field, they appear to be epaxial and hypaxial respectively because of the peripheral pathways taken by their nerves relative to the horizontal septum. Interestingly, branches supplying the medial and intermediate muscles are not merely those that supply the general axial muscles but are separate sets of nerves in each case. Nerves to both muscles are probably mixed (motor and sensory) even though our dissections failed to demonstrate sensory fibers joining the nerves to the intermediate muscle. Additionally, while the specific segmental
levels probably vary from specimen to specimen, each musclc is innervated by multiple spinal segments situated far caudal to the vagal rootlets. I t is important to discover the central location of the motor neurons that supply the medial and intermediate muscles and to show their relationships with those that supply the lateral muscle, as well as those that supply the epaxial and hypaxial longitudinal musculature. This information could support our interpretation that the medial and intermediate muscles are parts of the general axial musculature and are not branchial. The location of the motor neurons that innervate the cucullaris of sharks and skates is unknown. Barry ('87), who studied the central connections of the vagus nerve of the clearnose skate, shows that the most caudal rootlet of the vagus contains only motor components and speculates that it is the accessory nerve. Moreover, he describes a column of large motor neurons, situated ventrolateral to the dorsal vagal motor nucleus, which
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extends from the middle vagal rootlets to the level of the 5-6th ventral root segments of the spinal cord. The cells of this column, named the ventral nucleus of the vagus, are believed to have migrated into this position from the dorsal vagal column (see Barry, '87) and may be the possible homologue of ambiguus of amniotes. We predict that the ventral motor nucleus of the vagus is the source of axons that comprise the nerve to the lateral muscle of skates. Although the specific aim of this investigation was to compare the cucullaris in skates with their selachian relatives, the more general problem of cucullaris (trapezius) and accessory nerve homologues among vertebrates becomes apparent. Among other fishes and tetrapods, a variety of conditions have been reported for the cucullaris or trapezius muscle, i.e., absence, reduction, number of separate parts, position, and attachments. A common characteristic, among fishes, amphibians, and reptiles, is that a cucullaris or trapezius is innervated by a branch of the vagus, although rostra1 spinal nerves may participate in its innervation (Takahasi, '25; Edgeworth, '35; Straus and Howell, '36; Paterson, '39). This is the condition in elasmobranchs and may represent the primitive gnathostome pattern. In birds, e.g., chick and cockatoo, cucullaris or trapezius is innervated by a true accessory nerve formed from fibers that arise from the medulla, posterior to the rootlets of the vagus, and from the first and second segments of the spinal cord (Rogers, '65;Wild, '811. In mammals, e.g., rat and human, the trapezius complex is likewise innervated exclusively by a spinal accessory nerve. The rootlets of the mammalian accessory nerve are, in comparison to birds, more caudally located and not superficially attached to the medulla in intimate association with vagal rootlets (Brodal, '59; Pearson et al., '64; Krammer et al., '87). The evolutionary history of the cucullarisi trapezius musculature and the accessory nerve is uncertain. An explanation for the transition from a cucullarishrapezius muscle innervated by a branch of the vagus, as in elasmobranchs, to one innervated by a separate accessory nerve that is not a n integral part of the vagus, as in birds and mammals, is of phylogenetic importance. The relations of the accessory motor neurons to vagal and occipito-spinal motor neurons are controversial and there is no consensus of opinion that the accessory motor neurons are correctly
classified as special visceral that supply striated branchial muscle of unsegmented hypomeric origin (Pearson et al., '64; Wild, '81; Krammer et al., '87). Indeed, recent evidence indicates that, unlike previously and longbelieved, the ventral mesoderm of the head may arise embryonically from paraxial somitomeres or somites (Noden, '84; Gilland, '85; Martindale et al., '87). This mesoderm may include the mesoderm giving rise to those arch levators that fuse to form the cucullaris of selachians. If this is true, the ventral motor nucleus of the vagus in skates may be part of a larger population of occipito-spinal motor neurons innervatinga cucullarisitrapezius rather than a population of special visceral motor neurons derived from the dorsal vagal nucleus. Evidence to support these suggestions will contribute to an understanding of unresolved problems in comparative anatomy that include, in particular, the origin and functional classification of the components of the accessory nerve and, more generally, the relationships between cranial nerve organization and segmentation of the chordate head (Northcutt, '90). ACKNOWLEDGMENTS
This work was supported by USPHS grants NS11272 and NS21878. LITERATURE CITED Barry, M.A. (1987) Central connections of the IXth and Xth cranial nerves in the clearnose skate, Raja eglanteria. Brain Res. 425r159-166. Brodal, A. (1959) The Cranial Nerves. Oxford: Blackwell. Compagno, L.J.V. (1977) Phyletic relationships of living sharks and rays. Am. Zool. I7r303-322. Edgeworth, F.H. (1935) The Cranial Muscles of Vertebrates. London: Cambridge Univ. Press. Gilland, E.H. (1985) Morphology and development of head mesoderm in early embryos of Squalus acanthias. Am. Zool. 25r93A. Goodrich, E.S. (1930) Studies on the Structure and Development of Vertebrates. London: The Macmillan Co. (Reprinted by Dover Publications, New York, 1958). Hildebrand, M. (1968) Anatomical Preparations. Berkeley: Univ. of California Press. Kent, G.C. (1987) Comparative Anatomy of the Vertebrates. St. Louis: C.V. Mosby Co. Krammer, E.B., M.F. Lischka, T.P. Egger, M. Riedl, and H. Gruber 11987) The motoneuronal organization of the spinal accessory nuclear complex. Adv. Anat. Embryol. Cell Biol. 103:l-62. Marion, G.E. (1905)Mandibular and pharyngeal muscles ofAcanthzas and Raia. Am. Naturalist 39:891-924. Martindale, M.Q., S. Meier, and A.G. Jacobson (1987) Mesodermal metamerism in the teleost, Oryzias latipes (the Medaka). J. Morphol. 293:241-252. Noden, D.M. (1984) Craniofacial development new views on old problems. Anat. Rec. 208r1-13. Norris, H.W., and S.P. Hughes (1920) The cranial, occipital, and anterior spinal nerves of the dogfish, Squalus acanthias. J. Comp. Neurol. 31.293-402.
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Northmtt, R.G. (1990) Ontogeny and phylogeny: A reevaluation of conceptual relationships and some applications. Brain Behav. Evol. 36t116-140. Northcutt, R.G., and C. Gans (1983) The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Quart. Rev. Bid. 58:1-28. Paterson, N.F. (1939)The head ofXenopus lueuis. Quart. J. MicroscopicalSci. New Series 81:161-234 (16 plates). Pearson, A.A., R.W. Sauter, and G.R. Herrin (1964)The accessory nerve and its relation to the upper spinal nerves. Am. J. Anat. 114t371-391. Rasmussen, G.L. (1961)A method of staining the statoacaustic nerve in bulk with Sudan black B. Anat. Rec. 139t465-470. Rogers, K.T. (1965) Development of the XIth or spinal accessory nerve in the chick. J. Comp. Neural. 125273285.
Romer, A.S., and T.S. Parsons (1986) The Vertebrate Body, 6th ed.New York: CBS College Publishing. Straus, W.L., and A.B. Howell (1936) The spinal accessory nerve and its musculature. Quart. Rev. Biol. 11: 387405. Takahasi, N. (1925) On the homology of the cranial muscles of the cypriniform fishes. J. Morphol. 40:l109. Tanaka, S. (1988) A macroscopical study of the trapezius muscle of sharks, with reference to the topographically related nerves and vein. Anat. Anz. (Jena) 165:7-21. Wild, J.M. (1981) Identification and localization of the motor nuclei and sensory projections of the glossopharyngeal, vagus and hypoglossal nerves of the cockatoo (Cdcatua rose~cupiZZu), Cacatuidae. J. Comp. NeuroI. 203:351-377.
Topography and Nerve Supply of the Cucullaris (Trapezius) of Skates ROBERF L. BOOR11 AND DAVID G. SPERRY School of Life and Health Sciences, University of Delaware, Newark, Delaware 1971 6
ABSTRACT Dissections of Sudan black B stained specimens reveal that, of a complex of medial, intermediate, and lateral muscles of skates, presumed homologous to the cucullaris of sharks, only the lateral muscle is innervated by a branch or branches of the vagus and is inserted, in part, to the fused pharyngobranchials of the caudal visceral arches. The medial and intermediate muscles are supplied by separate branches of rostral spinal nerves and do not attach to the branchial skeleton. The lateral muscle therefore is the most likely homologue of the cucullaris (trapezius) of sharks and perhaps other fishes and tetrapods. The medial and intermediate muscles appear to be part of the axial musculature. The cucullaris (trapezius), among selachians, is a large superficial branchial muscle originating from the fascia covering the sides of the epaxial musculature and inserting on the pectoral girdle and last branchial arch. On the basis of its attachments, the cucullaris probably elevates and protracts the pectoral girdle and a part of the branchial skeleton. The cucullaris is innervated by a branch of the vagus termed the ramus accessorius (Marion, '05; Norris and Hughes, '20; Tanaka, '88). This ramus is generally, but not universally, believed t o contain special visceral motor neuronal components t o muscle derived from unsegmented hypomeric branchial mesoderm (Straus and Howell, '36; Romer and Parsons, '86; Kent, '87; Krammer et al., '87). The skeleton of rajoid elasmobranchs (skates),in contrast t o sharks, is highly modified, e.g., rostral vertebrae are fused to form a synarcium, a part of the pectoral girdle is fused with this synarcium to form a large rigid synarcual-pectoral girdle complex that encircles the body, and the number of independent branchial skeletal elements is reduced by fusion (Compagno, '77). The topography and attachments of a cucullaris muscle in skates, as a consequence of skeletal changes that significantly reduce mobility, can he expected to be modified but the muscle retained as a basic part of the elasmobranch body plan. Among rajoids, however, a homologue of cucullaris is uncertain. Marion ('05) de-
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1991 WILEY-LISS, INC.
scribes, on the basis of position and attachments, a complex of three muscles in Raja that resembles cucullaris of the dogfish shark and suggests that this complex is, wholly or in part, cucullaris (trapezius). Although attachments and functions may be modified, the cucullaris or its homologue in rajoids can be expected, as in selachians, to be innervated by a branch (or branches) of the vagus. However, the nerves supplying the three muscles of the presumed cucullaris complex in skates have not been described. The purpose of this study, therefore, using attachments and innervation as criteria, is to identify the homologue of the cucullaris in skates. With this information the central nucleus of origin of the motor components that supply this muscle can he identified by experimental methods. Knowledge of the cucullaris and its innervation in skates is important because elasmobranchs are considered generalized vertebrates and likely show primitive gnathostome patterns. This kind of information can be expected to lead to a better understanding of the evolution of the accessory nerve and the muscles it innervates among cartilaginous fishes, as well as in other vertebrates. Moreover, theories of vertebrate origins and relationships are based, to a large extent, on the branchial skeleton, musculature and nerves (Goodrich, '30; Northcutt and Gans, '831, and comparisons of different elasmobranchs (i.e., sharks and skates) will be useful for distinguishing possible morpho-
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types needed to test newly emerging theories regarding chordate cranial organization (Northcutt, '90). MATERIALS AND METHODS
Two clearnose skates, Raja eglanteria (males; 28.0 cm rostrum to vent lengths), and two little skates, Raja erinacea (females; 42.0 and 45.0 cm total lengths), caught by otter trawl in the Delaware Bay, were used in this study. A dry skeleton of one clearnose skate was prepared according t,o the procedure described by Hildebrand ('68). The remaining three specimens were anesthetized with ethyl m-aminobenzoate methanesulfonic acid salt (Aldrich), fixed by intracardial perfusion with 10%formal-saline, and stored in 10% neutral formalin. Of these, the clearnose skate was used €or gross dissection. The head and trunk to a level immediately caudal to the pectoral girdle of the two little skates were stained en toto with Sudan black B
(Rasmussen, '61) and used to reveal, by dissection, the nerve supply to relevant muscles. The blue/black stained myelinated axons and relatively unstained ganglion cells are easily seen with moderate magnifications ( x 10-16). RESULTS
Three muscles, termed medial, intermediate, and lateral (Marion, '05) are situated, in both Raja eglanteria and R. erinacea, between the dorsal synarcual process and the pectoral girdle. This complex of muscles, at the surface, is bounded medially by the dorsal longitudinal muscle mass and laterally by the most caudal dorsal superficial branchial constrictors (Fig. 1).Each of these three muscles differs in its attachments and innervation.
The medial muscle The medial muscle (Fig. 1A,B) is superficial and more-or-less separated from the un-
B Fig. 1. A: Topography of medial, intermediate, and lateral muscles of the clearnose skate (Ruju eglunteriu), dorsal view. B: Diagram of A. Scale bar = 2.00 cm.
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derlying and adjacent epaxial muscle by connective tissue septa. It arises from the caudal and medial surfaces of the dorsal synarcual process and its fibers pass caudally to insert on the middle one-third of the rostral and ventral border of the suprascapula (Fig. 2A,C,E).
T h e medial muscle is innervated by branches of the dorsal and ventral roots of segmental spinal nerves 10-16 (Fig. 3) that course peripherally, within the horizontal septum. The sensory components of these nerves spring directly from the dorsal root ganglia (Fig. 3A,B). The majority of the sensory fi-
LATERAL MUSCLE
F Fig. 2 A,B: Dorsolateral and lateral views, respectively, of a skeletal preparation of the clearnose skate at synarcual, branchial and pectoral levels C: Diagram of A (* = pharyngobranchials) D: Diagram of B E: Diagram
showing the attachments of medial and intermediate muscles F: Diagram showing the attachments of the lateral muscle Scale bar = 2 00 cm
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Fig. 3. A The spinal nerves at segmental dorsal root levels 13-15 of the little skate Raja erinacea, dorsal view. Rostra1 is toward the top of the figure. B: Diagram of a portion of A showing the origin of the sensory nerves (cross hatching) that innervate the medial muscle and skin. The nerves (oblique hatching) from the ventral roots supply the dorsal (epaxial) longitudinal muscle. C:
A dorsal root and its ganglion have been retracted to expose a motor nerve (arrow) emanating from a ventral root and joining a sensory nerve. D: Diagram of C showing the sensory (cross hatching) and motor (solid) components of a nerve that supplies the medial muscle. Scale bar = 1.00 mm.
bers are distributed to the skin, but a proportion enters the muscle on its medial aspect. The sensory nerves are joined, at the level of the ganglia, by small branches of the ventral roots (Fig. 3C,D) that accompany the former, enroute to the medial muscle. It proved possible to demonstrate the motor branches on segmental ventral root number 12 on one specimen and on ventral roots 15 and 16 on another specimen. The nerves that supply the medial muscle are separate from the large spinal nerve rami that course ventral to the horizontal septum to supply the fin musculature as well a s those rami emanating from the ventral roots (Fig. 3A,B) that cross the
ganglia and turn dorsally to supply the dorsal longitudinal muscle bundles medial t o the medial muscle. The intermediate muscle The origin of this muscle is by a deep, broad tendon from the ventral surface and lateral edge of the shelf of the synarcium, a t the level of the dorsal process. Its fibers pass dorsolaterally to insert on the rostrodorsal surface of the scapulocoracoid and, to a lesser extent, on the rostra1 edge of the lateral part of the suprascapula (Fig. ZA,C,E). The intermediate muscle is innervated primarily by branches of the ventral roots of spinal nerves
CUCULLARIS OF SKATES
10-12 (Fig. 4A,B), with a minor contribution from 13 and 14.These branches course caudally, ventral to the horizontal septum, and form a plexus from which fibers enter the dorsomedial surface of the muscle. No sensory fibers from the dorsal roots could be traced to this muscle.
The lateral muscle The lateral muscle consists of a smaller deep part and a larger superficial part. From a common origin on the lateral surface of the dorsal synarcual process, the fibers of the deep part pass ventrolaterally and caudally to insert on the lateral surface of the fused pharyngobranchials of the caudal visceral arches. The fibers of the superficial part pass ventrolaterally and caudally to insert on the rostroventral surface of the scapulocoracoid (Fig. 2B,D,F). Both parts of the lateral muscle are innervated by a branch (or branches) of the intestinal ramus of the vagus. These branches course caudodorsally to enter the medial surface of the muscle (Fig. 5). DISCUSSION
The lateral muscle, of the three muscles described by Marion ('05) and presumed to represent a trapezius complex in skates, is
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the most likely homologue of the cucullaris (trapezius) of sharks because 1) it is the only one of the complex innervated by a branch or branches (an accessory nerve) of the vagus and 2) it is the only one attached to an element of the branchial skeleton. The cucullaris of sharks is supplied by a n accessory nerve branching from the vagus (Alopias and Cynias: Edgeworth, '35; Mustelus: Tanaka, '88; Squalus acanthias: Norris and Hughes, 'go), although in some species branches of the first four spinal nerves also contribute to its innervation (Chlamydoselachus, Heptranchias, Heterodontus, Hexanchus, S. mitsukurzi: Edgeworth, '35). The presence of two heads to the lateral muscle of skates, with one head attached to the branchial skeleton and one head to the girdle, parallels the condition of the cucullaris of sharks where cranial and caudal parts are inserted onto the last branchial arch and scapula, respectively (Mustelus: Tanaka, '88). The cucullaris of other cartilaginous fishes, i.e., the Holocephali (chimaeras), like the lateral muscle of skates, is composed of superficial and deep parts inserting on the pectoral girdle and branchial skeleton, respectively (Edgeworth, '35). Each part of the holocephalian cucullaris is innervated by a separate branch of the vagus.
Fig. 4. A Ventral view showing branches of ventral roots 10-12 and their course to the intermediate musclc of the little skate. B: Diagram of A with nerve (solid) to the intermediate muscle indicated. Scale bar = 1.00mm.
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Fig. 5. A Ventral view showing the nerve to the lateral muscle of the little skate. B: Diagram ofA with nerve (solid) to the lateral muscle indicated. Scale bar = 1.00 mm.
Medial and intermediate muscles of the presumed cucullaris complex of skates, in contrast to the lateral muscle, are attached only to the vertebral column and pectoral girdle and each is innervated only by branches of the ventral roots of rostra1 spinal nerves. Muscles of similar topography and innervation are not described in sharks. While the position and nerve supply of the medial and intermediate muscles of skates do not preclude them from being parts of a larger cucullaris muscle field, they appear to be epaxial and hypaxial respectively because of the peripheral pathways taken by their nerves relative to the horizontal septum. Interestingly, branches supplying the medial and intermediate muscles are not merely those that supply the general axial muscles but are separate sets of nerves in each case. Nerves to both muscles are probably mixed (motor and sensory) even though our dissections failed to demonstrate sensory fibers joining the nerves to the intermediate muscle. Additionally, while the specific segmental
levels probably vary from specimen to specimen, each musclc is innervated by multiple spinal segments situated far caudal to the vagal rootlets. I t is important to discover the central location of the motor neurons that supply the medial and intermediate muscles and to show their relationships with those that supply the lateral muscle, as well as those that supply the epaxial and hypaxial longitudinal musculature. This information could support our interpretation that the medial and intermediate muscles are parts of the general axial musculature and are not branchial. The location of the motor neurons that innervate the cucullaris of sharks and skates is unknown. Barry ('87), who studied the central connections of the vagus nerve of the clearnose skate, shows that the most caudal rootlet of the vagus contains only motor components and speculates that it is the accessory nerve. Moreover, he describes a column of large motor neurons, situated ventrolateral to the dorsal vagal motor nucleus, which
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extends from the middle vagal rootlets to the level of the 5-6th ventral root segments of the spinal cord. The cells of this column, named the ventral nucleus of the vagus, are believed to have migrated into this position from the dorsal vagal column (see Barry, '87) and may be the possible homologue of ambiguus of amniotes. We predict that the ventral motor nucleus of the vagus is the source of axons that comprise the nerve to the lateral muscle of skates. Although the specific aim of this investigation was to compare the cucullaris in skates with their selachian relatives, the more general problem of cucullaris (trapezius) and accessory nerve homologues among vertebrates becomes apparent. Among other fishes and tetrapods, a variety of conditions have been reported for the cucullaris or trapezius muscle, i.e., absence, reduction, number of separate parts, position, and attachments. A common characteristic, among fishes, amphibians, and reptiles, is that a cucullaris or trapezius is innervated by a branch of the vagus, although rostra1 spinal nerves may participate in its innervation (Takahasi, '25; Edgeworth, '35; Straus and Howell, '36; Paterson, '39). This is the condition in elasmobranchs and may represent the primitive gnathostome pattern. In birds, e.g., chick and cockatoo, cucullaris or trapezius is innervated by a true accessory nerve formed from fibers that arise from the medulla, posterior to the rootlets of the vagus, and from the first and second segments of the spinal cord (Rogers, '65;Wild, '811. In mammals, e.g., rat and human, the trapezius complex is likewise innervated exclusively by a spinal accessory nerve. The rootlets of the mammalian accessory nerve are, in comparison to birds, more caudally located and not superficially attached to the medulla in intimate association with vagal rootlets (Brodal, '59; Pearson et al., '64; Krammer et al., '87). The evolutionary history of the cucullarisi trapezius musculature and the accessory nerve is uncertain. An explanation for the transition from a cucullarishrapezius muscle innervated by a branch of the vagus, as in elasmobranchs, to one innervated by a separate accessory nerve that is not a n integral part of the vagus, as in birds and mammals, is of phylogenetic importance. The relations of the accessory motor neurons to vagal and occipito-spinal motor neurons are controversial and there is no consensus of opinion that the accessory motor neurons are correctly
classified as special visceral that supply striated branchial muscle of unsegmented hypomeric origin (Pearson et al., '64; Wild, '81; Krammer et al., '87). Indeed, recent evidence indicates that, unlike previously and longbelieved, the ventral mesoderm of the head may arise embryonically from paraxial somitomeres or somites (Noden, '84; Gilland, '85; Martindale et al., '87). This mesoderm may include the mesoderm giving rise to those arch levators that fuse to form the cucullaris of selachians. If this is true, the ventral motor nucleus of the vagus in skates may be part of a larger population of occipito-spinal motor neurons innervatinga cucullarisitrapezius rather than a population of special visceral motor neurons derived from the dorsal vagal nucleus. Evidence to support these suggestions will contribute to an understanding of unresolved problems in comparative anatomy that include, in particular, the origin and functional classification of the components of the accessory nerve and, more generally, the relationships between cranial nerve organization and segmentation of the chordate head (Northcutt, '90). ACKNOWLEDGMENTS
This work was supported by USPHS grants NS11272 and NS21878. LITERATURE CITED Barry, M.A. (1987) Central connections of the IXth and Xth cranial nerves in the clearnose skate, Raja eglanteria. Brain Res. 425r159-166. Brodal, A. (1959) The Cranial Nerves. Oxford: Blackwell. Compagno, L.J.V. (1977) Phyletic relationships of living sharks and rays. Am. Zool. I7r303-322. Edgeworth, F.H. (1935) The Cranial Muscles of Vertebrates. London: Cambridge Univ. Press. Gilland, E.H. (1985) Morphology and development of head mesoderm in early embryos of Squalus acanthias. Am. Zool. 25r93A. Goodrich, E.S. (1930) Studies on the Structure and Development of Vertebrates. London: The Macmillan Co. (Reprinted by Dover Publications, New York, 1958). Hildebrand, M. (1968) Anatomical Preparations. Berkeley: Univ. of California Press. Kent, G.C. (1987) Comparative Anatomy of the Vertebrates. St. Louis: C.V. Mosby Co. Krammer, E.B., M.F. Lischka, T.P. Egger, M. Riedl, and H. Gruber 11987) The motoneuronal organization of the spinal accessory nuclear complex. Adv. Anat. Embryol. Cell Biol. 103:l-62. Marion, G.E. (1905)Mandibular and pharyngeal muscles ofAcanthzas and Raia. Am. Naturalist 39:891-924. Martindale, M.Q., S. Meier, and A.G. Jacobson (1987) Mesodermal metamerism in the teleost, Oryzias latipes (the Medaka). J. Morphol. 293:241-252. Noden, D.M. (1984) Craniofacial development new views on old problems. Anat. Rec. 208r1-13. Norris, H.W., and S.P. Hughes (1920) The cranial, occipital, and anterior spinal nerves of the dogfish, Squalus acanthias. J. Comp. Neurol. 31.293-402.
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