Zbl. Vet. Med. C, 4,323-333
(1975)
0 1975 Verlag Paul Parey, Berlin und Hamburg ISSN 0041-4294/ASTM-Coden: AHEMA 5
Department of Veterinary Anatomy, Faculty of Agriculture, Nagoya University, Nagoya, 464 japan Director: Prof. Dr. M. Yasuda
Further Studies on the Hypoglossal Nucleus in the Fowl BY
TOHRU WATANABE, NOBUO IWATA and MIKIOYASUDA With 7 figrtres
and
2 rubles
(Received for publication: December 2 , 1974)
Introduction KOCH(1888) appears to have described the avian hypoglossal nucleus for the first time. Since then, cytoarchitectonic studies on this nucleus have been performed by many investigators (BRANDIS,1893; KOSAKA/YAGITA, 1903; ARIENSKAPPERS, 1911, 1912; SINN,1913; BOK, 1915; BLACK,1922; GROEBBELS, 1922; PAPEZ,1929; SANDERS, 1929; ADDENS,1933; BARNARD, 1940; 1971). GOLLER, 1969; JUNGHERR, 1969 and HILLEBRAND, KOCH(1888) compared the hypoglossal nucleus of pigeon and duck with those of mammals, and applied the mammalian nomenclature to the avian
BRANOIS(18931
A R I ~ N SKAPPERS
KOSAKA/ YAGITA
(1903I Ventraler Vaguskcrn (gemcinschaftlichcr Vagus- Hypoglossuskern1
Hypoglossuskern
Ventraler Hypoglossusker n
Obere Vorderhorn fortsetzung
SINN (19151
Nucl. intermedius XI1 Dorsaler Hauptkern des Hypoglossus
-
Box (19151
119111
Nucl. ventralis XI1
Nucl. mot. intermedius
Ventraler Nebenkern Nucl. dors. X I 1
des Hypoglossus Nucl. ventr. X I 1
GROEBBELS(19221
AOOENS (19331
BARNARO 119L01
GOLLER(19691
JUNGHERR (19691
Nucl. XI1
Nucl. XI1 dorsalis
Nucl. dorsalis nervi XI1
Nucl. nervl hypoglossi
Nucl. hypoglossus ventralis dorsornedialis
Nucl. cerv. I
Nucl. XI1 ventralis dorsomedialis
Nucl. ventralis nervi XI1
Nucl. residualis
Nucl. hypoglossus ventralis ventro lateralis
Nucl. XI1 ventralis ventroventralis
-
21*
3 24
WATANABE, IWATA and YASUDA
nucleus. BRANDIS (1893) asserted that in many kinds of birds the hypoglossal nerve arose from two nuclei, the ventral vagal or common vagal-hypoglossal (1903) were nucleus and the ventral hypoglossal nucleus. KOSAKA/YAGITA the first to carry out an experimental histological study on the hypoglossal nucleus in birds. They confirmed by the retrograde degeneration method that the hypoglossal nerve of the fowl originated from a nucleus whim was situated immediately below the dorsai vagal nucleus and which corresponded to the dorsal hypoglossal nucleus of KOCH(1888). The descriptions given so far by many investigators as to the central origin of the hypoglossal nerve in the fowl (Table 1) may be classified into three main groups: In group I, the hypoglossal nerve arises from two or three nuclei (SINN,1913; BOK, 1915; ADDENS,1933; BARNARD,1940; JUNGHERR, 1969). In group 11, the hypoglossal nerve arises from two nuclei, the dorsal one of w h i h intermingles with the dorsal vagal nucleus and is shown as 1911, 1912; BOK, the Nucleus intermedius (BRANDIS, 1893; ARIENSKAPPERS, 1915). I n group 111, the hypoglossal nerve arises from one nucleus according (1 903), GROEBBELS (1 922), GOLLER (1969). These previous to KOSAKA/YAGITA studies show considerable disagreements. The aim of this study was to investigate morphologically the origin of the hypoglossal nerve by the retrograde degeneration method in the fowl, Gallus domesticus L., in order to elucidate the functional significance of this nerve in relation to its localization pattern. Material and Methods The brain stem of 59 mature fowls of both sexes and vnious breeds were used. The medulla oblongata was obtained from 57 fowls (1.0 to 2.5 kg. in body weight) which had been subjected to operation and sacrificed 7-10 days later and from the TWO birds which had been left intact. The 57 fowls were operated under sodium pentobarbiturate anesthesia. Transection of nerves was made unilaterally in 47 birds, and in four the nerves were cut bilaterally. Transections were carried out as follows: (1) the hypoglossal nerve stem was cut in 24 birds, (2) the laryngolingual branch was cut in 10 birds, (3) the proximal part of the superior laryngeal bran& was transected unilaterally in 8 birds and the distal part was cut bilaterally in 4 birds, (4) the bran& of the first cervical nerve anastomosin with the hypogloss31 nerve was cut in 5 birds, and (5) a single or combined transection o f s o m e upper cervical nerves was performed in 6 birds. Immediately after decapitation, the whole brain was removed and immersed in 10°/o neutral formalin for a few hours. The medulla oblongata was isolated by two transverse sections made at the level of the lower border of the cerebellar peduncle and the second cervical nerve, respectively. All the specimens were left in 10 O/o neutral formalin for a week and embedded into paraffin wax in the conventional manner. Transverse sections 10 pn. chicit were cut serially and stained with Kluver-Barrera’s lux01 fast blue-cresyl fast violet method. Gomori’s d-irorne alum hematoxylin phloxin method and carbol thionin method were used in some cases. All the Celts, of which the nucIcolus was distinct were counted.
Results Although it was only made possible by employing an experimental approach to delineate the original nucleus of the hypoglossal nerve, the results obtained are presented more expediently in synthetic fashion by discussing first the nomenclature, giving then the normal topography, and finally quoting the protocols of the retrograde cellular changes in general. 1. Nomenclature The esperimental results of this study give evidence that the central origin of the hypoglossal nerve consists of one nucleus. It seems appropriate to apply the eclectic name “Nucleus nervi hypoglossi” to this origin. In a trans-
Further Studies on the Hypoglossal Nucleus in the Fowl
325
c
Fig. 1 a, b, C. Serial transverse sections through the medulla oblongata of a normal fowl showing the hypoglossal nucleus (XII). a: A section of a rostra1 portion 660 pm. distant from the obex. b: The level of the obex. c : A section of a caudal portion 530!tm. distant from the obex. C. Canalis centralis; Nc. Nuclei cervicales; Xd. Nucleus dorsalis n. vagi; Xv. Nucleus ventralis n. vagi; v. Ventriculus quartus. Kliiver and Barrera ( X 23)
326
WATANABE, IVATA and YASUDA
verse section of the medulla oblongata (Fig. 1 a, b, c) it is clearly possible to observe four cell groups which consist of large multipolar cells (Fig. 3) and w h i h are arranged obliquely in a dorso-ventral direction. The dorsal most cell group of the four is the dorsal vagal nucleus, which is situated immediately below the floor of the fourth ventricle and laterally to the dorsal median sulcus (Fig. 1 a, b). Immediately below this nucleus is located the second cell group, which is the hypoglossal nucleus in question (Figs. 1, 3). We regard the remaining two cell groups collectively as the Nuclei cervicales (see discussion) for convenience sake (Fig. 1 a, b, c).
Fig. 2 a, b. Transverse seaions through the medulla oblongata which show the hypoglossal nucleus, including severely chromatolytic cells, in a fowl 10 days after transection of the hypoglossal neme stem. Kliiver a n d Barrera. a: ( X 40), b: ( X 100) Fig. 3. Transverse section through the medulla oblongata near the obex showing the normil cyroarchitecture of the hypoglossal nucleus. Kliiver and Barrera. ( x 100)
327
Further Studies on the Hypoglossal Nucleus in the Fowl
2 . Topography of the normal nucleus In transverse sections cut near the obex, the hypoglossal nucleus was elliptical in shape (Fig. 1 b) and 300 !im. in maximum width on the average of 33 birds, including both intact and operated ones. It became very narrow toward both extremities (Fig. 1 a, c). It was situated dorso-laterally to the central canal in a portion caudal to the obex (Fig. 1 c) and in the dorso-medial periphery of the reticular formation in the rostral portion (Fig. 1 a). This slender cell column was 1300 pm. in average length (ranging from 660 to 1750 ,urn.) in the portion rostral to the obex and 1200 pm. in average length (ranging from 600 to 1680 ,urn.) in the portion caudal to the obex when determined in the 33 birds. The hypoglossal nucleus consisted of both large and medium-sized multipolar cells filling the whole cell column. The cytoplasm of these cells was almost entirely filled with massive Nissl granules (Fig. 3). Many chromophilic cells were usually scattered all over the cell column. One to 10 cells could be observed in a transverse section of the nucleus cut near the obex. The total cell count was 379.7 (ranging from 128 to 755) and 319.9 (ranging from 135 to 510) on the average of the 33 birds in the rostral and caudal portion, respectively. The main part of the nucleus was in the portion just caudal to the obex. 3. Experimental results a } Trunsecfion of the hypoglossal nerve s f e m
This operation was carried out near the dichotomy of the hypoglossal nerve on the right side. Significant retrograde cellular degeneration was observed in the entire hypoglossal nucleus. Degenerated cells were distributed mainly near the obex in 13 of 24 operated birds (Fig. 2 a, b). In the 13 birds used, severe chromatolysis was present in a t least 1 O / o of the cells in the cell column. There was, however, considerable variation in the incidence of chromatolytic cells among these birds. The average percentage of chromatolytic cells of the total cell population of this cell column was 38.01 O / o (ranging from 1.0 to 63.6 O/o) (Table 2j. N o chrornatolytic cells were observed in the Nuclei cervicales. b} Transection of the laryngolinguul branch
This operation was carried out at a level just superior and distal to the dichotomy of the hypoglossal nerve in the birds. Severely chrornatolytic cells were observed in all parts of the hypoglossal nucleus. They were distributed
~
N ~ of, FOWL
ST
NO.*
sections observed
13
265 - 359)
I189 LL
281
7 1231
SL
5
-
37L)
281 (256 - 302)
Left hypoglossal nucleus Normal cells
6Ll
Affected cells
0
(330 - 978)
6L8 IL02 - 9L31
0
538
0
I367
-
6221
Right hypoglossal nucleus Normal cells
Affected cells
L97 (295 - 920)
I9
621 (312 - 97L)
I 7
52L (323 - 7101
*/. of cells
178 38.01 - 613) (1.02 - 63.6 1 33
52
(16 -
5.9 9L)
10.7
- 17.6 1
9.0 103) (2.2 - 18.L71
328
Fig. 4. Transverse section through the rostra1 portion of the degenerated hypoglossal nucleus in a fowl 10 days after transection of the laryngolingual bran&. Chromatolytic cells are confined to the hypoglossal nucleus. Kluver and Barrera. ( X 40) Fig. 5. Transverse section through the caudal portion of the degenerated hypoglossal nucleus in a fowl 10 days after transection of the superior laryngeal branch. Chromatolytic cells are confined to the hypoglossal nucleus. Kliiver and Barrera. ( X 40)
Further Studies on the Hypoglossal Nucleus in the Fowl
329
especially densely near the obex in 7 of the 10 operated birds (Fig. 4). The percentage of chromatolytic cells of the total cell population of this column ranged from 0.7 to 17.6 O/o (4.9 O/o on the average) (Table 2). The distribution of chromatolytic cells was nearly the same in birds in which the laryngolingual branch had been cut as in birds with the hypoglossal nerve stem removed. The percentage of chromatolytic cells, however, was much lower in the former group than in the latter group. No mromatolytic cells were found in the Nuclei cervicales of any operated birds. c ) Transection of the superior laryngeal bran&
This operation was carried out at a level just inferior and distal to the dichotomy of the hypoglossal nerve in 8 birds. The severely chromatolytic cells were noticed frequently in the portion just caudal to the obex in five of the eight operated birds (Fi 5). The percentage of chromatolytic cells of the total cell population of t is group ranged from 2.2 to 18.5 O/o (9.0 O/o on the average) (Table 2 ) . The incidence of chromatolysis was frequently high in the portion caudal to the obex. It is clearly possible that the origin of the superior laryngeal branch lies in the portion caudal to the obex. The Nuclei cervicales showed no retrograde degeneration in any bird after this operation.
fl.
d ) Transection of the syringeal branch
WATANABE (1964) showed that the syringeal branch, which is a terminal branch of the Ramus laryngeus superior, ran down in the lateral tracheal muscle near the syrinx and that it also supplied the sternotracheal muscle. This syringeal branch corresponded to the R. cervicalis descendens superior of CORDS(1903). The transection of this branch was carried out bilaterally at the distal level of the syringeal branch in the lower cervical part in 4 birds. Severely chromatolytic cells were found near the level of the obex and most frequently in the caudal portion in one of the four birds (Figs. 6, 7). The percentage of chromatolytic cells to the total cell population of the cell column was 3.1 O/o on the left side and 0.9 O/o on the right side. The distribution of chromatolytic cells showed nearly the same tendency in these four birds as in the birds in which the superior laryngeal branch had been removed. The percentage of chromatolytic cells, however, was much lower in the former than in the latter. e) Transection of the anastornosing brand between the first cervical and the hypoglossal nerve
WATANABE (1964) showed that the hypoglossal nerve received an anastomosing branch from the first cervical nerve between the lateral and ventral rectus capitis muscle. To determine from which nucleus this anastornosing branch arose, the transection of the branch was carried out between the two cervical muscles mentioned above in 5 birds. N o chromatolytic cells were observed in any nucleus. Thus, the origin of this anastornosing branch remains unknown. Fig. 6. Transverse section through the caudal portion of the degenerated hypoglossal nucleus in a fowl 10 days after bilateral transection of the syringeal brand. A dromatolytic cell (arrow) is in the left hypoglossal nucleus. Kliiver and Barrera. ( X 40) Fig. 7. Transverse section through the rostra1 portion of the degenerated hypoglossal nucleus in the same fowl as shown in Fig. 6. A dvomatolytic cell is in the right hypoglossal nucleus. Kliiver and Barrera. ( X 40)
3 30
WATANABE, IWATAand YAWDA f ) A single or combined transection of some upper cervical nerves
This operation was carried out in the upper cervical part in the following four ways: (1) both first and second cervical nerves t o the cervical biventer muscle. (2) both nerves to the complex muscle and third cervical nerve t o the cutaneous muscle, (3) both nerves to the complex muscle only, and (4) both third and fourth cervical nerves to the cutaneous muscle in the occipital part. The Nuclei cervicales showed no retrograde degeneration in any birds after operation. Therefore, the relationship between the Nuclei cervicales and the hypoglossal nerve remains unknown in the fowl. Discussion KOSAKA/YAGITA ( 1 903), GROEBBELS (1922) and GOLLER(1969) had asserted that the hypoglossal nerve arose from one nucleus on the fowl. Recent(1971) demonstrated by his experiments that the hypoglossal ly HILLEBRAND nerve arose from one nucleus in the turkey, duck and goose, and that the hypoglossal nucleus came in contact with the dorsal vagal nucleus in the first two species of birds. The present experiment on the fowl show that the hypoglossal nerve arises from one nucleus which is distant from the dorsal vagal nucleus. These results are in accord with those obtained by KOSAKA/ YAGITA(1903), GROEBBELS (1922), GOLLER (1969) and HILLEBRAND (1971). It is very interesting to note that the same results were obtained by two previous authors who had used the retrograde degeneration method (KOSAKA/ YAGITA,1903 and GROEBBELS, 1922). The Nucleus residualis of GOLLER (1969) or Nuclei cervicales, which includes the ventral hypoglossal nucleus of BRANDIS(1593) and many other authors (ARIENSKAPPERS,1911; SINN,1913; BOK, 1915; ADDENS,1933; BARNARD, 1940; and JUNGHERR, 1969), showed no retrograde cellular cfianges in the present study following transection of the hypoglossal nerve. This result leads to the conclusion that these nuclei are not related to the hypoglossal nerve in the fowl. (1893) and other authors that there are two or The opinion of BRANDIS three nuclei for the hypoglossal nerve is based on their embryological and comparative morphological studies, but is not supported by experimental evidencc. It must be considered, however, that there is an opinion that the origin of the hypoglossal nerve is widely developed in such birds as the parrot which have the well-developed tongue musculature (BLACK,1922; SANDERS,1929). The reason why the percentage of chromatolytic cells of the total cell population was so different among the fowls examined and that why unaffected cells were observed after the transection of the projective nerve have not sufficiently been discussed and clarified. It is presumed that these reasons may depend upon the following possibilities: (1) There may be collaterals for the axon of each neuron. (2) There may be some nerve cells other than those affected with the transection of their nerve fibers. (3) Some cells may appear too early or too late in the cycle of change to show any undeniable sign of retrograde degeneration even at the time of maximal chromatolysis. As another reason, it is possible to consider that the hypoglossal nucleus may also include the origin of the vagal nerve. If this assumption were true, the nomenclature Nucleus intermedius of BRANDIS(1893), ARIENSKAPPERS (1911, 1912) and other authors would be suitable for this cell column. In fact, we have some unpublished observations that a few chromatolytic cells are present in the hypoglossal nucleus after the transection of the pharyngolaryngeal branch of the vagal nerve. Further studies are needed on the cyto-
Further Studies on the Hypoglossal Nucleus in the Fowl
331
architectonic relationship between Nucleus nervi hypoglossi and Nucleus intermedius to elucidate the reason why chromatolytic cells occur in the hypoglossal nucleus after the rransection of a branch of the vagal nerve. The present studies reveal that there is only an ipsilateral relationship between the origin and its projective nerve, and thus it is not probable that there are central crossing fibers of the hypoglossal nerve root in the medulla oblongata, as described by KOCH(1 888). To determine the relationship between the center and its peripheral nerve for the Nuclei cervicales, different experimental transections were also done in various cervical spinal nerves. N o chromatolytic cells, however, were observed in the Nuclei cervicales. It is presumed that these nuclei may project their axons into the ventral or deeper musculature of the upper cervical part.
Summary The delineation of the fowl’s hypoglossal nucleus was determined by severing the hypoglossal nerve or its branches and observing retrograde degeneration. Birds were killed 7 or 10 days after surgery, the brains embedded in paraffin and cut at 10 pm. Transection of the hypoglossal nerve stem resulted in chromatolysis near the obex and no chromatolysis was found in the Nuclei cervicales. Severing of the laryngolingual branch led to degeneration phenomena near the obex nearly similar to the degeneration observed after severing of the hypoglossal nerve stem. Cutting of the superior laryngeal branch caused a degeneration of cells caudal to the obex, and Cutting of the syringeal branch resulted in chromatolysis in about the same area. The origin of the anastomosing branch between the first cervical and hypoglossal nerve was not found because no chromatolytic cells could be detected. Similarly the cutting of several upper cervical nerves did not lead to chromatolysis in the areas we investigated. Zusammenfassung Weitere Studien des Nucleus hypoglossus beim Huhn Die Begrenzung des Nucleus hypoglossus des Huhnes wurde durch retrograde Degeneration nach Durchschneiden des N. hypoglossus oder seiner Asre bestimmt. Die Tiere wurden 7 oder 10 Tage nach dieser Durchschneidung getoret, ihre Gehirne wurden in 1O /cm d i k e Paraffinschnitte zerlegt. Durchschneiden des Hypoglossusstammes zeitigte nur Chromatolysis nahe dem Obex, nicht in den Nuclei cervicales. Durchschneiden der R. laryngolingualis ergab Degenerationserscheinungen nahe dem Obex, die den vorgenannten weitgehend glichen. Durchschneiden des R. laryngeus sup. verursachte Zelldegenerationen kaudal des Obex. In etwa derselben Gegend erfolgte Chromatolysis nach Durmschneiden des R. syringealis. Der Ursprung des R. anastomoticus zwischen erstem Halsnerven und N. hypoglossus konnre nicht gefunden werden, da keine chromatolytischen Zellen entdeckt werden konnten. Gleicherweise ergab die Durchschneidung verschiedener kranialer Halsnerven in den untersuchten Gebieten keine Chromatolysis. Resume NouveIIes recherches sur Ie noyau hypoglosse de la poule La ddirnitation du noyau hypoglosse de la Poule a CtC dCterminCe par des lCsions du nerf hypoglosse ou de ses branches et I’Ctude de la dCgCn6rescence
332
WATANABE, IWATAand YASUDA
ritrograde. Les Oiseaux furent sacrifiCs 7 i 10 jours a p r b 1’opCration et les encCphales inclus dans la paraf fine et coupCs A 10 microns. La transsection du tronc du nerf hypoglosse a provoquC une chromatolyse au voisinage de l’obex; aucune chrornatolyse n’a ktk rencontrde dans les noyaux cervicaux. La section de la branche laryngo-linguale dCterrnina un phknomhne de dCgCnCrescence prbs de I’obex i peu p r b semblable i celle observie a p r b ICsion du tronc du nerf hypoglosse. La section de la branme laryngCe sup& rieure a produit une dCgCnCrescence de cellules caudalement i l’obex et la section de la branche siryngie a entraPnC une chromatolyse B peu prds dans la meme aire. L’origine de la branche anastomotique entre le premier nerf cervical et le nerf hypoglosse n’a pu &tre dCterminCe, faute d’avoir pu ditecter des cellules en chrornatolyse. De &me, la section ou la ICsion des premiers nerfs cervicaux n’a produit aucune chromatolyse dans les aires ktudiCes.
Resumen Nuevos estudios sobre el nlicleo del nervio hipogloso en el pollo La delimitaci6n del Nucleus hypoglossus del pollo se determind mediante la degeneraci6n retrdgrada, luego de cortarse el nervio hipogloso o sus ramas. Los animales se sacrificaron 7 o 10 dias despuis y de sus cerebros, incluidos en parafina, se hicieron cortes histoldgicos de 10 pm. Cortes del tronco del nervio hipogloso produjeron cromatolisis cerca del obex, pero n6 en 10s nhcleos cervicales. A1 cortarse la rama laringo-lingual, se presentaron degeneraciones cerca del obex, muy simiIares a las anteriores. Cortes del R. laryngeus sup. resultaron con degeneraciones celulares en sentido caudal a1 obex. Aproximadamente en la misma regibn, se mostr6 cromatolisis luego de cortarse el R. syringealis. El origen de la rama anastom6tica entre el primer nervio cervical y el N. hipogloso, no pudo encontrarse porque no se descubrieron cClulas cromatoliticas. Del mismo modo, cortes de diferentes nervios cervicales craniales no resultaron con cromatolisis en las regiones estudiadas.
References ADDENS,J. L., 1933: The motor nuclei and roots of the cranial and first spinal nerves of vertebrates. I. Cyclostomens. Zschr. f. d. ges. Anat. I. Abt. ZOf, 307-410. ARIENSKAPPERS,c. u., 191 1 : in A R I ~ NKAPPERS, S HUBER and cROSBY(1960). ARIENSKAPPERS, C. U., 1912: in ARIENSKAPPERS, HUBER and C~ossY(1960). BARNARD, J. W.,1940: The hypoglossal complex of vertebrates. J. Comp. New. 72, 489524.
BLACK,D., 1922: The motor nuclei of the cerebral nerves in phylogeny. A study of the phenomena of neurobiotaxis. IV. Aves. J. Comp. Neur. 34, 233-275. BOK, S. T., 1915: Die Entwidrlung der Hirnnerveo und ihrer zentralen Bahnen. Die stimulogene Fibrilation. Folia neuro-biol. 9 , 475-565. BRANDIS, F., 1893: UntersuQun en iiber das Gehirn der Vogel. 11. Ursprung der Nerven der Medulla oblongata. Arm. mikrsk. Anat. 42, 623-649. CORDS,E., 1904: Beitrage zur Lehre vom Kopfnervensystem der Viigel. Anat. Hefte 26,
f
49-100.
GOLLER,H., 1969: Topographische Darstellung der Kerngebiete der Medulla oblongata des Huhnes (Gallus domesticus). Zbl. Vet. Med.A, 16, 257-270. F., 1922: Der Hypoglossus der Vogel. 2001. Jahrb. Abt. f. Anat. 43, 465-484. GROEBBELS, HILLEBRAND, A., 1971 : Studiu experimental $i descriptiv a1 nucleului nervului hipoglos la curcan $i gisci. Lucriri Stiinlifice, Seria C, 24, 45-56. JUNGHERI, E. L.. 1969: The neuroanaromy of the domestic fowl (Callus domesticvs). Avian Dis. Special Issue. pp. 75-76.
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KOCH,P. D.,1888: Untersuchungen uber den Ursprung und die Verbindungen des Nervus hypoglossus in der Medulla oblongata. Arch. mikr. Anat. 32, 54-71. KOSAKA, K., und K. YAGITA,1903: Experimentelle Untersuchungen iiber die Urspriinge des Nervus hypoglossus und seines absteigenden Astes. Jahrb. Psychiat. 24, 150-1 89. PAPEZ,J. W.,1929: Comparative Neurology. pp. 414-415. Hafner Publishing Co., New York. SANDERS, E. B., 1929: A consideration of certain bulbar, midbrain, and cerebellar centers and fiber tracts in birds. J. Comp. New. 49, 155-222. SINN,R., 1913: Beitrag zur Kenntnis der Medulla oblongata der Viigel. Msch. f. Psychiat. u. Neur. 33, 1-39. WATANABE, T.,1969: Comparative and topographical anatomy of the fowl. XVII. Peripheral courses of the hypoglossal, accessory and glossopharyngeal nerves. Jap. J. Vet. Sci. 26, 249-258. Address for correspondence: Dr. TOHRU WATANABE, Instructor of Veterinary Anatomy, Department of Veterinary Anatomy, Faculty of Agriculture, Nagoya University, Nagoya, 464 Japan.
(1975)
0 1975 Verlag Paul Parey, Berlin und Hamburg ISSN 0041-4294/ASTM-Coden: AHEMA 5
Department of Veterinary Anatomy, Faculty of Agriculture, Nagoya University, Nagoya, 464 japan Director: Prof. Dr. M. Yasuda
Further Studies on the Hypoglossal Nucleus in the Fowl BY
TOHRU WATANABE, NOBUO IWATA and MIKIOYASUDA With 7 figrtres
and
2 rubles
(Received for publication: December 2 , 1974)
Introduction KOCH(1888) appears to have described the avian hypoglossal nucleus for the first time. Since then, cytoarchitectonic studies on this nucleus have been performed by many investigators (BRANDIS,1893; KOSAKA/YAGITA, 1903; ARIENSKAPPERS, 1911, 1912; SINN,1913; BOK, 1915; BLACK,1922; GROEBBELS, 1922; PAPEZ,1929; SANDERS, 1929; ADDENS,1933; BARNARD, 1940; 1971). GOLLER, 1969; JUNGHERR, 1969 and HILLEBRAND, KOCH(1888) compared the hypoglossal nucleus of pigeon and duck with those of mammals, and applied the mammalian nomenclature to the avian
BRANOIS(18931
A R I ~ N SKAPPERS
KOSAKA/ YAGITA
(1903I Ventraler Vaguskcrn (gemcinschaftlichcr Vagus- Hypoglossuskern1
Hypoglossuskern
Ventraler Hypoglossusker n
Obere Vorderhorn fortsetzung
SINN (19151
Nucl. intermedius XI1 Dorsaler Hauptkern des Hypoglossus
-
Box (19151
119111
Nucl. ventralis XI1
Nucl. mot. intermedius
Ventraler Nebenkern Nucl. dors. X I 1
des Hypoglossus Nucl. ventr. X I 1
GROEBBELS(19221
AOOENS (19331
BARNARO 119L01
GOLLER(19691
JUNGHERR (19691
Nucl. XI1
Nucl. XI1 dorsalis
Nucl. dorsalis nervi XI1
Nucl. nervl hypoglossi
Nucl. hypoglossus ventralis dorsornedialis
Nucl. cerv. I
Nucl. XI1 ventralis dorsomedialis
Nucl. ventralis nervi XI1
Nucl. residualis
Nucl. hypoglossus ventralis ventro lateralis
Nucl. XI1 ventralis ventroventralis
-
21*
3 24
WATANABE, IWATA and YASUDA
nucleus. BRANDIS (1893) asserted that in many kinds of birds the hypoglossal nerve arose from two nuclei, the ventral vagal or common vagal-hypoglossal (1903) were nucleus and the ventral hypoglossal nucleus. KOSAKA/YAGITA the first to carry out an experimental histological study on the hypoglossal nucleus in birds. They confirmed by the retrograde degeneration method that the hypoglossal nerve of the fowl originated from a nucleus whim was situated immediately below the dorsai vagal nucleus and which corresponded to the dorsal hypoglossal nucleus of KOCH(1888). The descriptions given so far by many investigators as to the central origin of the hypoglossal nerve in the fowl (Table 1) may be classified into three main groups: In group I, the hypoglossal nerve arises from two or three nuclei (SINN,1913; BOK, 1915; ADDENS,1933; BARNARD,1940; JUNGHERR, 1969). In group 11, the hypoglossal nerve arises from two nuclei, the dorsal one of w h i h intermingles with the dorsal vagal nucleus and is shown as 1911, 1912; BOK, the Nucleus intermedius (BRANDIS, 1893; ARIENSKAPPERS, 1915). I n group 111, the hypoglossal nerve arises from one nucleus according (1 903), GROEBBELS (1 922), GOLLER (1969). These previous to KOSAKA/YAGITA studies show considerable disagreements. The aim of this study was to investigate morphologically the origin of the hypoglossal nerve by the retrograde degeneration method in the fowl, Gallus domesticus L., in order to elucidate the functional significance of this nerve in relation to its localization pattern. Material and Methods The brain stem of 59 mature fowls of both sexes and vnious breeds were used. The medulla oblongata was obtained from 57 fowls (1.0 to 2.5 kg. in body weight) which had been subjected to operation and sacrificed 7-10 days later and from the TWO birds which had been left intact. The 57 fowls were operated under sodium pentobarbiturate anesthesia. Transection of nerves was made unilaterally in 47 birds, and in four the nerves were cut bilaterally. Transections were carried out as follows: (1) the hypoglossal nerve stem was cut in 24 birds, (2) the laryngolingual branch was cut in 10 birds, (3) the proximal part of the superior laryngeal bran& was transected unilaterally in 8 birds and the distal part was cut bilaterally in 4 birds, (4) the bran& of the first cervical nerve anastomosin with the hypogloss31 nerve was cut in 5 birds, and (5) a single or combined transection o f s o m e upper cervical nerves was performed in 6 birds. Immediately after decapitation, the whole brain was removed and immersed in 10°/o neutral formalin for a few hours. The medulla oblongata was isolated by two transverse sections made at the level of the lower border of the cerebellar peduncle and the second cervical nerve, respectively. All the specimens were left in 10 O/o neutral formalin for a week and embedded into paraffin wax in the conventional manner. Transverse sections 10 pn. chicit were cut serially and stained with Kluver-Barrera’s lux01 fast blue-cresyl fast violet method. Gomori’s d-irorne alum hematoxylin phloxin method and carbol thionin method were used in some cases. All the Celts, of which the nucIcolus was distinct were counted.
Results Although it was only made possible by employing an experimental approach to delineate the original nucleus of the hypoglossal nerve, the results obtained are presented more expediently in synthetic fashion by discussing first the nomenclature, giving then the normal topography, and finally quoting the protocols of the retrograde cellular changes in general. 1. Nomenclature The esperimental results of this study give evidence that the central origin of the hypoglossal nerve consists of one nucleus. It seems appropriate to apply the eclectic name “Nucleus nervi hypoglossi” to this origin. In a trans-
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325
c
Fig. 1 a, b, C. Serial transverse sections through the medulla oblongata of a normal fowl showing the hypoglossal nucleus (XII). a: A section of a rostra1 portion 660 pm. distant from the obex. b: The level of the obex. c : A section of a caudal portion 530!tm. distant from the obex. C. Canalis centralis; Nc. Nuclei cervicales; Xd. Nucleus dorsalis n. vagi; Xv. Nucleus ventralis n. vagi; v. Ventriculus quartus. Kliiver and Barrera ( X 23)
326
WATANABE, IVATA and YASUDA
verse section of the medulla oblongata (Fig. 1 a, b, c) it is clearly possible to observe four cell groups which consist of large multipolar cells (Fig. 3) and w h i h are arranged obliquely in a dorso-ventral direction. The dorsal most cell group of the four is the dorsal vagal nucleus, which is situated immediately below the floor of the fourth ventricle and laterally to the dorsal median sulcus (Fig. 1 a, b). Immediately below this nucleus is located the second cell group, which is the hypoglossal nucleus in question (Figs. 1, 3). We regard the remaining two cell groups collectively as the Nuclei cervicales (see discussion) for convenience sake (Fig. 1 a, b, c).
Fig. 2 a, b. Transverse seaions through the medulla oblongata which show the hypoglossal nucleus, including severely chromatolytic cells, in a fowl 10 days after transection of the hypoglossal neme stem. Kliiver a n d Barrera. a: ( X 40), b: ( X 100) Fig. 3. Transverse section through the medulla oblongata near the obex showing the normil cyroarchitecture of the hypoglossal nucleus. Kliiver and Barrera. ( x 100)
327
Further Studies on the Hypoglossal Nucleus in the Fowl
2 . Topography of the normal nucleus In transverse sections cut near the obex, the hypoglossal nucleus was elliptical in shape (Fig. 1 b) and 300 !im. in maximum width on the average of 33 birds, including both intact and operated ones. It became very narrow toward both extremities (Fig. 1 a, c). It was situated dorso-laterally to the central canal in a portion caudal to the obex (Fig. 1 c) and in the dorso-medial periphery of the reticular formation in the rostral portion (Fig. 1 a). This slender cell column was 1300 pm. in average length (ranging from 660 to 1750 ,urn.) in the portion rostral to the obex and 1200 pm. in average length (ranging from 600 to 1680 ,urn.) in the portion caudal to the obex when determined in the 33 birds. The hypoglossal nucleus consisted of both large and medium-sized multipolar cells filling the whole cell column. The cytoplasm of these cells was almost entirely filled with massive Nissl granules (Fig. 3). Many chromophilic cells were usually scattered all over the cell column. One to 10 cells could be observed in a transverse section of the nucleus cut near the obex. The total cell count was 379.7 (ranging from 128 to 755) and 319.9 (ranging from 135 to 510) on the average of the 33 birds in the rostral and caudal portion, respectively. The main part of the nucleus was in the portion just caudal to the obex. 3. Experimental results a } Trunsecfion of the hypoglossal nerve s f e m
This operation was carried out near the dichotomy of the hypoglossal nerve on the right side. Significant retrograde cellular degeneration was observed in the entire hypoglossal nucleus. Degenerated cells were distributed mainly near the obex in 13 of 24 operated birds (Fig. 2 a, b). In the 13 birds used, severe chromatolysis was present in a t least 1 O / o of the cells in the cell column. There was, however, considerable variation in the incidence of chromatolytic cells among these birds. The average percentage of chromatolytic cells of the total cell population of this cell column was 38.01 O / o (ranging from 1.0 to 63.6 O/o) (Table 2j. N o chrornatolytic cells were observed in the Nuclei cervicales. b} Transection of the laryngolinguul branch
This operation was carried out at a level just superior and distal to the dichotomy of the hypoglossal nerve in the birds. Severely chrornatolytic cells were observed in all parts of the hypoglossal nucleus. They were distributed
~
N ~ of, FOWL
ST
NO.*
sections observed
13
265 - 359)
I189 LL
281
7 1231
SL
5
-
37L)
281 (256 - 302)
Left hypoglossal nucleus Normal cells
6Ll
Affected cells
0
(330 - 978)
6L8 IL02 - 9L31
0
538
0
I367
-
6221
Right hypoglossal nucleus Normal cells
Affected cells
L97 (295 - 920)
I9
621 (312 - 97L)
I 7
52L (323 - 7101
*/. of cells
178 38.01 - 613) (1.02 - 63.6 1 33
52
(16 -
5.9 9L)
10.7
- 17.6 1
9.0 103) (2.2 - 18.L71
328
Fig. 4. Transverse section through the rostra1 portion of the degenerated hypoglossal nucleus in a fowl 10 days after transection of the laryngolingual bran&. Chromatolytic cells are confined to the hypoglossal nucleus. Kluver and Barrera. ( X 40) Fig. 5. Transverse section through the caudal portion of the degenerated hypoglossal nucleus in a fowl 10 days after transection of the superior laryngeal branch. Chromatolytic cells are confined to the hypoglossal nucleus. Kliiver and Barrera. ( X 40)
Further Studies on the Hypoglossal Nucleus in the Fowl
329
especially densely near the obex in 7 of the 10 operated birds (Fig. 4). The percentage of chromatolytic cells of the total cell population of this column ranged from 0.7 to 17.6 O/o (4.9 O/o on the average) (Table 2). The distribution of chromatolytic cells was nearly the same in birds in which the laryngolingual branch had been cut as in birds with the hypoglossal nerve stem removed. The percentage of chromatolytic cells, however, was much lower in the former group than in the latter group. No mromatolytic cells were found in the Nuclei cervicales of any operated birds. c ) Transection of the superior laryngeal bran&
This operation was carried out at a level just inferior and distal to the dichotomy of the hypoglossal nerve in 8 birds. The severely chromatolytic cells were noticed frequently in the portion just caudal to the obex in five of the eight operated birds (Fi 5). The percentage of chromatolytic cells of the total cell population of t is group ranged from 2.2 to 18.5 O/o (9.0 O/o on the average) (Table 2 ) . The incidence of chromatolysis was frequently high in the portion caudal to the obex. It is clearly possible that the origin of the superior laryngeal branch lies in the portion caudal to the obex. The Nuclei cervicales showed no retrograde degeneration in any bird after this operation.
fl.
d ) Transection of the syringeal branch
WATANABE (1964) showed that the syringeal branch, which is a terminal branch of the Ramus laryngeus superior, ran down in the lateral tracheal muscle near the syrinx and that it also supplied the sternotracheal muscle. This syringeal branch corresponded to the R. cervicalis descendens superior of CORDS(1903). The transection of this branch was carried out bilaterally at the distal level of the syringeal branch in the lower cervical part in 4 birds. Severely chromatolytic cells were found near the level of the obex and most frequently in the caudal portion in one of the four birds (Figs. 6, 7). The percentage of chromatolytic cells to the total cell population of the cell column was 3.1 O/o on the left side and 0.9 O/o on the right side. The distribution of chromatolytic cells showed nearly the same tendency in these four birds as in the birds in which the superior laryngeal branch had been removed. The percentage of chromatolytic cells, however, was much lower in the former than in the latter. e) Transection of the anastornosing brand between the first cervical and the hypoglossal nerve
WATANABE (1964) showed that the hypoglossal nerve received an anastomosing branch from the first cervical nerve between the lateral and ventral rectus capitis muscle. To determine from which nucleus this anastornosing branch arose, the transection of the branch was carried out between the two cervical muscles mentioned above in 5 birds. N o chromatolytic cells were observed in any nucleus. Thus, the origin of this anastornosing branch remains unknown. Fig. 6. Transverse section through the caudal portion of the degenerated hypoglossal nucleus in a fowl 10 days after bilateral transection of the syringeal brand. A dromatolytic cell (arrow) is in the left hypoglossal nucleus. Kliiver and Barrera. ( X 40) Fig. 7. Transverse section through the rostra1 portion of the degenerated hypoglossal nucleus in the same fowl as shown in Fig. 6. A dvomatolytic cell is in the right hypoglossal nucleus. Kliiver and Barrera. ( X 40)
3 30
WATANABE, IWATAand YAWDA f ) A single or combined transection of some upper cervical nerves
This operation was carried out in the upper cervical part in the following four ways: (1) both first and second cervical nerves t o the cervical biventer muscle. (2) both nerves to the complex muscle and third cervical nerve t o the cutaneous muscle, (3) both nerves to the complex muscle only, and (4) both third and fourth cervical nerves to the cutaneous muscle in the occipital part. The Nuclei cervicales showed no retrograde degeneration in any birds after operation. Therefore, the relationship between the Nuclei cervicales and the hypoglossal nerve remains unknown in the fowl. Discussion KOSAKA/YAGITA ( 1 903), GROEBBELS (1922) and GOLLER(1969) had asserted that the hypoglossal nerve arose from one nucleus on the fowl. Recent(1971) demonstrated by his experiments that the hypoglossal ly HILLEBRAND nerve arose from one nucleus in the turkey, duck and goose, and that the hypoglossal nucleus came in contact with the dorsal vagal nucleus in the first two species of birds. The present experiment on the fowl show that the hypoglossal nerve arises from one nucleus which is distant from the dorsal vagal nucleus. These results are in accord with those obtained by KOSAKA/ YAGITA(1903), GROEBBELS (1922), GOLLER (1969) and HILLEBRAND (1971). It is very interesting to note that the same results were obtained by two previous authors who had used the retrograde degeneration method (KOSAKA/ YAGITA,1903 and GROEBBELS, 1922). The Nucleus residualis of GOLLER (1969) or Nuclei cervicales, which includes the ventral hypoglossal nucleus of BRANDIS(1593) and many other authors (ARIENSKAPPERS,1911; SINN,1913; BOK, 1915; ADDENS,1933; BARNARD, 1940; and JUNGHERR, 1969), showed no retrograde cellular cfianges in the present study following transection of the hypoglossal nerve. This result leads to the conclusion that these nuclei are not related to the hypoglossal nerve in the fowl. (1893) and other authors that there are two or The opinion of BRANDIS three nuclei for the hypoglossal nerve is based on their embryological and comparative morphological studies, but is not supported by experimental evidencc. It must be considered, however, that there is an opinion that the origin of the hypoglossal nerve is widely developed in such birds as the parrot which have the well-developed tongue musculature (BLACK,1922; SANDERS,1929). The reason why the percentage of chromatolytic cells of the total cell population was so different among the fowls examined and that why unaffected cells were observed after the transection of the projective nerve have not sufficiently been discussed and clarified. It is presumed that these reasons may depend upon the following possibilities: (1) There may be collaterals for the axon of each neuron. (2) There may be some nerve cells other than those affected with the transection of their nerve fibers. (3) Some cells may appear too early or too late in the cycle of change to show any undeniable sign of retrograde degeneration even at the time of maximal chromatolysis. As another reason, it is possible to consider that the hypoglossal nucleus may also include the origin of the vagal nerve. If this assumption were true, the nomenclature Nucleus intermedius of BRANDIS(1893), ARIENSKAPPERS (1911, 1912) and other authors would be suitable for this cell column. In fact, we have some unpublished observations that a few chromatolytic cells are present in the hypoglossal nucleus after the transection of the pharyngolaryngeal branch of the vagal nerve. Further studies are needed on the cyto-
Further Studies on the Hypoglossal Nucleus in the Fowl
331
architectonic relationship between Nucleus nervi hypoglossi and Nucleus intermedius to elucidate the reason why chromatolytic cells occur in the hypoglossal nucleus after the rransection of a branch of the vagal nerve. The present studies reveal that there is only an ipsilateral relationship between the origin and its projective nerve, and thus it is not probable that there are central crossing fibers of the hypoglossal nerve root in the medulla oblongata, as described by KOCH(1 888). To determine the relationship between the center and its peripheral nerve for the Nuclei cervicales, different experimental transections were also done in various cervical spinal nerves. N o chromatolytic cells, however, were observed in the Nuclei cervicales. It is presumed that these nuclei may project their axons into the ventral or deeper musculature of the upper cervical part.
Summary The delineation of the fowl’s hypoglossal nucleus was determined by severing the hypoglossal nerve or its branches and observing retrograde degeneration. Birds were killed 7 or 10 days after surgery, the brains embedded in paraffin and cut at 10 pm. Transection of the hypoglossal nerve stem resulted in chromatolysis near the obex and no chromatolysis was found in the Nuclei cervicales. Severing of the laryngolingual branch led to degeneration phenomena near the obex nearly similar to the degeneration observed after severing of the hypoglossal nerve stem. Cutting of the superior laryngeal branch caused a degeneration of cells caudal to the obex, and Cutting of the syringeal branch resulted in chromatolysis in about the same area. The origin of the anastomosing branch between the first cervical and hypoglossal nerve was not found because no chromatolytic cells could be detected. Similarly the cutting of several upper cervical nerves did not lead to chromatolysis in the areas we investigated. Zusammenfassung Weitere Studien des Nucleus hypoglossus beim Huhn Die Begrenzung des Nucleus hypoglossus des Huhnes wurde durch retrograde Degeneration nach Durchschneiden des N. hypoglossus oder seiner Asre bestimmt. Die Tiere wurden 7 oder 10 Tage nach dieser Durchschneidung getoret, ihre Gehirne wurden in 1O /cm d i k e Paraffinschnitte zerlegt. Durchschneiden des Hypoglossusstammes zeitigte nur Chromatolysis nahe dem Obex, nicht in den Nuclei cervicales. Durchschneiden der R. laryngolingualis ergab Degenerationserscheinungen nahe dem Obex, die den vorgenannten weitgehend glichen. Durchschneiden des R. laryngeus sup. verursachte Zelldegenerationen kaudal des Obex. In etwa derselben Gegend erfolgte Chromatolysis nach Durmschneiden des R. syringealis. Der Ursprung des R. anastomoticus zwischen erstem Halsnerven und N. hypoglossus konnre nicht gefunden werden, da keine chromatolytischen Zellen entdeckt werden konnten. Gleicherweise ergab die Durchschneidung verschiedener kranialer Halsnerven in den untersuchten Gebieten keine Chromatolysis. Resume NouveIIes recherches sur Ie noyau hypoglosse de la poule La ddirnitation du noyau hypoglosse de la Poule a CtC dCterminCe par des lCsions du nerf hypoglosse ou de ses branches et I’Ctude de la dCgCn6rescence
332
WATANABE, IWATAand YASUDA
ritrograde. Les Oiseaux furent sacrifiCs 7 i 10 jours a p r b 1’opCration et les encCphales inclus dans la paraf fine et coupCs A 10 microns. La transsection du tronc du nerf hypoglosse a provoquC une chromatolyse au voisinage de l’obex; aucune chrornatolyse n’a ktk rencontrde dans les noyaux cervicaux. La section de la branche laryngo-linguale dCterrnina un phknomhne de dCgCnCrescence prbs de I’obex i peu p r b semblable i celle observie a p r b ICsion du tronc du nerf hypoglosse. La section de la branme laryngCe sup& rieure a produit une dCgCnCrescence de cellules caudalement i l’obex et la section de la branche siryngie a entraPnC une chromatolyse B peu prds dans la meme aire. L’origine de la branche anastomotique entre le premier nerf cervical et le nerf hypoglosse n’a pu &tre dCterminCe, faute d’avoir pu ditecter des cellules en chrornatolyse. De &me, la section ou la ICsion des premiers nerfs cervicaux n’a produit aucune chromatolyse dans les aires ktudiCes.
Resumen Nuevos estudios sobre el nlicleo del nervio hipogloso en el pollo La delimitaci6n del Nucleus hypoglossus del pollo se determind mediante la degeneraci6n retrdgrada, luego de cortarse el nervio hipogloso o sus ramas. Los animales se sacrificaron 7 o 10 dias despuis y de sus cerebros, incluidos en parafina, se hicieron cortes histoldgicos de 10 pm. Cortes del tronco del nervio hipogloso produjeron cromatolisis cerca del obex, pero n6 en 10s nhcleos cervicales. A1 cortarse la rama laringo-lingual, se presentaron degeneraciones cerca del obex, muy simiIares a las anteriores. Cortes del R. laryngeus sup. resultaron con degeneraciones celulares en sentido caudal a1 obex. Aproximadamente en la misma regibn, se mostr6 cromatolisis luego de cortarse el R. syringealis. El origen de la rama anastom6tica entre el primer nervio cervical y el N. hipogloso, no pudo encontrarse porque no se descubrieron cClulas cromatoliticas. Del mismo modo, cortes de diferentes nervios cervicales craniales no resultaron con cromatolisis en las regiones estudiadas.
References ADDENS,J. L., 1933: The motor nuclei and roots of the cranial and first spinal nerves of vertebrates. I. Cyclostomens. Zschr. f. d. ges. Anat. I. Abt. ZOf, 307-410. ARIENSKAPPERS,c. u., 191 1 : in A R I ~ NKAPPERS, S HUBER and cROSBY(1960). ARIENSKAPPERS, C. U., 1912: in ARIENSKAPPERS, HUBER and C~ossY(1960). BARNARD, J. W.,1940: The hypoglossal complex of vertebrates. J. Comp. New. 72, 489524.
BLACK,D., 1922: The motor nuclei of the cerebral nerves in phylogeny. A study of the phenomena of neurobiotaxis. IV. Aves. J. Comp. Neur. 34, 233-275. BOK, S. T., 1915: Die Entwidrlung der Hirnnerveo und ihrer zentralen Bahnen. Die stimulogene Fibrilation. Folia neuro-biol. 9 , 475-565. BRANDIS, F., 1893: UntersuQun en iiber das Gehirn der Vogel. 11. Ursprung der Nerven der Medulla oblongata. Arm. mikrsk. Anat. 42, 623-649. CORDS,E., 1904: Beitrage zur Lehre vom Kopfnervensystem der Viigel. Anat. Hefte 26,
f
49-100.
GOLLER,H., 1969: Topographische Darstellung der Kerngebiete der Medulla oblongata des Huhnes (Gallus domesticus). Zbl. Vet. Med.A, 16, 257-270. F., 1922: Der Hypoglossus der Vogel. 2001. Jahrb. Abt. f. Anat. 43, 465-484. GROEBBELS, HILLEBRAND, A., 1971 : Studiu experimental $i descriptiv a1 nucleului nervului hipoglos la curcan $i gisci. Lucriri Stiinlifice, Seria C, 24, 45-56. JUNGHERI, E. L.. 1969: The neuroanaromy of the domestic fowl (Callus domesticvs). Avian Dis. Special Issue. pp. 75-76.
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KOCH,P. D.,1888: Untersuchungen uber den Ursprung und die Verbindungen des Nervus hypoglossus in der Medulla oblongata. Arch. mikr. Anat. 32, 54-71. KOSAKA, K., und K. YAGITA,1903: Experimentelle Untersuchungen iiber die Urspriinge des Nervus hypoglossus und seines absteigenden Astes. Jahrb. Psychiat. 24, 150-1 89. PAPEZ,J. W.,1929: Comparative Neurology. pp. 414-415. Hafner Publishing Co., New York. SANDERS, E. B., 1929: A consideration of certain bulbar, midbrain, and cerebellar centers and fiber tracts in birds. J. Comp. New. 49, 155-222. SINN,R., 1913: Beitrag zur Kenntnis der Medulla oblongata der Viigel. Msch. f. Psychiat. u. Neur. 33, 1-39. WATANABE, T.,1969: Comparative and topographical anatomy of the fowl. XVII. Peripheral courses of the hypoglossal, accessory and glossopharyngeal nerves. Jap. J. Vet. Sci. 26, 249-258. Address for correspondence: Dr. TOHRU WATANABE, Instructor of Veterinary Anatomy, Department of Veterinary Anatomy, Faculty of Agriculture, Nagoya University, Nagoya, 464 Japan.
