AUTHOR'S A B E T R A m OF rHIS P A P E R lELlUED BY T E E B I H L I O G R A P E I C S E R V I C E A U Q C S T 11. VARIATIONS OF THE CANALIS HYPOGLOSSI RALPH D. LILLIE F r o m the Division of A n a t o m y of the Stanford Medical School My attention was attracted to the subject of the variations of the hypoglossal canal by the discovery of a double hypoglossal canal in the dissecting room. Subsequent examination of about thirty skulls, about twenty of them European, revealed ten cases of complete division of the canal. Consultation of the ordinary reference books failed to give definite figures. So Dr. Meyer placed the collection of skulls in the anatomical museum and Indian skulls in the general museum at my disposal. Bartels ('04) found the hypoglossal canal doubled in 117 cases in 958 half skulls or in 12.2 per cent. In the seventeen varieties of skulls used by him the percentage varied from 0.0 per cent up to 27.9 per cent in Inca skulls. Weigner ('11) who examined 103 skulls in a study of the variations of the occipital bone found that the following percentages held for German skulls : Left side Clear, 62.1 per cent Incomplete or indicated division, 10.4 Complete division, 18.5 per cent Right side Clear, 59.2 per cent Indicated division, 18.5 per cent Complete division, 22.3 per cent Division into three parts was indicated in several cases. When the canal was double it was frequently divided into unequal parts so that the posterior canal was about twice the size of the anterior, or more rarely in the reverse ratio. Weigner believes that the division of the canalis hypoglossi is one of the manifestations of an occipital vertebra. Graf v. Spee ('96) notes the division of the canal and says that indications of division are almost constant in the adult but makes no mention of the character of the indications. Jaboulay and Lucy ('11) attribute the division of the canal to that of the nerve and Froriep ('11) showed 131 T H E ANATOMICAL RECORD, VOL. AUGUST, 1917 13, NO. 3 132 RALPH D. LILLIE that in the bovine embryo the hypoglossal nerve corresponds to three segmeatal nerves. Schafer and Symington in Quain’s Anatomy 111, part 2, 1909, also regard the hypoglossal nerve as representing three segmental nerves. Prentiss (’10) working on pig embryos, found eight ganglionic masses corresponding to four ganglia associated with the hypoglossal nerves as their dorsal root ganglia. These ganglia were in series between those of the vagus and of the first cervical nerves. They are interpreted as representing four hypoglossal nerves. Five or six ventral roots of the hypoglossal exist, but according to Bremer (’08) the more anterior of these represent ventral roots of the vagus and glossopharyngeal nerves. Martin (’91) working on cats, found five ganglia and five ventral roots and concluded all were hypoglossal. So it would seem that either three or four nerves exist developmentally and this could account for either three or four somites and their corresponding neural foramina and their corresponding vertebrae. Hence between tlie jugular foramen and the synchondroses petro-occipitalis and occipitosphenoidalis on one hand, and the atlas on the other, there must have existed four or five occipital vertebrae with three or four neural foramina or hypoglossal canals between them. Consequently we should expect to find traces of division of the hypoglossal canal into either three or four parts. In fact we do find such divisions. As stated above Weigner noted indications of divisions into three parts, also into two parts, the posterior of which was twice the size of the anterior. I also have seen a number of such cases. Such occurrences could be interpreted as partial or complete separation of the first hypoglossal nerve while the two following remain together. I have seen indications of division into three equal parts two of which may be completely separated. However, complete division into three parts has not been observed. McMurrich (’05) says “during the cartilaginous stage of the skull the anterior condyloid foramina are divided into three portions by two cartilaginous partitions which separate the three roots of the hypoglossal nerve,” and considers this as evidence of the existence of four fused vertebrae in the occipital bone. VARIATIONS O F THE CANALIS HYPOGLOSS1 133 These facts point toward three original hypoglossal canals. But a number of cases were observed in which the canal was completely or incompletely divided into two equal parts and in which the anterior canal showed indications of further division into two equal parts. In the light of the work of Prentiss and Bremer I must look upon such instances as an indication of division of the canal into four equal parts. Of course, it may be in this case that it is really divided into three and that the third hypoglossal nerve is larger than the others. Pokier et Charpy report cases in which the canal was divided into four parts. Professor Meyer suggested to me that some of the osseous processes observed may be secondary ossification in the dural septa extending between the fasciculi of the roots instead of remnants of arches of occipital vertebrae. Such a case was noted in No. 42, a dissecting-room specimen. In this skull the dried remains of a dural or connective tissue septum extended between two spurs on opposite sides of the foramen. Whether these spurs are to be looked upon as secondary ossifications of a dural septum or whether such septa are to be considered as unossified remnants of vertebral arches can not be decided in dried skulls. It is also probable, indeed almost certain, that in some cases these divisions are significant not of division of the nerve, but, of vascular variation. Some of the variations recorded here are unquestionably due to aberrant vessels and not to division of the nerve. I refer here to those cases in which tortuous canals leave the main canal more or less obliquely to reenter in another place in similar fashion. On the other hand a large number of these variations are in all probability due to division of the nerve, for the nerve has been observed to pass through as two separate nerves, each in a canal of its own. In the more caudal parts of the body the metamerism of nerves and vertebrae holds strictly. Metamerism of the nerves exists in the head, showing best in the embryo. Indications of bony segmentation of the canal corresponding to the nervous segmentation are also found. Moreover an occipital vertebra may be partially separated. These facts all point in the same direction. 134 RALPH D. LILLIE OBSERVATIONS 35 Indian skulls from Jersey County, Il1inoi.s Character of hypoglossal canals NUMBEE LEFT RIGHT 7615 A slight superior spur not at either opening 7613 7612 7630 Simple Simple, smaller A slight superior prominence near t h e margin Simple, round A septum a few millimeters thick a t internal opcning. The foramina equal Simple Simple, larger A slight superior tubercle a t theinner margin __ 7609 7607 7605 7608 7606 7604 7616 7618 7619 7620 7627 7626 76'5 -_ A small antero-superior spur Simple A heart shaped internal opening wit,h a prominence superior A small antero-superior notch The internal margin is rough superiorly h sept,um 3 mrn. wide by I mm. thick internally. The anterior canal is smaller than the posterior A slight superior spur Opposed spurs above and below A broad septum within canal. Anterior canal half t h e size of t h e posterior Simple A slight superior tuhercle Bimplc An inferior spinc, a flattened internal opening and a slight indication abovc a t the internal margin. Round externally A small antero-superior spur A rough superior internal margin An anterior foramen right through t o a common external opening. A larger posterior foramen giving rise t o a small anterior canal through to the common extcrnal opening and a large posterior blind pit. I n t h e external opening are three small pits abovc and posterior t o t h e two canals A small antcro-superior notch A marked internal superior spine with a n indication opposite on the lower margin. The anterior division is half the size of the posterior A projcction on t h e superior margin Two equal canals Compresscd dorso-ventrally d broad scptum within the canal. The anterior canal half the size of the posterior Simple il slight superior spur Simple VARIATIONS O F THE CANALIS HYPOGLOSSI OBSERVATIONS-Continued NUM- LEFT BER - Simple 7623 Simple 7622 Simple 7639 A superficial internal septum. Small anterior, large posterior canal 7638 A broad superficial internal septum. Anterior canal smaller Slight antero-superior spur on roof Simple Simple, larger Anterior superior spur. One t o two division Antero-superior notch Simple Simple Simple A ridge below, a spur above Simple Simple A marked superior spur Simple 7635 7634 7633 7631 7628 7632 7610 7624 7641 7640 7643 7642 - RIGHT A deep septum half the length of t h e canal. 7624 7637 135 Equal division. A slight double spur on the internal superior margin A slight spur from the roof near the internal orifice A rough superior margin internally. The medial side of the posterior condyloid canal opens into the skull posterior t o canalis hypoglossi A slight superior spur. The anterior division half the posterior Slight antero-superior notch Simple Simple, smaller Slight double superior spur Two slight superior elevations Simple Simple Simple Simple Simple Simple Simple Simple Two I n d i a n skulls from L a Conner, Washington 7645 7644 An internal septum. Anterior canal half the posterior Simple Simple Simple Three I n d i a n skulls from the Longueville graves, Plumas County, California I A superior spur IA 7648 A broad superficial inter- narrow, septum Simple 7649 nal septum Simple Simple 7647 median, superficial internal RALPH D. LILLIE OBSERVATIONS-Continued 16 I n d i a n skulls .from Ponce mound near M a y f e l d , California NUXBER E. 7650 7651 7652 7653 7654 7655 7657 7656 7660 7658 7662 7661 MI hi12 __ LEFT Simple A thin, narrow septum in the mid-portion of t h e canal Clear Spur on the sup.erior internal margin Simple Simple Simple (young, first permanent molar) Simple Simple Simple, flattened Simple A deep internal septum in inner third of canal Simple A thin, superficial internal septum. Anterior foramen half the size of the posterior Both foramina round. Septum deep i n middle third of canal. Anterior canal larger RIGHT Simple Superior tongue-like process and a slight inferior tubercle Complete septum. Anterior canal half the size of the posterior Opposed spurs on internal margin Simple A superior anterior roughening Simple Simple Simple Simple, flattened Simple Simple Simple Simple Flattened from t o p down. Five I n d i a n slculls from near S a n Jose, California M3 hIedian septum near internal foramen M4 Antero-superior spur and notch Simple, round M5 M6 117 Broad flat septum. Two internal foramina are equal. External foramen single Simple Median septum near internal foramen. Opposed spurs divide anterior canal into two Simple Opposed spines. Anterior division half posterior Basioccipital of this side is destroyed Strong superior and slight inferior spines on internal margin. Anterior division half posterior VARIATIONS OF THE CANALIS HYPOGLOSSI 137 Twelve whole skulls or entire occipital bones NUMBER LEFT RIQHT Completely divided nerve Clear. Only one hole i n dura 1 in both canals Rough superior internal Rough superior internal margin 2 margin Slight median superior Clear. (Anterior part atlas assimilated) 3 spur Clear 4 (102.) Clear Clear Antero-superior notch 5 Medium superior spur. Opposed median spurs 6 Also superior spur i n middle of anterior division Clear 7 Clear (13.) Strong septum an- Septum in middle third of canal. Ante8 terior canal 2-3 times rior canal is twice the size of the posterior as large a s posterior An anterior-superior notch Anterio-superior notch. (Occipital only) 9 Clear. (Occipital only) Clear internally. At external opening a 10 small superior canal cut off Clear Clear 11 Slight median superior C1ea.r 12 elevation. Two small orifices just above internal opening ~~ - Twenty-two European skulls IV. Clear Antero-superior cleft and spur 1 2 V. Thin median septum Thicker median septum i n middle third. i n inner third Spur in middle of Vuperior margin. Small inferior spur and opposed superior ridge i n middle of anterior canal XIII. Large and clear, Large and clear 3 posterior condyloid canal opens laterally Median superior tubercle 11. Clear 4 XV. Antero-superior ir- Antero-superior and antero-medial spurs. 5 Small canal antero-superior t o two spurs regular process 1 t o 2 mm. long Thin septum in middle Opposed elevations. Anterior part con6 third of canal. Antestricted and half the size of the posterior rior two-thirds size of posterior. ’ (6 on medial side of left mastoid) RALPH D. LILLIE OESERVATIONS-Continued NUMBER RIGHT - 16 17 XII. Opposed antcro-superior and -mrdial spurs which enclosc a sinall canal XIV. Clcar VII. A n t e r o -sii p e r i o r marginal elevation 111. Slight antcro-superior tubercle XVII. Triangular. A fossa runs hack from posterior superior corner into a small pit IX. Clear opening. A small venous canal runs antero-mcdlally from roof ncar posterior orifice t o ncar the external orifice of canal XVI. Clear VIII. Clear Heavy septum. Anterior canal small, almost slitlike. The slit points toward the condyle V. Clear 111. Clear 18 11. Strong septum in in- 7 8 9 10 11 12 13 14 15 19 20 21 22 Same a s left but cnclosed canal smaller Clear Clear Clear Antero-superior notch clear through Clear Clear Clear Clear Clear A long superior spine which almost divides the main canal into a smaller anterior canal and a larger posterior. A wide opening in the postero-lateral wall opening into the posterior condyloid canal. Clear ncr half. Anterior canal slight.ly smaller (04.) (Separate occipital) Median superior spur Clear B11. Opposed median Clear spurs, t h e superior being stronger Clear C11. Clear Clear Clear 139 VARIATIONS O F THE CANALIS HYPOGLOSSI _ _ ~ n W ; m$ SIDE LOCALITY 4 % W 9s z Illinois Indians. . . . . . . California Indians.. . . , Specimens from dissecting room .... . . . European skulls.. . . . . . Ew $ 8 4 Left Right Both n 14 17 48.6 15 15 42.9 29 32 45.7 I Left Right Both 14 16 30 56.0 66.7 61.2 I Left Right Both 31 31 62 43.7 43.7 43.7 30 31 61 Left Right Both 13 13 26 Left Right Both 75 75 150 ~~ 1 I I 1 Total.. . . . . . . , . . . . . . . . 1 Ew Em gz E2 zg 2 ~ gz u __ 2; 6 @ D. @ w i; ,", 40.0 42.9 41.4 4 5 9 11.4 14.3 12.9 35 35 70 3 12.0 5 20.8 8 16.3 8 3 11 32.0 12.5 22.4 25 24 49 42.2 43.7 42.9 10 9 19 14.1 12.7 13.4 71 71 142 59.1 59.1 59.1 5 22.7 8 36.4 13 29.5 4 1 5 18.2 4.5 11.4 22 22 44 49.0 49.3 49.1 52 33.9! 59 38.8: 111. 36.3! 26 18 44 16.99 11.84 14.43 153 152 305 ~ L'npaired series. $2 82 ai; ZE Z$ ~ ~ Fifty-nine left sides of skulls or of occipital bones f r o m cadavers dissected in the dissecting room 1. Anterior superior spine and notch. 2. Anterior superior spine and notch. 3. Clear. A small canal from the lateral wall of the canal opens behind t h e ocripital condyl. Anterior t o this are two other apparently blind small canals. 4. A superior tubercle in the middle of the internal margin and another midway between t h e first and the antero-medial internal margin. 5. Clear. 6. A strong septum with a superior spur projecting inward. The anterior canal is smaller. 7. The superior wall of the canal is destroyed, the remainder appears clear. 8. A strong superior spur internally. The anterior division i s half the posterior. 9. Clear. 10. A small superior elevation between anterior and middle thirds of the internal margin. 11. Clear. 12. Large. Rough superior and antero-medial margin. 13. (13L.) A strong complete septum clear through t o the external opening. The antcrior canal is half the posterior. A canal from the postero-lateral 140 RALPH D. LILLIE wall of the posterior canal opens into the medial side of the posterior condyloid canal. Anterior canal has marked anterior construction. From anterior opening the anterior canal has marked superior diverticulum which communicates with top of posterior canal. Latter has smaller anterior opening. 14. Clear. 15. Large, clear. 16. Posterior condyloid canal opens just posterior t o posterior internal margin. The internal orifice had slight antero-superior notch. Opposed superior and inferior ridges near the external orifice divide t h e canal evenly. 17. Antero-superior cleft. 18. Clear. One pit i n superior, another i n postero-lateral wall of t h e canal. 19. Rough superior margin. A small vascular canal goes laterally then forward from the posterior internal margin and reenters the canal a t the external orifice. 20. Afitero-superior cleft internally. 21. The superior wall is destroyed. Rest clear. 22. Strong median superior spine internally. 23. Small antero-superior cleft. 24. Clear. 25. Clear. 26. Clear. 27. (27L.) A strong internal septum divides t h e canal equally. The internal orificc of the posterior canal is much larger. A wide postero-lateral opening into the posterior rondyloid canal and a large superior diverticnlum opening posteriorly and internally. The internal opening of the anterior canal has a sharp spine from the antero-medial wall with a deep cleft below. A superior diverticulum from the conimon external opening. 28. Clear. 29. Clear Slight antero-medial constriction. 30. A septum in the outer t,hird or half of t h e canal. The posterior canal is half the anterior. 31. Antero-medial or -superior notch. 32. Large. Antero-medial notch. Posterior condyloid canal has opening into postero-lateral wall. 33. Opposed spurs. Anterior division is half or third the size of t h e posterior. 34. Antero-superior spur. 35. (35L.) Internally a n antero-superior spur has bridged t h e canal completely, cut,ting off a small sntero-superior canal which has a median superior spur t h a t makes it U-shaped. 36. Rough superior margin. Anterior constriction. Two small canals from postero-superior wall probably t o the posterior condyloid canal. 37. Clear. 38. Clear. 39. Antero-superior notch. Canal from postero-superior internal margin probably t o posterior condyloid canal. 40. Clear. 41. Median and anterior superior notches. 42. Clear. VARIATIONS OF THE CANALIS HYPOGLOSSI 141 43. Clear. 44. Clear. 45. Internal superior marginal spur, between middle and posterior thirds. 46. Clear. 47. Antero-superior spur. 48. Antero-medial tubercle. 49. A superior spine and a n opposed inferior elevation. Almost complete division, so t h a t the posterior division is one and half times the size of the anterior division. 50. Antero-superior internal notch includes a small spine and opposed spines i n the middle of the canal dividing i t equally into postero-superior and anteroinferior parts. 51. Antero-superior notch. 52. Opposed spurs. Anterior canal smaller. 53. Clear. 54 Median superior notch. 55. Strong median septum. 56. Opposed spines-superior longer. Anterior c'anal smaller. 57. Clear. 58. Clear. Only one hole in dura mater. 59. Large. Strong slightly anterior septum in middle third of canal. Fifty-nine right hnlves I. Antero-superior cleft. 2. Thin septum which is incomplete a t the inner opening. Anterior canal smaller with further anterior notch. 3. Flattened from above down. An indicated spur in the middle of the superior internal margin. Anterior half of orifice especially flattened. External orifice rounded. 4. Superior median elevation and a n anterior superior spur with a n opposed inferior elevation. 5. Narrow septum. Anterior canal smaller. 6. Clear. 7. Clear. 8. Rough superior margin. Elevation between anterior and middle thirds of superior internal margin. 9. Antero-superior notch. 10. Constricted anteriorly. 11. Strong septum with superior internal spur. Equal canals. 12. Clear. 13. Small antero-superior cleft. 14. Opposed spurs which separate the anterior third of the canal. I n addition there is a n antero-medial spur. 15. Clear. 16. Greatly flattened. Median spur within the canal on its roof. 17. Clear. Flattened. 142 RALPH D. LILLIE 18. (I8R.) Large oval inner orifice. At the outer orifice a thin strand of bone divides off a smaller posterior division. Postero-lateral t o this is a pocket opening back and inward with a round hole 1 mm. i n diameter i n the middle which opens through into the external orifice and a pit 2 m r n . in diameter above, which opens anteriorly into a large superior diverticulum from the anterior canal. 19. Median superior spine. 20. Clear. Large canal from posterior wall to posterior condyloid canal. 21. Clear. 22. Clear. 23. Antero-supcrior spur and notch. 24. Strong septum. Anterior canal smaller. Common external opening has superior diverticulum. 25. Slight spur internally on upper third of antero-medial margin. 26. Clear. 27. Superior spur on inner margin posterior division half the size of t h e ant,erior. 28. Clear. 29. Antero-superior spur and notch. 30. Clear. Foramen magnum and condyle malformed. 31. Clear. 32. 1,argc internal opening clear. A canal starts off from the middle of the postero-superior wall opening separately a t outer opening. An antcro-medial notch. Antero-superior diverticulum i n middle of canal. 33. Clear. 34. Slight. opposed elevations anteriorly o n inner margin. Inferior elevation stronger. 35. Large. Clear. 36. Large. Opposed spurs between anterior and middle thirds. 37. Clear. 38. Large. Antero-superior spur. 39. Slight ant,erior superior eminence between anterior and middle thirds. 40. Clear. 41. Clear. 42. Opposed elcvations and dried remains of a connective tissue septum. Ant,erior canal half posterior. 43. Slight superior spur between anterior and middle thirds of internal margin. 44. Median and anterior superior spurs with slight opposed inferior ridges. A small canal from anterior superior corner returns by a curved course to superior wall near external orifice. 45. (IV.) Antero-superior notch. 46. Two superior internal spurs equally spaced with a n anterior medial spur opposed t o the anterior superior spur. A canal from posterior wall probably t o posterior condyloid ca.naI. 47. An anterior c~onstriction. 48. Sniell 1 t o 1.5 mm. round notch o n antero-medial internal margin which is set off by two spurs. 49. Antero-supcrior notch. VARIATIONS O F T H E CANALIS HYPOGLOSSI 143 50. Median superior tubercle. 51. (5llt.) Strong horizontal septum. Smallcr inferior, larger superior ranal. 52. Large. Clear. 53. Septum i n internal part of canal not quite t o inner orifice. Anterior canal half the size of the posterior. 54. A complete thin, 2 mm. wide, supcrficial internal septum. Anterior canal slightly smaller. 55. Two equally spaced superior internal tubercles. Antero-inferior spur opposes anterior one. 56. Anteriorly constricted internal opening. 57. Clear. 58. Clear. 59. Clear Although the number of skulls from different groups or types was too small for a comprehensive view, the above table indicates a variation in the frequency of division among the different racial types. This was also found t o be true by Bartels ('04). Complete division shows itself in the Illinois Indians in only 12.9 per cent of the cases, while in the California Indians it was seen in 22.4 per cent. In the dissecting room specimens and in the European skulls the incidence was 13.4 per cent and 11.4 per cent respectively. Distinct differences between the right and left sides exist. Complete division is more frequent on the left side-16.99 per cent as against 11.84 per cent-while indicated division is more common on the right-38.82 per cent as compared with 33.99 per cent. The canal is clear in an equal number of cases on each side. Racial differences seem to be indicated here, too. In the Illinois Indian skulls and in those from our dissecting room there is practically no difference between the two sides, but in the California Indians and in the European skulls decided differences were found. The canal is clear in an equal unmber of cases on both sides This agrees very well with Weigner's ('11) who found the canal clear in 62.1 per cent of the skulls on the left and in 59.2 per cent on the right. I find 49.02 per cent on the left and 49.34 per cent on the right. Weigner found indicated division in 19.4 per cent on the left and in 18.5 per cent on the right-practi- 144 RALPH D. LILLIE cally in equal numbers in 103 skulls. I find 33.99 per cent and 38.82 per cent for the left and right sides respectively. Complete division of the canal was present on the left in 18.5 per cent and on the right in 22.3 per cent of Weigner’s specimens, but in only 17.0 per cent on the left and in 11.8 per cent on the right side in my series. Frequently in cases of complete or indicated divisions the two canals are unequal, one being about twice the size of the other. The anterior usually is the smaller. Indications of further division of the larger of the two canals occurs in a few cases. The two canals are often equal in size. In the latter case some few examples of further indicated division of the anterior canal were seen. From the variations in form of the hypoglossal canal in adult skulls I am unable to decide whether there were three or four hypoglossal canals developmentally. I take pleasure in thanking Professor Meyer for his assistance and suggestions. LITERATURE C I T E D BARTELS,P. 1904 TJbcr Rasseniinterscheide am Schadel I. Intern Monschr. f . Anat. u. Physiol. Bd. 21. BREMER,J. 1,. 1908 Aberrant roots and branches of the abducent and hypoglossal nerves. Jour. Comp. Neur. Psychol., vol. 18. FRORIEP1911 Poirier e t Charpy. Tr. d’anat. hum. Tome 1, Paris. JAHoULAY ET LUCY 1911 Poirier e t Charpy. Tr. d’anat. hum. Tome 1, Paris. :MARTIN 1891 Die Entwickelung der neunten bis ewolften Kopfnerven bei der Katee. Anat. Am. Bd. 6. J. P. 1905 The development of the human body. Phila. MCMURRICH, POIRIERE T CHARPY 1911 Trait6 d’Anatomie humaine. Tome 1, Paris. PRENTISS,C . W. 1910 The development of t h e hypoglossal ganglia of pig embryos. Jour. Comp. Ncur. Psychol., vol. 20. QCHAFER AND SYMINGTON1909 Quain’s Anat., vol. 3, p t . 2. 11th ed. London. GRAF VON SPEE 1896 Bardeleben Handb. d. Anat. d. Menschen. Bd. 1, Abth. 2. WEIONER, K. 1911 o b e r dic Assimilation des Atlas und uber die Variationen am 0 s occipitale beim Menschen. Anat. Hefte Bd. 45.