International Journal of Osteoarchaeology

Int. J. Osteoarchaeol. 15: 140–145 (2005)

Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/oa.738

SHORT REPORT

Variations in the BridgingTrait of the

Hypoglossal Canal in13th Century
Byzantine Skulls
I. ARI*, M. A. KURT, I. H. OYGUCU AND E. SENDEMIR
Department of Anatomy, Uludag University, School of Medicine, 16059, Bursa, Turkey

ABSTRACT The presence of a bony bridge in the (bridging trait) hypoglossal canal, with five different
modes, was investigated in 25 adult male Byzantine (13th century) skulls. First, we re-
evaluated the viability of proposed classification schemes, then for the first time, provided
information on the structural features of this part of the occipital bone in a population of Asia
Minor. Analysis of the data revealed minor differences in the Byzantine population compared
to those previously investigated. Diverse geographical sources may be beneficial in under-
standing the role of developmental and genetic factors in bridging trait. Copyright ß 2005
John Wiley & Sons, Ltd.

Key words: hypoglossal canal; bridging trait; population differences

Introduction Variations in the form of the hypoglossal canal

The hypoglossal canal, which starts internally a
little above the anterolateral part of the for-
amen magnum and continues anterolaterally, is
located above the occipital condyles of the
occipital bone. Apart from the hypoglossal nerve,
the hypoglossal canal contains a meni-
ngeal branch of the ascending pharyngeal artery
and an emissary vein from the basilar plexus
(Williams et al., 1989).
Variations in the shape of the hypoglossal canal
may be crucial for neuroradiologists and neurosur-
geons, since primary neoplasms (Smith et al., 1995,
Myatt et al., 1998) such as hypoglossal schwanno-
mas, as well as vascular anomalies such as enlarged
emissary veins (Shiozawa et al., 1996) and persistent
primitive hypoglossal artery (De Caro et al., 1995),
which are extremely rare, still bear a certain risk
for surgical procedures.
* Correspondence to: Department of Anatomy, Uludag University,
School of Medicine, 16059 Bursa, Turkey. e-mail: iari@uludag.edu.tr
Copyright # 2005 John Wiley & Sons, Ltd.
have been widely studied, yielding substantial
descriptive and evolutionary information (Hori,
1925; Ishida & Dodo, 1997; Lang et al., 1983;
Schmidt, 1975). Particular interest has been
paid to division of the canal by either a bony
bridge or a septum, which supports Hauser and
De Stefano’s (1985) theory. This theory suggests
that the basioccipital bone is formed by fusion of
three or four formerly separated vertebrae and
the canal itself reflects amalgamation of interver-
tebral foramina.
Understanding embryological development of
the hypoglossal canal and nerve is crucial in the
perception of different types of variations in the
bridging trait of the canal. An embryo can be
characterized by its age, size or developmental
stage (Drews, 1995). Streeter (1942) and
O’Rahilly and Müller (1984) have described
stages for human embryonic development, which
divides this period into 23 stages. The stages of
this description coincide with the following
embryonic ages; stage 1–3 ‘first week’, stage 4, 5
Received 6 November 2002
Revised 12 May 2003
Accepted 5 January 2004
Bridging Trait of the Hypoglossal Canal
‘second week’, stage 6–9 ‘third week’, stage 10–13
‘fourth week’ and finally stage 14–23 ‘5 to 8th
weeks’. An embryo has been described to consist
of 25–29 pairs of somites and four somites situ-
ated rostral to the first cervical nerve are
designated as occipital somites. Occipital scler-
otomes, which are constituted by some of the
somatic cells, were found to arise from each of
the four occipital somites, initially forming a
continous column on each side at stage 13.
Each column then becomes subdivided into a
rostral and a caudal part, and the right and left
caudal portions unite in the median plane at stage
14. The caudalmost root of the hypoglossal
nerve and the hypoglossal artery pass between
these two parts. Thus, morphology of the hypo-
glossal canal, which is situated rostral to caudal
part of the column, is closely related to (1) the
process of occipital condrification that is
reported to occur at stage 17 and (2) the devel-
opment of the hypoglossal nerve. Since, the
hypoglossal nerve roots become very closely
arranged by stage 17, a persistent septum in the
hypoglossal canal would have to develop prior to
that stage. Therefore, the presence and type of
hypoglossal canal briding are connected to the
appearance of first hypoglossal nerve fibres,
their subsequent development into roots and
their incorporation in to the hypoglossal foramen
as well as the loss of material between the roots
during hypoglossal canal development (O’Rahilly
& Müller, 1984).
Bridging has also been considered as a varia-
tion, a discrete cranial trait and included among
epigenetic characters in physical anthropological
studies (Berry, 1975; Corruccini, 1974; Ossenberg,
1970; Rösing, 1982). Bastianini et al., (1985) and
Hauser and De Stefano (1985) have developed
schemes to classify the modes of hypoglossal
canal division. We applied these schemes to
find the incidence of hypoglossal bridging trait
in Byzantine skulls.
Material and Method
A total of 25 adult male skulls, which were
excavated from a Byzantine (13th century)
burial site near Iznik (Nicaea), Turkey, were
studied. The mean age at death was calculated
Copyright # 2005 John Wiley & Sons, Ltd.
141
as approximately 35 years; these individuals were
thought to have been killed during a battle
(Ozbek, 1984).
Variations of division of the hypoglossal canal
have been classified into five types, which indi-
cate increasing completeness of bridging (Fig. 1),
based on the classification of Hauser and De
Stefano (1985).
The numbers of each expression were recorded
and the
2 test was used to compare their later-
alization frequencies. Our data were further com-
pared to those reported in other populations using
the binomial test.
Results
The incidence of different hypoglossal canal types,
classified according to their bridging traits, is pre-
sented in Table 1. On these skulls, the type 2
hypoglossal canal, that expresses only one osseous,
spine and the type 1 hypoglossal canal that
expresses no trace of division, occurred most fre-
quently (42 and 38%, respectively). Type 3 mode of
expression, however, was found on only one (left)
hypoglossal canal. A total of five (10%) type 4 and,
four (8%) type 5 hypoglossal canal bridging modes
were further observed on these crania.
When the data were analysed with respect to
their localization (Table 1) type 1 expression was
more frequent on the right side than on the left
(12 versus 7). Type 4 expression mode, on the
other hand, was found to be more frequent on the
left side (4 versus 1). However, statistical analysis
did reveal significant differences between the two
sides, with regard to the above two, as well as for
the other modes of expression (p < 0.05), when
the two sides were compared individually for
each type.
When the data were reclassified according to
its presence or absence (Table 2); nine (18%) out
of 50 hypoglossal canal were found to be
bridged. Six (12%) bridges were on the left and
three (6%) were on the right side (Table 2); only
one skull had bilateral bridging.
Comparisons with previous series have been
made by pooling expression scores of types
1 þ 2 þ 3 as distinct from 4 þ 5, which corresponds
to the threshold set by Berry and Berry (1967). No
significant difference was found between the data
Int. J. Osteoarchaeol. 15: 140–145 (2005)
142 I. Ari et al.

Figure 1. Types of hypoglossal canals: (a) a simple canal; (b) an osseous spine at either the outer or inner orifice of the canal; (c) two or
more osseous spines anywhere along the walls of the canal; (d) complete osseous hypoglossal bridging in the internal or external
part of the canal; and (e) complete osseous hypoglossal bridging along the whole canal. Arrows denote osseous spines and osseous
hypoglossal bridging.

obtained from the Byzantine series and those from
the previous studies (Table 3).
Discussion
Variations in the formation of the hypoglossal
canal have been studied in different populations
Copyright # 2005 John Wiley & Sons, Ltd.
(Spee, 1896; Hori, 1925; Hyrtl, 1859; Ishida &
Dodo, 1997; Lang et al., 1983; Lillie, 1917; Piffer
& Zorzetto, 1982; Weigner, 1911). This study
is the first to investigate the topographical
and structural features of this part of the occipital
bone, in a population inhabited in Asia Minor.
When the results were compared to those of
previous less systematic studies, which considered
Int. J. Osteoarchaeol. 15: 140–145 (2005)
Bridging Trait of the Hypoglossal Canal 143
Table1. The distributionof hypoglossal canal types on rightand supremacy of type 2 expression appears to be due
left sides of the Byzantine skulls
to the increased incidence of this type on the left
Left Right Total side, since type 1 expression occurred more
n (%) n (%) n (%) frequently on the right side (see Table 1). This
Type1 7 (14) 12 (24) 19 (38)
discrepancy observed in the Byzantine popula-
Type 2 11 (22) 10 (20) 21 (42) tion is unlikely to be due to a sex bias, since no
Type 3 1 (2)
1 (2) significant sex differences were found within the
Type 4 4 (8) 1 (2) 5 (10) same population (Bastianini et al., 1985). The
Type 5 2 (4) 2 (4) 4 (8)
existence of genetic factors in the expression of
Total 25 (50) 25 (50) 50 (100)
the bridging trait should also be considered.
Bridging of the hypoglossal canal has been
suggested to occur as a developmental feature
Table 2. The absence (types 1 þ 2 þ 3) and presence (types (O’Rahilly & Müller, 1984), and has been used
4 þ 5) of the hypoglossal canal bridging trait effectively as an ‘epigenetic character’ in anthro-
pological studies (Berry, 1975; Corruccini, 1974;
Left Right Total
n (%) n (%) n (%) Ossenberg, 1970; Perizonius 1979a,b).
In accordence with the previous studies, no
Absence (Type1, 2, 3) 19 (38) 22 (44) 41 (82) side dimorphism was found except the slight
Presence (Type 4, 5) 6 (12) 3 (6) 9 (18)
tendency for type 1 canals to be expressed
Total 25 (50) 25 (50) 50 (100) more frequently on the right side and for type 4
canals on the left (Table 1).
The partial influence of age-dependent
the expression scores 1 þ 2 þ 3 and 4 þ 5 as the changes has been postulated as a factor in the
existence of bridging trait, no significant differ- formation of certain modes of bipartition of this
ence was found. However, when compared with canal (Buikstra, 1972; Cheverud & Buikstra, 1981;
studies whose methodology was based on the Corruccini, 1974; Ossenberg, 1970). After sub-
scheme proposed by Hauser and De Stefano dividing 300 Sienese skulls into two age groups
(1985), subtle differences for the Byzantine popu- (<36 and 37–80 years), Bastianini et al., (1985)
lation were noticed. Hauser and De Stefano observed a substantial increase in the frequency
(1985) found that type 1 mode was the most of types 4 and 5 in the older age group, and
predominant hypoglossal canal expression in higher frequency of types 2 and 3 in the younger
European, Egyptian and Peruvian populations age group. This supports the hypothesis that age
on both sides. In another study, Bastianini et al., is an important factor in determination of the
(1985) reported that the first mode of expression bridging trait. This might also well explain the
was the most frequent on both sides, and in both higher incidence of type 2 trait (42%) compared
sexes. However, in the present study, type 2 to type 4 (10%) and type 5 (8%) observed in the
mode of expression appeared to be more fre- present study, since their mean age was approxi-
quent (42%) compared to type 1 (38%). This mately 35 years (relatively young).

Table 3. The frequencies and percentages of hypoglossal bridging in different populations; (
) absence (types 1, 2, 3) and ( þ )
presence (types 4, 5) of hypoglossal canal bridging

Rome and Austria Egypt Peru Sardinia Amsterdam India Japan Sienese Byzantine

R L N (%) N (%) N (%) N (%) N (%) N (%) N (%) N (%) N (%)

86 (66.2) 46 (74.2) 48 (71.6) 81 (70.4) 130 (77.8) 28 (80.0) 187 (83.1) 203 (67.6) 17 (68.0)
þ
11 (8.5) 5 (8.1) 9 (13.4) 13 (11.3) 10 (6.0) 3 (8.6) 12 (5.3) 38 (12.6) 2 (8.0)

þ 23 (13.7) 8 (12.9) 6 (9.0) 10 (8.7) 16 (9.6) 3 (8.6) 21 (9.3) 41 (13.6) 5 (20.0)
þ þ 10 (7.7) 3 (4.8) 4 (6.0) 11 (9.6) 11 (6.6) 1 (2.9) 5 (2.2) 18 (6.0) 1 (4.0)
Total 130 62 67 115 167 35 225 300 25
Gender < < < <=, < < <=, <=, <

Copyright # 2005 John Wiley & Sons, Ltd. Int. J. Osteoarchaeol. 15: 140–145 (2005)
144
Considering the embryonic developmental
process, O’Rahilly and Müller (1984) investi-
gated the early development of the hypoglossal
nerve and canal in human embryos. They con-
cluded that morphology of the canal is inti-
mately related: 1) with the process of occipital
chondrification beginning at stage 17, and 2)
with the development of the hypoglossal
nerve, from the appearance of the first nerve
fibres to their incorporation in the hypoglossal
foramen that subsequently develops into the
canal. It is the rate and timing of these processes,
and of the opposing process of loss of material,
that determines the presence and extent of
hypoglossal canal bridging, established before
stage 17. Thus, examination of additional cra-
nial series from diverse geographical sources
is still needed to strengthen the role of embryo-
nic development and genetic factors in this
bridging trait.
References
Bastianini A, Guidotti A, Hauser G, De Stefano GF.
1985. Variations in the method of the division of
the hypoglossal canal in Sienese skulls of known
age and sex. Acta Anatomica 123: 21–24.
Berry AC. 1975. Factors affecting the incidence of
nonmetrical skeletal variants. Journal of Anatomy
120: 519–535.
Berry AC, Berry RJ. 1967. Epigenetic variation in
the human cranium. Journal of Anatomy 101: 361–
379.
Buikstra J. 1972. Techniques for coping with age-
regressive nature of nonmetric traits. American Jour-
nal of Physical Anthropology 37: 431–432.
Cheverud JM, Buikstra J. 1981. Quantitative genetics
of skeletal non-metric traits in the Rhesus macaques
of Cayo Santiago I þ II. American Journal of Physical
Anthropology NS 54: 43–49, 51–58.
Corruccini RS. 1974. An examination of the meaning
of cranial discrete traits for human skeletal biologi-
cal studies. American Journal of Physical Anthropology
40: 425–446.
De Caro R, Parenti A, Munari PF. 1995. The persistent
primitive hypoglossa artery: a rare anatomic varia-
tion with frequent clinical implications. Anatomische
Anzeiger 177(2): 193–198.
Drews U. 1995. Color Atlas of Embryology. Georg
Thieme Verlag: Stuttgart.
Copyright # 2005 John Wiley & Sons, Ltd.
I. Ari et al.
Hauser G, De Stefano GF. 1985. Variations in form of
the hypoglossal canal. American Journal of Physical
Anthropology 67: 7–11.
Hori T. 1925. Über die Anomaliendes Hinterhaupts-
beines. Okajimas Folia Anatomica Japonica Tokyo 3:
291–312.
Hyrtl J. 1859. Lehrbuch der Anatomie des Menschen. 6 Aufl.
Wien: W. Braunmüller.
Ishida H, Dodo Y. 1997. Cranial variations in pre-
historic human skeletal remains from the marianas.
American Journal of Physical Anthropology 104: 399–
410.
Lang J, Schaffhauser O, Hoffman S. 1983. Über die
postnatale Entwicklung der transbasalen Schädelp-
forten: canalis caroticus, foramen jugulare, canalis
hypoglossalis, canalis condylaris und foramen mag-
num. Anatomischer Anzeiger 153: 315–357.
Lillie RS. 1917. Variations of the canalis hypoglossis.
The Anatomical Record 13: 131–144.
Myatt HM, Holland NJ, Cheesman AD. 1998. A skull
base extradural hypoglossal neurilemmoma re-
sected via an extended posterolateral approach.
The Journal of Laryngology and Otology 112(11):
1052–1057.
O’Rahilly R, Müller F. 1984. The early development of
the hypoglossal nerve and occipital somites in
staged human embryos. The American Journal of
Anatomy 169: 237–257.
Ossenberg N. 1970. The influence of artificial cranial
deformation on discontinuous morphological traits.
American Journal of Physical Anthropology 33: 357–372.
Ozbek M. 1984. Roma Açikhava tiyatrosundan (Iznik)
çikartilan Bizans iskeletleri. Hacettepe Üniversitesi Ede-
biyat Fakültesi Dergisi 2: 81–89.
Perizonius WRK. 1979a. Nonmetric cranial traits:
Symmetry and side difference. Proc Koninklijke Ne-
derlandse Akademie van Wetenschapen (series C), 82: 91–
112.
Perizonius WRK. 1979b. Nonmetric cranial traits: sex
difference and age dependence. Journal of Human
Evolution 8: 679–684.
Piffer CR, Zorzetto NL. 1982. Mesoskopische und
mikroskopische Betrachtungen des N. hypoglossus.
Anatomischer Anzeiger 151: 367–373.
Rösing FW. 1982. Discreta des menschlichen
Skeletts- ein kritischer Überblick. HOMO 33:
100–125.
Schmidt T. 1975. Der canalis hypoglossi. Topographie,
Form, Lange, Durchmesser und Volumen. Med.
Diss: Würzburg.
Shiozawa Z, Koike G, Segochi K, Shindo K, Sugita K.
1996. Unilateral tongue atrophy due to enlarged
emissary vein in the hypoglossal canal. Surgical
Neurology 45(5): 477–479.
Int. J. Osteoarchaeol. 15: 140–145 (2005)
Bridging Trait of the Hypoglossal Canal
Smith PG, Backer RJ, Kletzker GR, Mishler ET,
Loosmore JL, et al. 1995. Surgical manage-
ment of transcranial hypoglossal schwannomas.
American Journal of Otolaryngology 16(4): 451–456.
Spee V. 1896. Skelettlehre. In Bardelebens Handbuch der
Anatomie des Menschen. Jena: G. Fischer.
Streeter GL. 1912. The development of the nervous
system. In Manual of Human Embryology, Vol 2, Keibel
F, Mall FP (eds). Lippincott: Philadelphia; 1–144.
Copyright # 2005 John Wiley & Sons, Ltd.
145
Weigner K. 1911. Über die Assimilation des Atlas und über
die Variationen am Os occipitale des Menschen. Anato-
mische Hefte. 45. Arbeiten aus Anatomischen In-
stituten: Munchen, Bergmann.
Williams PL, Warwick R, Dyson M, Bannister LH.
1989. The Individual Cranial Bones: Occipital Bone. In
Gray’s Anatomy, Williams PL, Warwick R, Dyson M,
Bannister LH (eds). Churchill Livingstone: London;
371–373.
Int. J. Osteoarchaeol. 15: 140–145 (2005)