The intracranial denticulate ligament: anatomical study with

J Neurosurg 114:454–457, 2011
The intracranial denticulate ligament: anatomical study with
neurosurgical significance
Laboratory investigation
R. Shane Tubbs, M.S., P.A.-C., Ph.D.,1 Martin M. Mortazavi, M.D.,1
Marios Loukas, M.D., Ph.D., 2 Mohammadali M. Shoja, M.D., 3
and Aaron A. Cohen-Gadol, M.D., M.Sc. 3
Pediatric Neurosurgery, Children’s Hospital, Birmingham, Alabama; 2Department of Anatomical Sciences,
St. George’s University, Grenada; and 3Clarian Neuroscience, Goodman Campbell Brain and Spine,
Department of Neurological Surgery, Indiana University, Indianapolis, Indiana
1
Object. Knowledge of the detailed anatomy of the craniocervical junction is important to neurosurgeons. To the
authors’ knowledge, no study has addressed the detailed anatomy of the intracranial (first) denticulate ligament and
its intracranial course and relationships.
Methods. In 10 embalmed and 5 unembalmed adult cadavers, the authors performed posterior dissection of the
craniocervical junction to expose the intracranial denticulate ligament. Rotation of the spinomedullary junction was
documented before and after transection of unilateral ligaments.
Results. The first denticulate ligament was found on all but one left side and attached to the dura of the marginal
sinus superior to the vertebral artery as it pierced the dura mater. The ligament always traveled between the vertebral
artery and spinal accessory nerve. On 20% of sides, it also attached to the intracranial vertebral artery and, histologically, blended with its adventitia. In general, this ligament tended to be thicker laterally and was often cribriform in
nature medially. The hypoglossal nerve was always superior to the ligament, which always concealed the ventral
roots of the C-1 spinal nerve. The posterior spinal artery traveled posterior to this ligament on 93% of sides. On one
left side, the ascending branch of the posterior spinal artery traveled anterior to the ligament and the descending
branch traveled posterior to it. Following unilateral transection of the intracranial denticulate ligament, rotation of the
spinomedullary junction was increased by approximately 25%.
Conclusions. Knowledge of the relationships of the first denticulate ligament may prove useful to the neurosurgeon during procedures at the craniocervical junction. (DOI: 10.3171/2010.9.JNS10883)
Key Words • anatomy • craniocervical junction • foramen magnum •
vertebral artery • neurosurgery • dentate ligament
T
denticulate (dentate) ligaments were first described and depicted by Johann Jacob Huber
(1707–1778).12 These 20–21 paired ligaments are
meningeal extensions that primarily attach the lateral
cord to the internal aspect of the spinal dura mater.4 However, the most rostral of these meningeal specializations
attaches intracranially (Fig. 1). At the foramen magnum,
this intracranial or first (highest) denticulate ligament
travels between the vertebral artery and the ventral rootlets of the C-1 spinal nerve anteriorly and the branches of
the posterior spinal artery, spinal accessory nerve and if
present, dorsal rootlets of C-1 posteriorly.2,13,17 Because
this region is often encountered by the neurosurgeon and
the intracranial denticulate ligament is surrounded by
multiple important neurovascular structures, knowledge
of its anatomical relationships is important.14,16 Therefore, the goal of the present study was to define the specific relationships, histological features, and attachments
of the intracranial denticulate ligament.
454
he
Methods
Ten fresh and 5 embalmed adult cadavers (30 sides)
underwent dissection of the craniocervical junction.
Nine specimens were male and 6 were female, and the
age range of the individuals at the time of death was
49–101 years (mean 75 years). In the prone position, the
specimens underwent removal of the posterior musculature of the upper neck and occiput. We performed an
intermastoid occipital craniectomy and then removed the
posterior arch of C-1 using a high-speed drill and bone
rongeurs. The dura mater was incised and retracted laterally while maintaining the arachnoid mater. Using a Zeiss
surgical microscope, careful arachnoid dissection was
performed and the dorsal roots of the C-1 spinal nerve
and spinal accessory nerve were identified. The first denticulate ligament was found deep to these structures and
followed intracranially to its point of attachment. This
attachment site was carefully observed. We documented
J Neurosurg / Volume 114 / February 2011
Intracranial denticulate ligament
Fig. 1. Schematic drawing illustrating the relationships of the left intracranial denticulate ligament (lig). Note the relationship
between the course of the vertebral artery and its branches and the spinal accessory nerve (n) and first cervical rootlets to this
ligament. a = artery. Used with permission from Clarian Health.
the relationships of regional neurovascular structures to
this intracranial denticulate ligament and measurements
of it. Rotation in the vertical axis was performed before
and after transection of all left-sided intracranial denticulate ligaments to visualize any difference in motion of the
spinomedullary junction. Last, samples of these ligaments
were harvested and submitted for histological analysis.
Results
The intracranial denticulate ligament was found on
all but one left side, and, in all specimens, was seen immediately superior to the vertebral artery as it pierced the
posterior atlantooccipital membrane and dura mater (Fig.
2). On the single side with no ligament, the vertebral artery and spinal accessory nerve had an intimate relationship. On 6 sides (20%), the ligament was found to attach
to the posterolateral aspect of the intracranial vertebral
artery as it coursed to attach laterally. At this location,
the vertebral artery pushed the intracranial denticulate
ligament posteriorly with the ligament, acting as a sling
on 10 sides (30%) (that is, the ligament was draped over
the posterior aspect of the vertebral artery and did not assume its normal vertical course). Laterally, the ligament
was found to attach at the level of the foramen magnum
onto the outer layer of dura mater of the marginal sinus
in all specimens and traveled between the vertebral arJ Neurosurg / Volume 114 / February 2011
tery and spinal accessory nerve. The medial broad aspect
of the ligament arose along the spinomedullary junction.
The mean length and width of this ligament was 10 and
8 mm, respectively. In general, this ligament tended to be
thicker laterally and was often cribriform in nature medially. The hypoglossal nerve rootlets were always superior
to the lateral attachment of the intracranial denticulate
ligament. The ventral roots of the C-1 spinal nerve were
present on all sides and were always concealed by this
ligament. The dorsal rootlets of the C-1 spinal nerve were
seen on 14 sides (46.7%) and, when present, were always
posterior to this ligament. Of the sides with dorsal rootlets of C-1, communications between it and the spinal accessory nerve were observed on 6 sides (43%). Two of
these connections (33%) were noted to pierce the intra­
cranial denticulate ligament as they traveled laterally. The
posterior spinal artery with its branches traveled posterior
to this ligament on 93% of sides and anterior to it on the
remaining sides. On one left side, the ascending branch
of the posterior spinal artery traveled anterior to the ligament and the descending branch traveled posterior to it.
With unilateral transection of the ligaments, rotation of
the spinomedullary junction was increased by approximately 25% in all specimens. Histologically, the ligament
consisted of extensions of arachnoid and pia mater, and in
the specimens with connections to the intracranial segment of the vertebral artery, this ligament blended with
the adventitia of the vessel.
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R. S. Tubbs et al.
Fig. 2. Cadaveric view of the right intracranial denticulate ligament
(D). Note the spinal accessory nerve (XI), vertebral artery (VA), ventral
root of C-1 spinal nerve (C1), and descending branch of the posterior
spinal artery (PSA).
Discussion
Lang8 has stated that in relation to the first denticulate ligament, the lowermost fibers of the spinal accessory nerve are farther dorsal than the upper ones. Linn et
al.9 found that the spinal accessory nerve always crossed
the vertebral artery dorsomedially. These authors further
noted that in 76% of their MR imaging–examined cases
that the vertebral artery at its dural entrance was in direct
contact with the spinal accessory nerve.9 Treating patients
for spasmodic torticollis, Nagata and colleagues10 found
compression of the spinal accessory nerve between the
dural perforation of the vertebral artery and dural attachment of the first denticulate ligament. Shima et al.15 reported a case of spasmodic torticollis in an adult patient
in whom a cure was achieved by vascular decompression
of the spinal accessory root without any nerve sectioning.
The nerve compression was produced by the posterior inferior cerebellar artery and was released by transposing
the artery from the nerve, using the divided intracranial
denticulate ligament. The intracranial and upper cervical
denticulate ligaments are important for isolating all contributions to the spinal accessory nerve during denervation procedures for spasmodic torticollis.5,10 The German
anatomist Herbert von Luschka believed that turgescence
of the vertebral artery may compress the hypoglossal
nerve at this point, although based on our study the hypoglossal nerve was always superior to the most superior
aspect of the intracranial denticulate ligament.1 If anything, the intracranial denticulate ligament may offer a
protective barrier between the spinal accessory nerve
and vertebral artery as demonstrated in our specimens
in which the ligament was bowed posteriorly due to the
posterior protrusion of the vertebral artery. In a cadaveric study, Nanda et al.11 found that the spinal accessory
nerve passed posterior to the denticulate ligament in all
but one specimen where the nerve was seen coursing anterior to this structure. De Oliveira et al.2 mentioned that
the lateral aspect of the intracranial denticulate ligament
456
may be adherent to the posterior spinal arteries and first
cervical rootlets, making separation of these structures
difficult. These authors went on to state that the “most
rostral denticulate ligament” is attached to the intradural
segment of the vertebral artery, implying that this is always the case.2 We found such an association in only 20%
of sides and also noted that the ascending branch of the
posterior spinal artery, on occasion, may travel anterior to
the intracranial denticulate ligament. Rhoton13 has stated
that the first denticulate ligament is often incorporated
into the dural cuff around the vertebral artery at the site
of dural penetration. Therefore, care should be taken in
manipulating the intracranial denticulate ligament as its
inadvertent traction may injure the vertebral artery or its
branches.
Some authors have stated that while approaching
aneurysms of the vertebrobasilar junction that following
transection of the intracranial denticulate ligament, the
medulla is allowed to more easily “fall away.”12 Similarly,
Kashimura et al.7 have described a technique for exposing
the vertebrobasilar junction with traction of the intracranial denticulate ligament via the far lateral suboccipital
approach with partial condylar resection. The result of
this method was that the medulla oblongata was lifted
dorsally and slightly rotated via the denticulate ligament
thus allowing a more superior or inferior approach. Rhoton13 has stated that sectioning the upper 2 denticulate ligaments allows greater access anterior to the spinal cord.
Nanda and associates11 have stated that the intracranial
denticulate ligament may need to be cut with far-lateral
approaches to lesions of the foramen magnum. We found
that unilateral sectioning of the intracranial denticulate
ligament resulted in approximately 25 more degrees of
rotation of the spinomedullary junction, which would allow better visualization of anteriorly located structures.
Pathologically, Jung et al.6 reported on a 72-year-old
woman who presented with neck pain and tingling in the
left arm. Via a midline suboccipital approach, the authors
identified what was found to be a meningioma arising
from the intracranial denticulate ligament. Of note, meningiomas arising anterior to the plane between the intra­
cranial denticulate ligament and the lower cranial nerves
are defined as ventral foramen magnum meningiomas.6
In an earlier study of these ligaments, we found that
the average tensile force of the cervical denticulate ligaments was 0.07 N and that such forces were greater in the
cervical than the thoracic or lumbar regions.18 Developmentally, these ligaments in the upper cervical/cranial region have been implicated in the formation of the “knickung” or kinking of the spinomedullary junction as seen in
patients with the Chiari malformation Type 2.3 This kinking is hypothesized to be caused by caudal displacement
of a portion of the medulla held in relative immobility by
the intracranial denticulate ligament.
Conclusions
The first denticulate ligament is likely to be encountered with approaches to the craniocervical region. Detailed anatomical information regarding its morphology
and neurovascular relationships may, therefore, assist the
J Neurosurg / Volume 114 / February 2011
Intracranial denticulate ligament
neurosurgeon during manipulation in this area, thereby
maximizing surgical maneuvers and minimizing mor­
bidity.
Disclosure
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this
paper.
Author contributions to the study and manuscript preparation
include the following. Conception and design: Tubbs. Acquisition
of data: Tubbs, Mortazavi. Analysis and interpretation of data:
Tubbs, Mortazavi. Drafting the article: Tubbs, Mor­tazavi, Loukas.
Critically revising the article: Tubbs, Loukas, Sho­ja, Cohen-Gadol.
Reviewed final version of the manuscript and approved it for submission: Tubbs, Cohen-Gadol.
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Manuscript submitted July 2, 2010.
Accepted September 1, 2010.
Please include this information when citing this paper: published online October 8, 2010; DOI: 10.3171/2010.9.JNS10883.
Address correspondence to: R. Shane Tubbs, M.S., P.A.-C.,
Ph.D., 1600 7th Ave­nue South, ACC 400, Birmingham, Alabama
35233. email: [email protected].
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