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The veins of the nucleus dentatus: Anatomical and radiological findings

Antonio Di Ieva a,b,,1, Manfred Tschabitscher a,1, Renato Juan Galzio c, Gnther Grabner d,Claudia Kronnerwetter d, Georg Widhalm b, Christian Matula b, Siegfried Trattnig d

a Centre for Anatomy and Cell Biology, Department of Systematic Anatomy, Medical University of Vienna, Vienna, Austriab Department of Neurosurgery, Medical University of Vienna, Vienna, Austriac Department of Neurosurgery, Medical School of the University of L'Aquila, Italyd Department of Radiology, MR Centre of Excellence, Medical University of Vienna, Vienna, Austria

a b s t r a c ta r t i c l e i n f o

Article history:

Received 23 April 2010

Revised 8 July 2010

Accepted 19 July 2010

Available online 23 July 2010

Keywords:

Cerebellum

Dentate nucleus

Posterior fossa veins

Vena centralis nuclei dentati

7 Tesla MR

SWI

Ultra-high field MR

The veins of the dentate nucleus are composed of several channels draining the external surface and one

single vein draining the internal surface. We analyzed specimens of the human cerebellum and described the

central vein of the nucleus dentatus as the main venous outflow of the nucleus. The central vein of the

nucleus dentatus is formed by a network of smaller vessels draining the sinuosities of the gray matter; it

emerges from the hilum of the nucleus and runs along the superior cerebellar peduncle, opening in the

anterior vermian vein. We looked for this structure and for the surrounding veins on ultra-high-field

(7 Tesla) MR, using susceptibility-weighted imaging. An anatomical and radiological description of the veins

of the dentate nucleus is provided, with some remarks on the future clinical applications that these findings

could provide.

2010 Elsevier Inc. All rights reserved.

Introduction

Despite the large number of articles that have been published on

the neurophysiology of the dentate nucleus (DN), there are not many

reports about its vascularization in the literature. The DN occupies a

strategic position and is involved in a myriad of physiological

networks; its function is related to attention, working memory, pro-

cedural reasoning, salience detection, and task-planning (Manto and

Oulad Ben Taib, 2010). The anatomical and functional connectivity of

theDNisreflected in itsvascularnetwork. The venoussystem is oneof

the most variable and heterogeneous organs of the human body, and

cerebellar veins show several different anatomic patterns (Namin,

1955). Although some attempts to describe the cerebellar venous

system were published before the nineteenth century, the first

systematic study of the venous system of the posterior fossa was

performed only in 1950 (Gomez Oliveros, 1950). Later, several anat-

omical studies were performed, with some specific remarks on the

angiographic comparisons. In 1978 a monograph was published that

emphasized the diagnostic importance of the phlebogram in the

posterior fossa (Wackenheim and Braun, 1978), because veins are

important reference points: they trace the contours of the nervous

system parenchyma and cisterns. For this reason, despite the het-

erogeneity of the venous system, veins are critical landmarks for

neuroradiological diagnosis and surgical orientation. The most

relatively recent reports about the venous system of the brain and

the infratentorial structures were published by Duvernoy (1975,

1978, 1999).

Only a fewreports have focused on thevascularization of thenucleus

dentatus (Fazzari, 1933; Goetzen, 1964; Icardo et al., 1982; Lang, 1991;

Shellshear, 1922; Tschabitscher and Perneczcy, 1976), and, particularly,

on the veins of the nucleus dentatus (Tschabitscher, 1979). In the

neuroradiologic developments of the last several decades, digital

subtractionangiographyand MR imaging haveconfirmedthe possibility

of detecting the small veins of the cerebellum, although the smaller

veins of the dentate nucleus have not been described by these

techniques. In order to compare the neuroradiological findings to

those obtained in anatomical dissections, ultra-high-field 7 Tesla

susceptibility-weighted imaging (SWI) (Haacke et al., 2004, 2005)

was performed. SWI is a novel imaging technique that is sensitive to

paramagnetic structures, such as deep brain nuclei(Haackeet al.,2005),

which are known to have an elevated iron level, and veins; the

technique has already been used for vessel related studies (Essig et al.,

1999; Rauscher et al., 2005a,b; Reichenbach et al., 2000).

NeuroImage 54 (2011) 7479

Corresponding author. Centre of Anatomy and Cell Biology, Department of

Systematic Anatomy, Medical University of Vienna, Waehringerstrasse 13, 1090

Vienna, Austria. Fax: +43 1 4277 611 24.

E-mail address: [email protected] (A. Di Ieva).1 These authors contributed equally.

1053-8119/$ see front matter 2010 Elsevier Inc. All rights reserved.

doi:10.1016/j.neuroimage.2010.07.045

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Materials and methods

Anatomical study

The veins of the nucleus dentatus have been studied in 25 human

cadavers obtained from the Department of Anatomy of the Medical

University of Vienna (Vienna, Austria), with no selection for age or

gender. The specimens were studied by gross dissection, microscopic

dissection, dissection of the white matter using the Klinglertechnique, corrosion procedures, and vascular injections (Fig. 1).

The veins were filled in a retrograde manner, injecting the internal

jugular vein with latex or Technovit of different colors (blue and

yellow) (Figs. 1 and 2). In some specimens the vertebral arteries were

injected with red latex or Technovit to observe the relationships with

the venous system (Figs. 1A and C, 7, and 8A and B). The specimens

were dissected to expose the cerebellar nuclei, with regard to the

vascular relationships (Figs. 7 and 8). One specimen underwent

plastination, according to von Hagens' technique (Figs. 4 and 5). Some

pictures were obtained with an exoscope VITOM and recorded by the

AIDA documentation system (Karl Storz GmbH, Tuttlingen, Germany)

(Figs. 2B and 3).

Neuroradiological imaging

Two healthy volunteers underwent 7 Tesla MR imaging (Magnetom

7T, Siemens Healthcare, Erlangen, Germany). The subjects were

informed of the potential side effects of ultrahigh-field 7.0-T MR

imaging, which include vertigo, nausea, loss of balance, claustrophobia,

feelings of electric shocks, and skeletal muscle contractions (Theysohn

et al., 2008). In our cases, after scanning, the volunteers reported only a

transitory (few minutes) vertigo.

SWI data were acquired using a three-dimensional, fully first-

order flow-compensated gradient-echo (SWI) sequence with a TE of

15 ms at 7 T. Other sequence parameters were: TR =28 ms; image-

matrix=704 704 pixel; slices= 96; parallel imaging factor= 2,

acquisition time= 10.18 min, resolution= 0.3 0.3 1.2 mm.

The coil was an eight-channel RF coil (RAPID Biomedical,Wrzburg, Germany). All DICOM data were converted to the MINC

(Medical Imaging NetCDF) format. Phase images were filtered using

Homodyne filtering (Noll et al., 1991), with a Gaussian filter kernel

(full-width at half-maximum= 5 mm in image space), andSWI image

processing was accomplished by performing four phase mask multi-

plications. All image processing was performed using the MINC-

Toolbox (Vincent et al., 2004).

Results

The venous system of the cerebellum is formed by three groups of

vessels: the superior group, drained by the great vein of Galen; the

anterior group, drained by the superficial petrosal veins; and the

posterior group, drained by the sinuses of the tentorium (Huang and

Wolf, 1965). These groups have been further classified as follows: the

basal veins and their tributaries; the superior and inferior vermian

veins; the precentral veins; the peduncular and pontine veins; the

superior petrosal veins with their tributaries (Wackenheim and

Braun, 1978).

Fig. 1. Specimens of human cerebellum. A, tentorial surface: arteries injected with red latex, veins injected with blue latex. B, ventral surface: veins injected with blue latex.

C, tentorial surface, on the left side exposition of the dentate nucleus; arteries injected with red Technovit, veins injected with yellow Technovit. D, tentorial surface, Klingler

technique, exposure of cerebellar white matter and dentate nuclei. 1, postero-superior cerebellar vein; 2, paravermian veins; 3, inferior vermian veins; 4, superior cerebellar artery;

5, great cerebellar veins; 6, anastomotic vein connections (stars of veins); 7, cerebellar tonsills; 8, networks of the tonsillar veins; 9, culmen; 10, declive; 11, anterior part of

quadrangular lobule; 12, primaryfissure; 13, lobulus simplex; 14, posterior superiorfissure; 15, superior semilunar lobule; 16, horizontalfissure; 17, thirdventricle;18, pinealgland;

19, dentate nucleus; 20, nodulus.

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The cerebellar hemispheric veins drain into the superior petrosal

vein and the superior petrosal sinus (anterior group), into the vein ofthe great horizontal fissure of Vicq d'Azyr (affluent of the superior

petrosal vein), which is parallel to the lateral sinus (posterior group),

and into the paravermian and inferior vermian veins (medial group)

(Figs. 1, 2 and 3). On the tentorial surface of the cerebellum, the

antero-superior cerebellar hemispheric veins (great cerebellar veins)

(Figs. 1A, 2 and 3) drain into the great vein of Galen. Several direct

communications among these three systems occur. On the hemi-

spheric surface several stars of vessels are visible (Figs. 1A and 3).

On the tentorial surface of the cerebellum, the superior vermian

vein is visible (supraculminate vein) (Fig. 2), a singleor doublemedialFig. 2. Tentorial surface of the cerebellum on which the superior vermian veins(1, supraculminate veins) are evident as a double trunk in A and a single trunk in B.

(Veins injected with blue latex, arteries with red latex; B: exoscopic image.)

Fig. 3. Tentorial surface of the cerebellum, 7 T-SWI MR imaging. SWI minimum

intensity projection (MIP) over 15.6 mm. 1, paravermian veins; 2, great cerebellar

veins; 3, anastomotic vein connections (stars of veins), also shown in the exoscopic

image in the upper inset; 4, vein of the great horizontal fissure.

Fig. 4. Cerebellum, plastinated specimen, veins injected with blue Technovit, arteries

injected with red Technovit. In the upper inset, 7 T MR SWI phase of the dentate nuclei.

The anatomical and neuroradiological imaging show the characteristic form of the

dentate nucleus as a sac with corrugated walls and an opening, the hilum, directedmedially and anteriorly. The average size of the DN is approximately 15 16 22 mm

(Dimitrova et al., 2002). DN, dentate nucleus; N, nodulus; iVV, inferior vermian veins;

SCA, superior cerebellar artery; the white arrows indicate the rhomboidal arteries,

draining into the SCAs.

Fig. 5. Dentate nucleus, plastinated specimen and 7 T-SWI MR imaging (SWI minimum

intensity projection [MIP] over 9.6 mm). The pictures show the nodulus and the

transversal nodular vein. 1, transversal nodular vein; 2, paravermian vein; 3, nuclear

vein; 4, rhomboidal artery.

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trunk draining into the great vein of Galen, and, more rarely, into the

Rosenthal's basal vein (Wackenheim and Braun, 1978).

A constant landmark of the midline of the posterior fossa is the

anterior vermian vein (precentral vein), (Gomez Oliveros, 1950)

which arises in the groove between the lobules centralis and the

lingual lobule. The superior and inferior segments of this vein form an

angle opening backward, the peak of which corresponds to the

summit of the inferior quadrigeminal tubercules: the so-called

collicular point by Huang has been a very useful landmark in the

period in which the use of phlebogram was very common (Huang and

Wolf, 1966).

The inferior vermian veins have also been useful landmarks.

Delimiting the anterior wall of the cistern magna, these veins enable

the evaluation of the depth of the cistern with regard to the occipital

squama, indirectly indicating hypertension or a malformation of the

inferior pole of the cerebellum (Wackenheim and Braun, 1978). The

inferior vermian veins can be a singleor a double structure, also called

the paravermian vein when situated laterally on the internal face of

the cerebellar hemispheres (Figs. 1A, 3, 4, 5, 7 and 10). The superior

and inferior tonsillar veins (Fig. 1B) converge in the inferior vermianveins at the copular point (Huang et al., 1969). The peritonsillar

venous network runs in two directions: an ascending direction, the

paravermian, which drains into the inferior vermian veins, and

another directionmore anterior andsuperior, to thevena of thelateral

recess of the fourth ventricle, which drains the blood from the plexus

choroideus.

The cerebellar internal veins drain the deep nuclei (nuclear veins)

and the surrounding white matter (medullary veins) (Figs. 8C and

10). The medullary veins form a cortex-perforating group and a group

located in the basal medullary region. These veins (in German,

Venensternen, meaning stars of veins) form a venous arborization

of blood vessels that open into the vein of the lateral recess of the

fourth ventricle (Tschabitscher, 1979).

The arterial andvenous systemof thenucleus dentatus is similar to

the suprarenal gland; a series of arteries on the external cortex and

one central out-flowing vessel (Tschabitscher, 1979) (Figs. 610).

The external veins of the DN open in to the venous star and the

cortex-perforating veins (Fig. 6). The veins that arise from the smaller

veins of the ND and go to the superior and inferior sinus petrosus are

described in some articles as venen floccularis (Braus and Elze, 1960;

Clara, 1959).

The internal nuclear vein (described for the first time in 1979)

(Tschabitscher, 1979) emerges from the hilum of the DN (vena

centralis nuclei dentati) and runs along the superior cerebellar

peduncle, opening in the anterior vermian vein (Figs. 69). The origin

of the central vein of the nucleus dentatus resembles a tuft of smaller

veins (Tschabitscher, 1979) (Fig. 9). Anatomically the two symmet-

rical nuclear zones areseparated by the vermian nodule, on which it is

possible to recognize a thick transversal vein (Krause, 1951) (Fig. 5).The DN is sprinkledby a collateral branchof the superior cerebellar

artery, the so-called rhomboidal artery (Fazzari, 1933; Tschabitscher

and Perneczcy, 1976) (Figs. 4 and 5). It runs in a downward direction

following the superior cerebellar peduncle until it penetrates the

cerebellar tissue, dividing into two to four arteries, and, in a few cases,

reaching the dentate nucleus as a single artery ( Icardo et al., 1982).

When the hilum of the DN is reached, the rhomboidal artery divides

into a network of smaller vessels, the arcuate arterioles (Fazzari,

1933), which penetrate the sinuosities of the gray matter of the

nucleus, forming a kind of vascular olive and showing a precise

vascular pattern (Icardo et al., 1982) (Fig. 8B). Some wigs of the

rhomboidal artery surround the convex face of the DN, where there

can be some anastomoses with some cortical branches coming from

the posterior inferior cerebellar artery (PICA) (Goetzen, 1964; Lang,1991; Shellshear, 1922). The gray matter of the DN has a specific

somatotopic representation of the body (Orioli and Strick, 1989); the

central vein of the DN and the rhomboidal artery form a vascular

network that resembles this structural organization.

Discussion

Several anatomical and radiological studies have been performed

in the past about the vascularization of the dentate nucleus. However,

more recently, much attention has been focused on the neurophys-

iology of the cerebellar nuclei, particularly on the functional

neuroimaging of the DN. Magnetic resonance imaging with fields

strengths lower than 3 Tesla were unable to detect the smaller veins

of the cerebellar nuclei. Fundamental advances were made by

Fig. 6. Klingler technique with exposure of the cerebellar white matter and dentate

nuclei. On theleft side, thecentral veinof thenucleus dentatus is visible (arrow), which

emerges from the DN hilum, runs along the superior cerebellar peduncle, and opens

into the anterior vermian vein. On the right side, the external cortex of the dentate

nucleus has not been removed (asterisk) to show the demarcation between the

cerebellar white matter and the nuclear gray matter (upper inset). In the lower inset,the cortical veins of the DN are visible in yellow. DN, dentate nucleus; N, nodulus; WM,

white matter; SCP, superior cerebellar peduncle.

Fig. 7. Central vein of the dentate nucleus (arrow), visible in gross dissection (upper

image)and in the7 T MR (SWI minimum intensity projection [MIP] over15.6 mm). NV,

nodular vein; iVV, inferior vermian veins; aVV, anterior vermian vein; SCA, superior

cerebellar artery.

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analyzing three-dimensional MR imaging of the cerebellar nuclei,

even if no attempts were made to visualizethe vasculature (Dimitrova

et al., 2002, Dimotrova et al., 2006). Some authors performed MR

analysis of the veins of the posterior fossa (Giordano et al., 2009),

although the sensitivity for detecting smaller but very important veins

was quite low (Kilic et al., 2005); these authors concluded that new

and more sophisticated MR technology might fulfill this need.

Recently the application of ultra-high-field MR (7.0 Tesla) on

humans has enabled improved angiographic imaging of the microvas-

culature in vivo (Cho et al., 2008; Ladd, 2007; von Morze et al., 2007).

Ultra-high-field MR provides an increased signal-to-noise ratio (SNR)

for the in-flow signalat a high spatialresolution (Ladd, 2007; von Morzeet al., 2007). Some studies have shown the feasibility of imaging the

presumed microvascularity in gliomas (Moenninghoff et al., 2010) and

the lenticulostriate arteries with 7 Tesla MR, thus increasing the

understanding of the pathophysiology of brain tissue changes, such as

lacunar infarcts, correlated to small-vessel disease (Cho et al., 2008;

Hendrikse et al., 2008; Kang et al., 2009).

We performed anatomical neuroimaging of the veins of the DN

and we were able to recognize it on 7 Tesla SWI images. Thus, it is

clear that 7 T-SWI MR imaging is reliableand useful fordetecting even

the smaller vessels of the dentate nucleus. This result could have

important implications, not only for the understanding of the huge

variability of the vascular patterns of the deep cerebellar nuclei, but

also forthe planning of surgical operations in theinfratentorialregion.

Kanno et al. considered the surgical treatment of 30 cases ofpinealomas operated with an infratentorial supracerebellar approach,

reporting death in 3 cases. Among other conclusions, the authors

Fig. 8. Central vein of the nucleus dentatus (indicated by a white arrow). A and B, Klingler technique with exposure of the dentate nuclei. In B, it is evident the central vein, with its

smaller tributaries (in yellow), surrounded by a rich network of arcuate arteries, which penetrate in the sinuosities of the gray matter of the nucleus. C, 7 T-SWI MR imaging, axial

section at the level of the dentate nuclei (SWI minimum intensity projection [MIP] over 9.6 mm). D, SWI maximum intensity projection (MIP) over 27.6 mm. DN, dentate nucleus;

SCA, superior cerebellar artery; aa, arcuate arteries; 1, nuclear vein; 2, medullary veins.

Fig. 9. Schematic drawing showing the majorvenous outflowof thedentate nucleus (axialand sagittal sections).Note thetuftof smaller veins that converge in thecentral vein of the

nucleus dentatus.

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suggested that the coagulation and ablation of the precentral

cerebellar vein could have caused diffusion thrombosis of deep

veins (Kanno, 1995). According to the described anatomy of the veins

of the DN, it seems likely that the closure of the precentral veins could

cause a venous infarct of the DNs, although no data are available on

the physiological contribution due to the perinuclear venous plexus

draining into the pericerebellar sinuses. A future reliable integration

of 7 T MR images in intraoperative neuronavigation systems could

help neurosurgeons to avoid damage of such small vessels. MR

imaging at 7 Tesla could also improve the understanding of the

physiopathology in stroke patients due to by deep cerebellar infarcts

or affected by venous malformations. Additional confirmatory studies

are required to show the reproducibility of the ability to detect the

smaller veins of theDN using ultra-high-field MR, and demonstrate itsusefulness for clinical purposes.

Acknowledgments

We would like to thank Prof. Mircea-Constantin Sora, MD, for the

preparation of the plastinated specimen.

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Fig. 10. 7 T-SWI MR imaging, axial section on the dentate nuclei (SWI minimum

intensity projection [MIP]over 9.6 mm). 1, dentate nuclei; 2, central veinof the dentate

nucleus; 3, transversal nodular vein; 4, vermis; 5, inferior vermian veins; 6, brachium

pontis; 7, perpendicular vein; 8, anteromedian pontine vein; 9, superior petrous sinus;

10, nuclear vein draining into superior petrous sinus; 11, medullary veins draining into

the vein of the horizontal fissure (12).


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