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Three-dimensional microsurgical anatomy of cerebellar peduncles

Article in Neurosurgical Review · August 2012

DOI: 10.1007/s10143-012-0417-y · Source: PubMed

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Neurosurg Rev
DOI 10.1007/s10143-012-0417-y

ORIGINAL ARTICLE

Three-dimensional microsurgical anatomy of cerebellar

peduncles
Paolo Perrini & Giacomo Tiezzi & Maura Castagna &
Riccardo Vannozzi

Received: 2 April 2012 / Accepted: 17 June 2012

# Springer-Verlag 2012

Abstract The microsurgical anatomy of cerebellar peduncles Keywords Cerebellar peduncles . Dentate nucleus . Fibre
and their relationships with neighbouring fasciculi were in- dissection technique . Three-dimensional anatomy . White
vestigated by using a fibre dissection technique. As the dis- matter tracts
section progressed, photographs of each progressive layer
were obtained and stereoscopic images were created using
the 3D anaglyphic method. These findings provided the ana- Introduction
tomical basis for a conceptual division of cerebellar peduncles
into segments. The middle cerebellar peduncle (MCP) was The cerebellar peduncles are three paired, symmetrically
divided into two segments: cisternal and intracerebellar seg- placed bundles of white matter concentrating fibres, which
ments. The inferior cerebellar peduncle (ICP) was divided into enter and leave the cerebellum with complex anatomical
three segments: cisternal, ventricular and intracerebellar seg- three-dimensional (3D) relationships. Compared with the
ments. The superior cerebellar peduncle (SCP) was divided several published investigations relating to the structure
into three segments: intracerebellar, intermediate and intra- and functions of the cerebellum and its connections, few
tegmental segments. The fibre dissection technique disclosed studies described the detailed topographic anatomy of
a constant course of peduncular fibres inside the white core of cerebellar peduncles and their relationship with adjacent
the cerebellum. The pontocerebellar fibres of the MCP pass structures and overlying cerebellar lobules [3, 12, 13,
over and laterally to the bundles of the ICP and SCP. The 15, 22, 24].
centripetal fibres of the ICP wrap around the radiation of the In proceeding with operative exposures of the fourth
SCP and the dentate nucleus, directed towards the cortex of ventricle, a detailed knowledge of 3D relationships be-
the vermis. The centrifugal bundle of the SCP ascends to- tween the cerebellar peduncles and the fourth ventricle
wards the mesencephalon where it sinks passing below the and superficial anatomy of cerebellum is mandatory.
fibres the lateral lemniscus. The knowledge gained by study- Such surgical exposures are required for resection of
ing the intrinsic anatomy of the cerebellum is useful to ac- tumors of the fourth ventricle and resection of neoplastic or
complish appropriate surgical planning and, ultimately, to vascular lesions of its floor. In addition, the cerebellar
understand the repercussions of surgical procedures on the peduncles can be the site of pathological processes such as
white matter tracts in this region. neuroepithelial tumors and vascular malformations; hence,
understanding the morphological characteristics of these ner-
vous structures is crucial in performing safe surgery in this
P. Perrini (*) : G. Tiezzi : R. Vannozzi
region.
Department of Neurosurgery,
Azienda Ospedaliero Universitaria Pisana (AOUP), In this study we attempt to improve our understanding of
Via Paradisa 2, 56100 Pisa, Italy the topographic anatomy of cerebellar peduncles by apply-
e-mail: p.perrini@ao-pisa.toscana.it ing the operating microscope to Klinger’s method of white
matter fibre dissection [11, 27]. Stereoscopic images pro-
M. Castagna
Department of Human Pathology, University of Pisa, duced using the anaglyphic technique are provided to facil-
Pisa, Italy itate 3D comprehension of these anatomical structures.
 Neurosurg Rev

Materials and methods Fig. 1 2D (a–c, e–h) and 3D (d) illustrations of stepwise dissections„
of the tentorial and suboccipital surfaces of the cerebellum to demon-
strate the topographic anatomy of the cerebellar peduncles. The 2D
Five normal previously frozen, formalin-fixed human brains illustrations are labeled to facilitate understanding of the same illustra-
were dissected under the operating microscope (×3–40 mag- tion in 3D. The 3D image should be viewed with red and blue anaglyph
nification) by using fibre dissection technique originally glasses. a Superior view of the tentorial surface after removal of the
described by Ludwig and Klinger [11]. The brains were quadrangular lobule and culmen with wide exposure of the cerebello-
mesencephalic fissure. The lingula and the cisternal surface of superior
obtained from fresh autopsy specimens and were fixed in cerebellar peduncle constitute respectively the posterior and the ante-
10 % formalin for at least 1 month. The arachnoid mem- rior walls of the inner aspect of the fissure and the superior and medial
brane and vascular structures were carefully removed, and aspect of the middle cerebellar peduncle forms, in each side, its most
the brains were frozen at −15 °C for 15 days. Before the lateral limit. The cisternal segment of the middle cerebellar peduncle
begins lateral to the apparent origin of the CN V. The superior cere-
dissection began, the brains were washed under running bellar peduncle ascends at the lateral edges of the superior medullary
water and allowed to thaw. The cerebellum was dissected velum to enter the midbrain below the inferior colliculus. The inter-
from the superior and lateral aspects in a stepwise manner peduncular sulcus separates the cisternal segments of the middle and
using wooden spatulas with tips of various sizes and micro- superior cerebellar peduncles. b The white core of the cerebellum has
been divided with an axial at the level of the dentate nucleus in which
surgical dissectors. This technique enabled complete dissec- the centrifugal fibres of the superior cerebellar peduncle arise. The
tion of fibre bundles and allowed description of anatomical interpeduncular sulcus, which separates the middle and superior
relationships of cerebellar peduncles, especially in their peduncles, joins superiorly the lateral mesencephalic and the pontome-
course in the white core of the cerebellum. In two additional sencephalic sulci and ends caudally into a narrow pouch, the para-
brachial recess. c Additional cerebellum has been removed with a
specimens, the cerebellum was sliced along the axial and coronal cut at the level of tonsillar peduncle. The tonsillar peduncle,
coronal plane to demonstrate the relationships of the cisternal located along the superior margin of the tonsil, attaches the tonsil to the
segments of peduncles with the white core of the cerebellum white core of the cerebellum, inferior and lateral to the dentate nucleus.
and the dentate nucleus. The stereoscopic illustrations pre- d 3D illustration of the figure labeled in c. e The left tonsil has been
removed by dividing its peduncle. Removing the tonsil exposes the
sented here were performed with the anaglyphic technique as lower part of the roof of the fourth ventricle and the cisternal segment
previously described in the literature [23]. of the inferior cerebellar peduncle, which is not sharply demarcated
from the more caudally placed gracile and cuneate tubercles. The
cisternal segment of the inferior cerebellar peduncle terminates at the
attachment of the tela chorioidea to the taenia. f The tela chorioidea has
Results been removed to expose the ventricular segment of the inferior cere-
bellar peduncle, which forms the floor, and the rostral wall of the
Basic anatomic configuration of cerebellar peduncles lateral recess. g Additional cerebellum has been removed to expose
part of the floor of the fourth ventricle and the large peduncular mass
where the cerebellar peduncles converge. The inferior medullary velum
The middle cerebellar peduncle (MCP) or brachium pontis and the tonsil have been displaced downward to expose the supero-
is the largest afferent system of the cerebellum and is com- lateral recess. The dentate tubercle is anterior to the lateral margin of
posed of pontocerebellar fibres running from the pontine the inferior medullary velum. h The full length of the floor of the fourth
nuclei and the nucleus reticularis tegmenti ponti located ventricle has been exposed. In the lateral recess, the dorsal cochlear
nucleus produces a smooth prominence on the ventricular segment of
mainly on the contralateral side [8, 17, 18, 21]. This large the inferior cerebellar peduncle, the auditory tubercle. The union of the
white matter tract connects the pons with the cerebellum and cerebellar peduncles forms a large fibre bundle, which lines the ven-
has a cisternal and an intracerebellar segment (or MCP tricle. The fibres of superior and inferior cerebellar peduncles form the
radiation, Fig. 1). The cisternal segment of MCP begins ventricular surface of this peduncular mass, whereas the middle cere-
bellar peduncle runs more laterally. Cent., central; Cer., cerebellar;
lateral to the apparent origin of the cranial nerve (CN) V Cer.Mes., cerebellomesencephalic; Cer. Ped., cerebral peduncle; Cist.,
and includes the rostral and the lateral surface of the initial cisternal; CN, cranial nerve; Coch., cochlear; Coll., colliculus; Dent.,
part of the peduncle (Fig. 1a). The rostral surface of the dentate; Fiss., fissure; Horiz., horizontal, Inf., inferior; Interped., inter-
MCP runs in the cerebellomesencephalic fissure where it peduncular; Intracer., intracerebellar; Lat., lateral; Med., median, med-
ullary; Mes., mesencephalic; Mid., middle; Nucl., nucleus; Parabrach.,
forms the lateral part of the inner wall of the fissure parabrachial; Ped., peduncle; Quad., quadrangular; Rec., recess; Seg.,
(Fig. 1a). The lingula and the dorsal or cisternal surface of segment; Sup., superior; Surf., surface; Tub., tubercle; Vel., velum;
superior cerebellar peduncles (SCP) constitute respectively Vent., ventricular
the posterior and the anterior walls of the inner aspect of the
fissure. The lateral surface of the MCP runs between the two cerebellar peduncles that connects the brainstem and cere-
limbs of the V-shaped cerebellopontine fissure. The intra- bellum (Fig. 1g, h).
cerebellar segment begins where the pontocerebellar fibres The SCP or brachium conjunctivum consists of efferent
become deep with respect to the cerebellar lobules limiting fibres from the dentate, globose and emboliform nuclei to the
the cerebellomesencephalic and pontocerebellar fissures red nucleus of the opposite side [17, 18, 21]. This centrifugal
(Fig. 1b, c). The MCP enters the cerebellum on the lateral white matter system has an intracerebellar (or SCP radiation),
side of the large peduncolar mass formed by the three an intermediate and an intrategmental segment (Fig. 1a–d, g, h).
Neurosurg Rev

The intermediate segment forms the cisternal and ventricular the interpeduncular sulcus, which is a shallow groove joining
surfaces of the superolateral part of the roof of the fourth anteriorly the pontomesencephalic sulcus and superiorly the
ventricle (Fig. 1a–d, g). The dorsal or cisternal surface of lateral mesencephalic sulcus (Fig. 1b). At the caudal tip of the
intermediate segment is located in the cerebellomesencephalic interpeduncular sulcus is the parabrachial recess, which is a
fissure and forms longitudinal prominences ascending on the narrow pouch formed by the convergence of cisternal seg-
medial side of the MCP to enter the midbrain beneath the ments of superior and middle cerebellar peduncles (Fig. 1b).
inferior colliculi (Fig. 1a, b). The inner or ventricular surface The inferior cerebellar peduncle (ICP) ascends along the
of intermediate segment forms the lateral ventricular part of the lateral border of the fourth ventricle and consists of the
superior portion of the fourth ventricle (Fig. 1g, h). The superior lateral, afferent restiform body and the medial principally
medullary velum is a thin semitranslucent lamina of white efferent juxtarestiform body [17, 18, 21]. The restiform
matter, which stretches between the superior cerebellar body is composed of two main fascicles: the dorsal spino-
peduncles and forms the median part of the superior portion cerebellar tract, and the olivocerebellar fibres from the con-
of the fourth ventricle. The cisternal surfaces of the tralateral inferior olive [21]. In addition, fibres from the
superior and middle cerebellar peduncles are separated by lateral cuneate nucleus of the same side (dorsal external
 Neurosurg Rev

arcuate fibres) and from the reticular and arcuate nuclei this segment of the ICP (Fig. 1h). At this level, a
(ventral external arcuate fibres) compose the restiform body varying number of striae medullares running diagonally
[21]. The medial part of the ICP (juxtarestiform body) con- or horizontally cross the peduncle. The ventricular segment of
sists of vestibulocerebellar fasciculus composed of ascending the ICP makes a sharp turn dorsally to enter the white core of
branches of the vestibular nerve directed to the vestibular part the cerebellum on the inferomedial part of the fibre
of the cerebellum [21]. The ICP can be divided into three bundle formed by the union of the three cerebellar
segments from caudal to rostral, namely a cisternal, a peduncles (Fig. 1g, h).
ventricular and an intracerebellar segment (or ICP radiation, The fibres of the three peduncles blend in a large white
Fig. 1e–g). The cisternal segment of the ICP lies between the matter bundle lining the ventricular surface of the rostral
inferolateral edges of the fourth ventricle, where the tela wall of lateral recess and the inferior portion of the lateral
chorioidea is attached to the taenia, and the postolivary sulcus, part of the fourth ventricle (Fig. 1g, h). The fibres of supe-
where the glossopharyngeal and the vagus nerves arise rior and inferior peduncles form the ventricular surface of
(Fig. 1e, f). There is no definite demarcation between the this large peduncular mass, whereas the middle peduncle
ICP and the more caudally placed gracile and cuneate runs more laterally. In fact, the intrinsic anatomy of the
tubercles (Fig. 1e, h). The ventricular segment of the ICP peduncular mass and the relationships of peduncular radia-
begins at the line of attachment of the tela chorioidea to the tions are not disclosed with standard anatomical dissection.
taenia and courses upward and laterally in the floor of The fibre dissection technique enables complete exposure of
the lateral recess (Fig. 1e, f). The dorsal cochlear nu- the cerebellar peduncles and their radiations within the
cleus produces an eminence, the auditory tubercle, on cerebellar white matter (Fig. 2a–c).

Fig. 2 Illustrations demonstrating a general overview of the cerebellar tubercle; c, red nucleus; d, cranial nerve V; e, cranial nerve III; f, cranial
peduncles and their radiations within the white core of cerebellum. a nerve II; g, olfactory tract; h, anterior commissure. b Illustration
The inferior cerebellar peduncle is highlighted in shades of blue, the demonstrating the segments of the inferior cerebellar peduncle. The
superior cerebellar peduncle in shades of red and the middle cerebellar cisternal segment is highlighted in horizontal lines, the cisternal seg-
peduncle in shades of yellow. The cisternal segment of the middle ment in solid color and the intracerebellar segment in vertical lines. c
cerebellar peduncle has been transected to expose the fibres of the Illustration demonstrating the segments of the superior cerebellar pe-
inferior and superior cerebellar peduncles. The infradentate bundle duncle. This peduncle, which is mainly composed by fibres originating
(asterisk) is a fasciculus of the intracerebellar segment of the middle from the dentate nucleus directed toward the red nucleus of the oppo-
cerebellar peduncle running inferior to the dentate nucleus and site side, presents an intracerebellar (1), an intermediate (2), and an
connected with the tonsillar peduncle. a, dentate nucleus; b, auditory intrategmental segment (3)
Neurosurg Rev

Fibre dissection of the middle cerebellar peduncle Fibre dissection of the superior cerebellar peduncle

The pontocerebellar fibres in the ventral part of the Removal of the ICP fibres exposes the SCP radiation, which
pons are organized in three transverse orientated layers, arises from the dentate, globose and emboliform nuclei
superficial, intermediate and deep, divided by the pyra- (Fig. 3f, g). The dentate nucleus consists of well-defined,
midal fibres, which run as discrete fasciculi in the island-like almost parallel bars of gray matter that are sep-
middle layer. The cisternal segment of the MCP begins arated from each other by shallow grooves filled with white
distally to the apparent origin of the CN V where the matter. In close relation to the hilus of dentate nucleus,
pontocerebellar fibres merge together and is situated in delicate efferent fibres converge to form the SCP. On the
the cerebellopontine fissure laterally and in the cerebel- superolateral surface of the fourth ventricle, the dentate
lomesencephalic fissure superomedially. Removal of the nucleus, covered only by the ependyma and by a tiny layer
cortical gray matter of the quadrangular and simple of pontocerebellar fibres, produces a discrete prominence,
lobules exposes the underlying white matter organized the dentate tubercle. The fastigial nucleus is positioned next
in laminae, which are the projections into the lobules of to the midline. The globose nuclei and the emboliform
the white medullary body (Fig. 3a). The removal of nucleus are situated in an intermediate position. The inter-
cerebellar laminae exposes the MCP radiation. As the dissec- mediate segment of SCP emerges as distinct fibre bundle
tion of the MCP progresses, the radiation pattern of its fibres from the white core of cerebellum and ascends towards the
from the pontine nuclei to the cerebellar cortex is progressive- mesencephalon where it progressively sinks after passing
ly disclosed. The pontocerebellar fibres of the intracerebellar below the fibres of the lateral lemniscus, which border
segment of the MCP run with a posterior and medial caudally the lemniscal trigone (Fig. 3h–j).
orientation and show terminations in all lobules of the
cerebellum, with the exception of the nodulus and the Relationship between the cerebellar peduncles and other
flocculus (Fig. 3b, c). Just anterior to the dentate nucle- fascicles
us, the fibres of the MCP are divided into the thicker supra-
dentate and slender infradentate bundles (Fig. 3b). The Ventral spinocerebellar tract The ventral spinocerebellar
infradentate bundle of the MCP provided connections with tract, which consists of fibres originating from the cells of
the tonsillar peduncle (Fig. 3b). Removal of the deep ponto- posterior gray column of the same and opposite side, con-
cerebellar fibres exposes the purse-like prominence of the veys proprioceptive information to the cerebellum. Dissec-
dentate nucleus located posterior and inferior to the deep tion of the ventral spinocerebellar tract was difficult because
centripetal fibres of the ICP, lateral to the fastigium and above of its small size and could be not dissected accurately. The
the superolateral recess of the fourth ventricle (Fig. 3d, e). ventral spinocerebellar tract runs through the pontine retic-
ular formation and turns dorsolaterally at the rostral end of
Fibre dissection of the inferior cerebellar peduncle the pons [18]. This small afferent bundle courses over the
dorsolateral surface of SCP and passes rostral to the fibres of
Removal of the deep fibres of MCP exposes the centripetal trigeminal nerve to enter the cerebellum.
fibres of the ICP traversing from lateral to medial the central
core of cerebellum, with a slightly posterior direction towards Lateral lemniscus The lateral lemniscus is the central audi-
the cortex of the vermis and to a lesser extent to the cortex of tory tract from the cochlear nuclei towards the inferior
the cerebellar hemisphere (Fig. 3d, e). The superficial fibres of colliculus and the inferior quadrigeminal brachium. The
ICP wrap around the dentate nucleus and arch medially to- fibres of lateral lemniscus, which are the continuation of
wards the vermis. A characteristic white matter prominence is the trapezoid body, ascend from the tegmental part of the
created by the fibres of ICP crossing the dentate nucleus. The pons where they are located laterally to the medial lemnis-
deep fibres of ICP proceed in a groove located at the junction cus and dorsally to the deep stratum of pontocerebellar
of the dentate nucleus and the initial portion of the SCP fibres. In their course towards the inferior colliculus, the
(Fig. 3d, e). On the basis of the different orientation of both fibres of lateral lemniscus turn dorsolaterally until they
white matter tracts on the medial side of the peduncular mass, occupy a position on the superolateral aspect of the SCP
they could be progressively dissected and differentiated. The marking the transition between the cisternal and the intra-
fibres of trigeminal nerve are observed ventromedial to the tegmental part of the peduncle (Fig. 3h–j).
ICP and posterior to the lateral and medial lemnisci. At the
anterior portion of white core of the cerebellum, the fibres of Medial lemniscus The medial lemniscus is a broad bundle
ICP form the posterior boundary of parabrachial recess, which of longitudinal fibres, which arise from the nuclei gracile,
is a triangular pouch lined by the SCP on its medial side and and cuneatus of the opposite side. These fibres convey
by the MCP on its lateral side. sensory impulses from the muscles, joints and tendons, as
 Neurosurg Rev

well some elements of tactile sensibility. This bundle is Fig. 3 2D (a, b, d, f, h, j) and 3D (c, e, g, i) illustrations of stepwise„
located ventromedially in the tegmental part of the pons fibre dissection of the right hemisphere and cerebellar peduncles. The
2D illustrations are labeled to facilitate understanding of the same
and shifts progressively to the lateral portion of the tegmen- illustration in 3D. The 3D images should be viewed with red and blue
tum of the mesencephalon displaced by the red nucleus anaglyph glasses a Extensive dissection of the lateral aspect of the
(Fig. 3h–j). Due to this dorsolateral displacement, the me- brain reveals the corona radiata which joins the internal capsule, the
dial lemniscus is ventral to the SCP in the rostral part of the sagittal stratum and the mediobasal temporal region. The cerebellar
gray matter has been removed, and the basilar pons has been dissected.
pons and becomes laterally placed to the SCP at the level of The pontocerebellar fibres merge together distally to the apparent
the inferior colliculus where it lies at the ventrolateral border origin of the CN V where they form the middle cerebellar peduncle,
of the tegmentum close to the substantia nigra (Fig. 3j). which courses superficial and laterally to the inferior and superior
Several observations about the spatial relationships of the cerebellar peduncles. b The middle cerebellar peduncle has been par-
tially removed (asterisk) while preserving its deep layer of pontocer-
intracerebellar segment of cerebellar peduncles can be ebellar fibres, which spread around the prominence, created by the
made. First, in all 10 cerebellar hemispheres that were dentate nucleus. A bundle of pontocerebellar fibres running below the
dissected, the pontocerebellar fibres of MCP covered the dentate nucleus (the infradentate bundle, arrows) joins with the tonsil-
white matter tracts of inferior and superior cerebellar lar peduncle. c 3D illustration of the figure labeled in b. d The middle
cerebellar peduncle has been transected and its fibres removed to
peduncles running with horizontal or slightly oblique direc- expose the centripetal fibres of the inferior cerebellar peduncle, which
tion. Second, progressive dissection of the MCP superior to reach the cortex of the vermis and to a lesser extent the cortex of the
the apparent origin of the trigeminal nerve in the direction of hemisphere. In addition, the postero-lateral fibres of the inferior cere-
the deep layer of pontocerebellar fibres will produce an alley bellar peduncle have been removed to expose the parallel bars of gray
matter of the dentate nucleus. e 3D illustration of the figure labeled in
directed towards the basilar pons limited ventrally by the d. f the radiation of the inferior cerebellar peduncle has been partially
corticospinal tract and dorsally by the medial and lateral transected (arrowheads) to fully expose the superior cerebellar pedun-
lemnisci. Third, in all specimens, the tonsillar peduncle cle, which arises from the dentate nucleus and ascends towards the
was attached to the infradentate bundle of the MCP, which, mesencephalon where it sinks after passing below the fibres of the
lateral leminscus. g 3D illustration of the figure labeled in f. h Supero-
in turn, was posterior to the initial part of the ICP radiation. lateral view of another specimen. The white matter of the right cere-
Fourth, the dentate nucleus at the level of superolateral bellum has been dissected, and a sagittal section of the basilar part of
recess is covered by a tiny layer of pontocerebellar fibres the pons has been made to demonstrate the relationship of the pyrami-
on its ventricular side and is medial and inferior to the ICP dal tract with the medial and lateral lemnisci. i 3D illustration of the
figure labeled in h. j Enlarged view of h. The fibres of the lateral
radiation. lemniscus run toward the inferior colliculus on the superolateral aspect
of the superior cerebellar peduncle and mark the transition between the
cisternal and the intrategmental part of the peduncle. Ant., anterior;
Discussion Cap., capsule; Cer., cerebellar; Cer. Ped., cerebral peduncle; Chor.,
choroid; CN, cranial nerve; Coll., colliculus; Comm., commissure;
Dent., dentate; Glob., globus; Hippo., hippocampal; Inf., inferior;
Nomenclature of cerebellar peduncles Int., internal; Intracer., intracerebellar; Lat., lateral; Lemn., lemniscus;
Med., medial; Mid., middle; Nucl., nucleus; Pall., pallidus; Ped., pe-
Surgical exposure of cerebellar peduncles is a critical com- duncle; Plex., plexus; Pyram., pyramidal; Rad., radiata; Sag., sagittal;
Seg., segment; Spinocer., spinocerebellar; Subs., substantia; Sup.,
ponent of many neurosurgical approaches for neoplastic and superior
vascular lesions located in the posterior fossa. Surgical
approaches must be tailored to the site of the pathological
findings with a thorough understanding of the anatomy of single cerebellar peduncle [26]. Tomita’s classification is use-
this region. Microsurgical anatomy of cerebellar peduncles ful for understanding the location and extension of a cerebellar
has been described by Matsushima et al. [13] and by Rhoton lesion, but is anatomically inaccurate. In this report, we pro-
[22], but a segmental nomenclature has not been established pose a nomenclature, which describes the segments of the
in neurosurgical literature. In addition, controversies remain cerebellar peduncles according to a detailed understanding
regarding the course of the cerebellar peduncles at the level of the compartments through which they travel. In addition,
of the white core of the cerebellum because of the admixture by applying the operating microscope to Klinger’s method of
of peduncular fibres, which assume complex 3D relation- fibre dissection, we could dissect the white core of the cerebel-
ships. In 1986, Tomita subdivided the intracerebellar seg- lum and demonstrate the intracerebellar course of peduncles.
ment of peduncles into three portions (i.e. brain stem Our dissections disclosed a constant course of peduncular
portion, ventricular portion and cerebellar portion) by using fibres inside the white core of the cerebellum. The pontocer-
two arbitrary reference lines superimposed on a cross section ebellar fibres of MCP course with a posteromedial direction
of the brainstem and the cerebellum at the midpontine level and pass over and laterally the bundles of the inferior and
[26]. Tomita’s report did not consider the intracerebellar seg- superior cerebellar peduncles. The centripetal fibres of ICP
ments of peduncles as separate structures and described the after a sharp turn in the roof of the lateral recess pass medially
three distinct bundles in the white core of cerebellum as a to the MCP fibres and wrap around the fibres of SCP and the
Neurosurg Rev
 Neurosurg Rev

dentate nucleus, directed towards the cortex of the vermis. transpeduncular approach requires a small neurotomy rostral
Removal of fibres of ICP exposes the centrifugal bundle of to the apparent origin of the trigeminal nerve and gentle
SCP, which ascends towards the mesencephalon inferior the dissection along the pontocerebellar fibres [5]. According to
ICP fibres and inferomedial the MCP bundle. Lesions of cer- our results, when such an approach is directed towards the
ebellar peduncles are usually described generically in the liter- deep layer of pontocerebellar fibres, the anatomical bound-
ature, indicating the peduncle affected without reporting the aries to be respected are the corticospinal tract ventrally, the
exact lesion location [10, 26]. The proposed nomenclature trigeminal nerve caudally and the medial and lateral lemnisci
allows localizing precisely a pathological process in the cere- posteriorly in the tegmental pars of the pons. The lateral
bellar peduncles. Careful anatomical description of a peduncu- transpeduncular approach is suited for intrinsic cavernous
lar lesion is relevant since it dictates the surgical approach. For malformations of the basilar pons in symptomatic patients [5].
example, a cavernous malformation of the cisternal portion of The ICP can be damaged when approaching pathological
ICP requires a midline suboccipital craniotomy and dissection processes involving the medullotonsillar space and the lateral
of the inferior extension of the cerebellomedullary fissure, the recess of the fourth ventricle. Experimental sectioning of the
so-called medullotonsillary space [14]. On the other hand, a ICP induces disturbances of the equilibrium with truncal
cavernous malformation of the ventricular portion of the ICP ataxia, staggering gait and tendency to fall towards the side
requires exposure of the lateral recess with elevation of the of the lesion [20]. These disturbances are analogous to those
tonsil and division of the tela chorioidea using the telovelar produced by lesion of the flocculonodular lobe [13, 20].
approach [6, 7, 16, 32]. Thanks to the technological advances Similarly, the consequence of surgical removal of tumors
in magnetic resonance imaging, the precise location of a pe- attached to the floor of the lateral recess can be temporary
duncular lesion can now be preoperatively identified. In addi- disequilibrium [6]. The use of natural clefts in the cerebello-
tion, the development of diffusion tensor (DT) tractography medullary fissure to avoid sacrifice of normal cerebellar tissue
allows the study of the intrinsic structure of cerebellum and the (i.e. the transvermian approach) was initially described by
creation of maps of white matter connectivity [1, 25]. The 3D Yasargil who entered the fourth ventricle through the “tonsil-
relationships of the intracerebellar segments of peduncles dis- louveal” sulcus, along the medial division of the posterior
closed in our dissections are similar to those obtained with DT inferior cerebellar artery [30, 31]. Subsequently, refinements
tractography [1, 25]. 3D anatomical knowledge of the white of the transcerebellomedullary fissure approach have been
matter pathways of the cerebellum acquired with fibre dissec- described by different authors [14, 16]. The “lateral recess
tion improves the spatial understanding of tractographic recon- opening method” proposed by Matsushima et al. [14] provides
structions of cerebellar peduncles, especially when there is exposure of the ventricular portion of the ICP elevating the
compression and displacement of bundles in the presence of tonsil, cutting the unilateral taenia and extending the telar
pathological processes. opening laterally towards the lateral recess. This approach
was duplicated with minor modifications by Ziyal et al. [32]
Cerebellar peduncles, clinical relevance and surgical and by Jean et al. [6] with satisfactory results in management
approaches of tumors in the lateral recess. Recently, Lawton et al. [10]
proposed a supratonsillar trajectory through the tonsillobiven-
To reach lesions in and around the cerebellar peduncles, tral fissure to resect cavernous malformations of the ICP. This
surgeons must use strategies to avoid transgressing the approach relies on extraventricular route, requires inferome-
peduncular fibres and the cerebellar nuclei, since devastat- dial retraction of the tonsil and transgresses the tonsillar pe-
ing morbidity has been historically reported to occur. The duncle to reach the ICP [10]. Our fibre dissection indicates
MCP is located on the cisternal surface of the large pedun- that the supratonsillar approach exposes the initial part of the
cular mass where all peduncles converge and may be injured radiation of the ICP, at the level where its centripetal fibres
during operations on lesions involving the cerebellomesen- running from the roof of the lateral recess arch medially
cephalic and pontocerebellar fissures. Lesions of the MCP crossing the dentate nucleus. In fact, such an approach risks
induce ataxia, hypotonia and dysmetria on the same side of injury of the dentate nucleus, which is located just above the
the lesion similar to that caused by injury of the lateral part tonsillar peduncle. If the dentate nucleus is damaged, equili-
of the hemisphere [2, 13]. In fact, clinical experience sug- bratory disturbances, intention tremor, dyskinesia and dysto-
gests that the MCP tolerates small neurotomies to access nia can occur [4, 9].
peduncular lesions that do not reach the surface (i.e. intrinsic Lesions of the SCP induce symptoms similar to those
lesions) [19]. The incision must be made on the dorsal of the dentate nucleus. The symptoms are generally mild
surface of the MCP parallel and longitudinal to respect the and transient in case of partial sectioning of the peduncle
pontocerebellar fibres [19]. Recently, transgression of the [28].
MCP has been proposed to resect intrinsic lesions of the The paramedian supracerebellar approach first described by
basilar pons with relatively low morbidity [5]. The lateral Yasargil [29] for aneurysms of the superior cerebellar artery
Neurosurg Rev

provides access to the cisternal surface of the intermediate References

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anterior to the lateral margin of the inferior medullary velum. ONS26–ONS29
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(2001) Transcerebellomedullary fissure approach with special ref-
duncular fibres inside the white core of cerebellum, but did
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The Klinger’s dissection technique has proven valuable in and cerebellum. Springer, Wien
18. Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human
understanding the intrinsic anatomy of the cerebellum and
central nervous system. Springer, Berlin
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is of surgical significance has been provided. Applying the gery 40:101–105
20. Pickel VM, Krebs H, Bloom FE (1973) Proliferation of
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the morbidity for complete removal of tumors and vascular Saunders, Philadelphia
22. Rhoton AL Jr (2000) Cerebellum and fourth ventricle. Neurosur-
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23. Ribas GC, Bento RF, Rodrigues AJ (2001) Anaglyphic three-
Acknowledgments We thank Nicola Benedetto Ph.D., M.D., for the dimensional stereoscopic printing: revival of an old method for
illustrations of cerebellar peduncles. anatomical reporting. J Neurosurg 95:1057–1066
 Neurosurg Rev

24. Riley HA (1960) An atlas of basal ganglia, brain stem and spinal as adopted for the equivalent segment of the inferior cerebellar pedun-
cord. Hafner, New York cle, which, in our understanding, is a more “surgical” term that would
25. Salamon N, Sicotte N, Drain A, Frew A, Alger JR, Jen J, Perlman enhance its comprehension.
S, Salamon G (2007) White matter fiber tractography and color Also regarding denominations, now related to the current utilization
mapping of the normal human cerebellum with diffusion tensor of different types of stereoscopic images, maybe the expression “three-
imaging. J Neuroradiol 34:115–128 dimensional (3D) relationships” could be changed to “spatial relation-
26. Tomita T (1986) Surgical management of cerebellar peduncle ships” or to “tridimensional relationships”, leaving the expression
lesions in children. Neurosurgery 18:568–575 “three-dimensional (3D)” only to designate generically stereoscopic
27. Türe U, Yasargil MG, Friedman A, Al-Mefty O (2000) Fiber images. Congratulations for your excellent article.
dissection technique: lateral aspect of the brain. Neurosurgery 47
(2):417–427
28. Walker AE, Botterell EH (1937) The syndrome of the superior João Paulo C. de Almeida and Evandro de Oliveira, São Paulo, Brazil
cerebellar peduncle in monkey. Brain 60:329–353 We would like to congratulate Perrini et al. for the excellent de-
29. Yasargil MG (1984) Microneurosurgery: microsurgical anatomy of scription of the anatomical nuances of the cerebellar peduncles. The
the basal cisterns and vessels of the brain, diagnostic studies, authors present in a detailed fashion the microsurgical anatomy of the
general operative techniques and pathological considerations of cerebellar peduncles and their white fibres using the Klinger’s method
the intracranial aneurysms, vol I. George Thieme-Verlag, Stuttgart of white dissection with the support of the operating microscope. The
30. Yasargil MG (1988) Microneurosurgery: AVM of the brain, clini- high-quality 3D images presented adequately demonstrate such com-
cal considerations, general and special operative techniques, sur- plex anatomy, facilitating the comprehension of the manuscript.
gical results, nonoperated cases, cavernous and venous angiomas, As an original contribution, the authors describe the complex anat-
neuroanesthesia, vol IIIB. George Thieme-Verlag, Stuttgart omy of the intracerebellar segments of the peduncles considering the
31. Yasargil MG (1994) Microneurosurgery: CNS tumors-surgical pathway of the fibres (superior, middle or inferior peduncle) and
anatomy, neuropathology, neuroradiology, neurophysiology, clini- propose a detailed classification of the segments of the peduncles.
cal considerations, operability, treatment options, vol IVA. George According to such classification, the superior cerebellar peduncle is
Thieme-Verlag, Stuttgart divided in three segments: intracerebellar, intermediate and intrateg-
32. Ziyal IM, Sekhar LN, Salas E (1999) Subtons illar- mental; the middle cerebellar peduncle in two segments: cisternal and
transcerebellomedullary approach to lesions involving the fourth intracerebellar; and the inferior cerebellar peduncle in three segments:
ventricle, the cerebellomedullary fissure and the lateral brainstem. cisternal, ventricular and intracerebellar. Such classification, as the
Br J Neurosurg 13(3):276–284 authors comment, may help in the decision of the surgical approach
for cavernomas and arteriovenous malformations affecting the
peduncles. It is important to remember, however, that the surgical route
for brainstem cavernomas must remain the area wherein the lesion
abuts the pial or ependymal surface.
Comments
The authors have added a significative contribution to the literature
regarding the microsurgical anatomy of the brainstem and cerebellar
Antonio Bernardo, New York, USA peduncles. For the neurosurgeons interested in vascular malformations
The authors have performed a detailed, richly illustrated anatomical and brainstem surgery, it represents an interesting guide for the surgical
study of the cerebellar peduncles. The elegant 3D photography helps to planning of such complex procedures.
understand the intricate anatomy of the region. Mastering the complex
anatomy of the cerebellar peduncles and their relationship with adjacent
structures and overlying cerebellar lobules is required in order to attempt Toshio Matsushima, Saga, Japan
the exposure of the fourth ventricle. Several studies have already inves- My congratulations to Dr. Paolo Perrini and the authors for this
tigated the structure and functions of the cerebellum and its connections, paper which shows well-done anatomical study of the cerebellar
providing beautiful 2D photography. A significant problem with this peduncles by using a fibre dissection technique. Each peduncle is
method is the inherent conceptual limitation of conveying or teaching explained being divided into a few segments.
3D relationships via 2D images. The ability to visualize and understand When I studied the anatomy of the fourth ventricle and developed
anatomical spatial relationships is crucial in surgical planning, and the use transcerebellomedurally fissure approach, we did not think of incising
of stereoscopic projection is invaluable for this purpose. The elegant 3D the brainstem at all (1, 2, 3, 4). After development of MRI, however,
representation provided by the authors helps to improve surgeons’ con- many cases of cavernoma have been found as a cause of pontine
ceptual grasp of the complex anatomy of the region. hemorrhage, and now neurosurgeons try to attack an intrinsic lesion
in the brainstem. This study will be useful in incising the brainstem.
If I were to venture an opinion, I would say that the authors should have
Guilherme Carvalhal Ribas, São Paulo, Brazil shown by an illustration which portion of the brainstem should have been
Despite having been based only in five specimens and being more incised and which direction of an incision should be selected in order to
descriptive than analytical (in the sense that it does not evaluate/ minimize the postoperative neurological deficits, though I understand that
describe anatomical variations and/or measure structures) as most of this study had limitation. Recently cavernoma in the pons is removed not
the surgical anatomy articles, and in spite of the density of the topic only through the floor of the fourth ventricle but also through the lateral
itself (complex cerebellar and brainstem nuclei and tracts), the article wall of the pons including the middle cerebellar peduncle (5). It is because
definitely describes very well the surgical anatomy pertinent to these the injury of the middle cerebellar peduncle develops lower morbidity than
structures, and the 3D illustrations, as usually, enhance very much its that of the floor of the fourth ventricle. In conclusion again my congrat-
comprehension. ulations to Dr. Perrini for this well-done paper.
The didactic division of the cerebellar peduncles into topographic
segments here proposed is very appropriate for posterior fossa micro- References
neurosurgery, and the text is very well subdivided. Regarding their 1. Kawashima M, Matsushima T, Nakahara Y, Takase Y, Masuoka
naming, maybe the intermediate segment of the superior cerebellar J, Ohata K (2009) Trans-cerebellomedullary fissure approach with
peduncle (SCP) could be designated as SCP intraventricular segment, special reference to lateral route. Neurosurg Rev 32:457–464
Neurosurg Rev

2. Matsushima T, Fukui M, Inoue T, Natori Y, Baba T, Fujii K contributes to our understanding of the complex anatomy of the cerebel-
(1992) Microsurgical and magnetic resonance imaging anatomy of the lum and the three cerebellar peduncles. However, concentrating with
cerebello-medullary fissure and its application during fourth ventricle anatomical studies solely upon the neural tissue after having removed
surgery. Neurosurgery 30:325–330 the arachnoid membrane and vascular structures does not completely
3. Matushima T, Inoue T, Inamura T, Natori Y, Ikezaki K, Fukui M reflect the clinical situation at surgery. My experience with primarily
(2001) Transcerebellomedullary fissure approach with special refer- intrinsic brainstem lesions comprises over 250 surgical cases treated for
ence to methods of dissecting the fissure. J Neurosurg 94:257–264 cavernous malformations and gliomas. Only a part of these lesions were
4. Matsushima T, Abe H, Kawashima M, Inoue T (2012) Exposure readily visible on the surface of the brainstem and thus directly accessible.
of the wide interior of the fourth ventricle without splitting the vermis: In a great number of cases, the surface of the brainstem showed at
importance of cutting procedures for the tela choroidea. Neurosurg Rev exposure either an apparently normal aspect or perhaps a bulging or
DOI 10.1007/s10143-012-0384-3 discoloration in case of an intraaxial hemorrhage. In all these cases, I
5. Ohue S, Fukushima T, Friedman A, Kumon Y, Ohnishi T (2010) had to penetrate the pial surface at some point and enter into the brainstem
Retrosigmoid suprafloccular transhorizontal fissure approach for resec- to reach the underlying pathological lesion. I am convinced that choosing
tion of brainstem cavernous malformation. Neurosurgery 66(ONS the optimal location for this entry point was of crucial importance for the
Suppl 2): ons306–ons313 surgical result. In my experience, the selection of the entry point into the
brainstem was not only dictated by the location of the intrinsic fibre
system and nuclei but also by the (quite variable) vascular anatomy on
Helmut Bertalanffy, Hannover, Germany the surface of the brainstem. Particularly the area of the cerebellomesen-
The authors are to be commended for this detailed anatomical de- cephalic fissure contains an abundant vascular network. I was very careful
scription of the cerebellar peduncles using the white matter dissection in preserving perforating arteries supplying the brainstem and superficial
technique. A detailed anatomical knowledge is always an important draining veins as much as possible, which also influenced my choice of
prerequisite for safe surgery in this area, and this nicely illustrated article the optimal entry point into the brainstem.

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