ORIGINAL ARTICLE

Three-dimensional microsurgical anatomy of cerebellarpeduncles

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 pedunclesand their relationships with neighbouring fasciculi were in-vestigated by using a fibre dissection technique. As the dis-section progressed, photographs of each progressive layerwere obtained and stereoscopic images were created usingthe 3D anaglyphic method. These findings provided the ana-tomical basis for a conceptual division of cerebellar pedunclesinto segments. The middle cerebellar peduncle (MCP) wasdivided into two segments: cisternal and intracerebellar seg-ments. The inferior cerebellar peduncle (ICP) was divided intothree segments: cisternal, ventricular and intracerebellar seg-ments. The superior cerebellar peduncle (SCP) was dividedinto three segments: intracerebellar, intermediate and intra-tegmental segments. The fibre dissection technique discloseda constant course of peduncular fibres inside the white core ofthe cerebellum. The pontocerebellar fibres of the MCP passover and laterally to the bundles of the ICP and SCP. Thecentripetal fibres of the ICP wrap around the radiation of theSCP and the dentate nucleus, directed towards the cortex ofthe vermis. The centrifugal bundle of the SCP ascends to-wards the mesencephalon where it sinks passing below thefibres the lateral lemniscus. The knowledge gained by study-ing the intrinsic anatomy of the cerebellum is useful to ac-complish appropriate surgical planning and, ultimately, tounderstand the repercussions of surgical procedures on thewhite matter tracts in this region.

Keywords Cerebellar peduncles . Dentate nucleus . Fibredissection technique . Three-dimensional anatomy .Whitematter tracts

Introduction

The cerebellar peduncles are three paired, symmetricallyplaced bundles of white matter concentrating fibres, whichenter and leave the cerebellum with complex anatomicalthree-dimensional (3D) relationships. Compared with theseveral published investigations relating to the structureand functions of the cerebellum and its connections, fewstudies described the detailed topographic anatomy ofcerebellar peduncles and their relationship with adjacentstructures and overlying cerebellar lobules [3, 12, 13,15, 22, 24].

In proceeding with operative exposures of the fourthventricle, a detailed knowledge of 3D relationships be-tween the cerebellar peduncles and the fourth ventricleand superficial anatomy of cerebellum is mandatory.Such surgical exposures are required for resection oftumors of the fourth ventricle and resection of neoplastic orvascular lesions of its floor. In addition, the cerebellarpeduncles can be the site of pathological processes such asneuroepithelial tumors and vascular malformations; hence,understanding the morphological characteristics of these ner-vous structures is crucial in performing safe surgery in thisregion.

In this study we attempt to improve our understanding ofthe topographic anatomy of cerebellar peduncles by apply-ing the operating microscope to Klinger’s method of whitematter fibre dissection [11, 27]. Stereoscopic images pro-duced using the anaglyphic technique are provided to facil-itate 3D comprehension of these anatomical structures.

P. Perrini (*) :G. Tiezzi : R. VannozziDepartment of Neurosurgery,Azienda Ospedaliero Universitaria Pisana (AOUP),Via Paradisa 2, 56100 Pisa, Italye-mail: p.perrini@ao-pisa.toscana.it

M. CastagnaDepartment of Human Pathology, University of Pisa,Pisa, Italy

Neurosurg RevDOI 10.1007/s10143-012-0417-y

Materials and methods

Five normal previously frozen, formalin-fixed human brainswere dissected under the operating microscope (×3–40 mag-nification) by using fibre dissection technique originallydescribed by Ludwig and Klinger [11]. The brains wereobtained from fresh autopsy specimens and were fixed in10 % formalin for at least 1 month. The arachnoid mem-brane and vascular structures were carefully removed, andthe brains were frozen at −15 °C for 15 days. Before thedissection began, the brains were washed under runningwater and allowed to thaw. The cerebellum was dissectedfrom the superior and lateral aspects in a stepwise mannerusing wooden spatulas with tips of various sizes and micro-surgical dissectors. This technique enabled complete dissec-tion of fibre bundles and allowed description of anatomicalrelationships of cerebellar peduncles, especially in theircourse in the white core of the cerebellum. In two additionalspecimens, the cerebellum was sliced along the axial andcoronal plane to demonstrate the relationships of the cisternalsegments of peduncles with the white core of the cerebellumand the dentate nucleus. The stereoscopic illustrations pre-sented here were performed with the anaglyphic technique aspreviously described in the literature [23].

Results

Basic anatomic configuration of cerebellar peduncles

The middle cerebellar peduncle (MCP) or brachium pontisis the largest afferent system of the cerebellum and is com-posed of pontocerebellar fibres running from the pontinenuclei and the nucleus reticularis tegmenti ponti locatedmainly on the contralateral side [8, 17, 18, 21]. This largewhite matter tract connects the pons with the cerebellum andhas a cisternal and an intracerebellar segment (or MCPradiation, Fig. 1). The cisternal segment of MCP beginslateral to the apparent origin of the cranial nerve (CN) Vand includes the rostral and the lateral surface of the initialpart of the peduncle (Fig. 1a). The rostral surface of theMCP runs in the cerebellomesencephalic fissure where itforms the lateral part of the inner wall of the fissure(Fig. 1a). The lingula and the dorsal or cisternal surface ofsuperior cerebellar peduncles (SCP) constitute respectivelythe posterior and the anterior walls of the inner aspect of thefissure. The lateral surface of the MCP runs between the twolimbs of the V-shaped cerebellopontine fissure. The intra-cerebellar segment begins where the pontocerebellar fibresbecome deep with respect to the cerebellar lobules limitingthe cerebellomesencephalic and pontocerebellar fissures(Fig. 1b, c). The MCP enters the cerebellum on the lateralside of the large peduncolar mass formed by the three

cerebellar peduncles that connects the brainstem and cere-bellum (Fig. 1g, h).

The SCP or brachium conjunctivum consists of efferentfibres from the dentate, globose and emboliform nuclei to thered nucleus of the opposite side [17, 18, 21]. This centrifugalwhite matter system has an intracerebellar (or SCP radiation),an intermediate and an intrategmental segment (Fig. 1a–d, g, h).

Fig. 1 2D (a–c, e–h) and 3D (d) illustrations of stepwise dissectionsof the tentorial and suboccipital surfaces of the cerebellum to demon-strate the topographic anatomy of the cerebellar peduncles. The 2Dillustrations are labeled to facilitate understanding of the same illustra-tion in 3D. The 3D image should be viewed with red and blue anaglyphglasses. a Superior view of the tentorial surface after removal of thequadrangular lobule and culmen with wide exposure of the cerebello-mesencephalic fissure. The lingula and the cisternal surface of superiorcerebellar peduncle constitute respectively the posterior and the ante-rior walls of the inner aspect of the fissure and the superior and medialaspect of the middle cerebellar peduncle forms, in each side, its mostlateral limit. The cisternal segment of the middle cerebellar pedunclebegins lateral to the apparent origin of the CN V. The superior cere-bellar peduncle ascends at the lateral edges of the superior medullaryvelum to enter the midbrain below the inferior colliculus. The inter-peduncular sulcus separates the cisternal segments of the middle andsuperior cerebellar peduncles. b The white core of the cerebellum hasbeen divided with an axial at the level of the dentate nucleus in whichthe centrifugal fibres of the superior cerebellar peduncle arise. Theinterpeduncular sulcus, which separates the middle and superiorpeduncles, joins superiorly the lateral mesencephalic and the pontome-sencephalic sulci and ends caudally into a narrow pouch, the para-brachial recess. c Additional cerebellum has been removed with acoronal cut at the level of tonsillar peduncle. The tonsillar peduncle,located along the superior margin of the tonsil, attaches the tonsil to thewhite core of the cerebellum, inferior and lateral to the dentate nucleus.d 3D illustration of the figure labeled in c. e The left tonsil has beenremoved by dividing its peduncle. Removing the tonsil exposes thelower part of the roof of the fourth ventricle and the cisternal segmentof the inferior cerebellar peduncle, which is not sharply demarcatedfrom the more caudally placed gracile and cuneate tubercles. Thecisternal segment of the inferior cerebellar peduncle terminates at theattachment of the tela chorioidea to the taenia. f The tela chorioidea hasbeen removed to expose the ventricular segment of the inferior cere-bellar peduncle, which forms the floor, and the rostral wall of thelateral recess. g Additional cerebellum has been removed to exposepart of the floor of the fourth ventricle and the large peduncular masswhere the cerebellar peduncles converge. The inferior medullary velumand the tonsil have been displaced downward to expose the supero-lateral recess. The dentate tubercle is anterior to the lateral margin ofthe inferior medullary velum. h The full length of the floor of the fourthventricle has been exposed. In the lateral recess, the dorsal cochlearnucleus produces a smooth prominence on the ventricular segment ofthe inferior cerebellar peduncle, the auditory tubercle. The union of thecerebellar peduncles forms a large fibre bundle, which lines the ven-tricle. The fibres of superior and inferior cerebellar peduncles form theventricular surface of this peduncular mass, whereas the middle cere-bellar peduncle runs more laterally. Cent., central; Cer., cerebellar;Cer.Mes., cerebellomesencephalic; Cer. Ped., cerebral peduncle; Cist.,cisternal; CN, cranial nerve; Coch., cochlear; Coll., colliculus; Dent.,dentate; Fiss., fissure; Horiz., horizontal, Inf., inferior; Interped., inter-peduncular; Intracer., intracerebellar; Lat., lateral; Med., median, med-ullary; Mes., mesencephalic; Mid., middle; Nucl., nucleus; Parabrach.,parabrachial; Ped., peduncle; Quad., quadrangular; Rec., recess; Seg.,segment; Sup., superior; Surf., surface; Tub., tubercle; Vel., velum;Vent., ventricular

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The intermediate segment forms the cisternal and ventricularsurfaces of the superolateral part of the roof of the fourthventricle (Fig. 1a–d, g). The dorsal or cisternal surface ofintermediate segment is located in the cerebellomesencephalicfissure and forms longitudinal prominences ascending on themedial side of the MCP to enter the midbrain beneath theinferior colliculi (Fig. 1a, b). The inner or ventricular surfaceof intermediate segment forms the lateral ventricular part of thesuperior portion of the fourth ventricle (Fig. 1g, h). The superiormedullary velum is a thin semitranslucent lamina of whitematter, which stretches between the superior cerebellarpeduncles and forms the median part of the superior portionof the fourth ventricle. The cisternal surfaces of thesuperior and middle cerebellar peduncles are separated by

the interpeduncular sulcus, which is a shallow groove joininganteriorly the pontomesencephalic sulcus and superiorly thelateral mesencephalic sulcus (Fig. 1b). At the caudal tip of theinterpeduncular sulcus is the parabrachial recess, which is anarrow pouch formed by the convergence of cisternal seg-ments of superior and middle cerebellar peduncles (Fig. 1b).

The inferior cerebellar peduncle (ICP) ascends along thelateral border of the fourth ventricle and consists of thelateral, afferent restiform body and the medial principallyefferent juxtarestiform body [17, 18, 21]. The restiformbody is composed of two main fascicles: the dorsal spino-cerebellar tract, and the olivocerebellar fibres from the con-tralateral inferior olive [21]. In addition, fibres from thelateral cuneate nucleus of the same side (dorsal external

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arcuate fibres) and from the reticular and arcuate nuclei(ventral external arcuate fibres) compose the restiform body[21]. The medial part of the ICP (juxtarestiform body) con-sists of vestibulocerebellar fasciculus composed of ascendingbranches of the vestibular nerve directed to the vestibular partof the cerebellum [21]. The ICP can be divided into threesegments from caudal to rostral, namely a cisternal, aventricular and an intracerebellar segment (or ICP radiation,Fig. 1e–g). The cisternal segment of the ICP lies between theinferolateral edges of the fourth ventricle, where the telachorioidea is attached to the taenia, and the postolivary sulcus,where the glossopharyngeal and the vagus nerves arise(Fig. 1e, f). There is no definite demarcation between theICP and the more caudally placed gracile and cuneatetubercles (Fig. 1e, h). The ventricular segment of the ICPbegins at the line of attachment of the tela chorioidea to thetaenia and courses upward and laterally in the floor ofthe lateral recess (Fig. 1e, f). The dorsal cochlear nu-cleus produces an eminence, the auditory tubercle, on

this segment of the ICP (Fig. 1h). At this level, avarying number of striae medullares running diagonallyor horizontally cross the peduncle. The ventricular segment ofthe ICP makes a sharp turn dorsally to enter the white core ofthe cerebellum on the inferomedial part of the fibrebundle formed by the union of the three cerebellarpeduncles (Fig. 1g, h).

The fibres of the three peduncles blend in a large whitematter bundle lining the ventricular surface of the rostralwall of lateral recess and the inferior portion of the lateralpart of the fourth ventricle (Fig. 1g, h). The fibres of supe-rior and inferior peduncles form the ventricular surface ofthis large peduncular mass, whereas the middle peduncleruns more laterally. In fact, the intrinsic anatomy of thepeduncular mass and the relationships of peduncular radia-tions are not disclosed with standard anatomical dissection.The fibre dissection technique enables complete exposure ofthe cerebellar peduncles and their radiations within thecerebellar white matter (Fig. 2a–c).

Fig. 2 Illustrations demonstrating a general overview of the cerebellarpeduncles and their radiations within the white core of cerebellum. aThe inferior cerebellar peduncle is highlighted in shades of blue, thesuperior cerebellar peduncle in shades of red and the middle cerebellarpeduncle in shades of yellow. The cisternal segment of the middlecerebellar peduncle has been transected to expose the fibres of theinferior and superior cerebellar peduncles. The infradentate bundle(asterisk) is a fasciculus of the intracerebellar segment of the middlecerebellar peduncle running inferior to the dentate nucleus andconnected with the tonsillar peduncle. a, dentate nucleus; b, auditory

tubercle; c, red nucleus; d, cranial nerve V; e, cranial nerve III; f, cranialnerve II; g, olfactory tract; h, anterior commissure. b Illustrationdemonstrating the segments of the inferior cerebellar peduncle. Thecisternal segment is highlighted in horizontal lines, the cisternal seg-ment in solid color and the intracerebellar segment in vertical lines. cIllustration demonstrating the segments of the superior cerebellar pe-duncle. This peduncle, which is mainly composed by fibres originatingfrom the dentate nucleus directed toward the red nucleus of the oppo-site side, presents an intracerebellar (1), an intermediate (2), and anintrategmental segment (3)

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Fibre dissection of the middle cerebellar peduncle

The pontocerebellar fibres in the ventral part of thepons are organized in three transverse orientated layers,superficial, intermediate and deep, divided by the pyra-midal fibres, which run as discrete fasciculi in themiddle layer. The cisternal segment of the MCP beginsdistally to the apparent origin of the CN V where thepontocerebellar fibres merge together and is situated inthe cerebellopontine fissure laterally and in the cerebel-lomesencephalic fissure superomedially. Removal of thecortical gray matter of the quadrangular and simplelobules exposes the underlying white matter organizedin laminae, which are the projections into the lobules ofthe white medullary body (Fig. 3a). The removal ofcerebellar laminae exposes the MCP radiation. As the dissec-tion of the MCP progresses, the radiation pattern of its fibresfrom the pontine nuclei to the cerebellar cortex is progressive-ly disclosed. The pontocerebellar fibres of the intracerebellarsegment of the MCP run with a posterior and medialorientation and show terminations in all lobules of thecerebellum, with the exception of the nodulus and theflocculus (Fig. 3b, c). Just anterior to the dentate nucle-us, the fibres of the MCP are divided into the thicker supra-dentate and slender infradentate bundles (Fig. 3b). Theinfradentate bundle of the MCP provided connections withthe tonsillar peduncle (Fig. 3b). Removal of the deep ponto-cerebellar fibres exposes the purse-like prominence of thedentate nucleus located posterior and inferior to the deepcentripetal fibres of the ICP, lateral to the fastigium and abovethe superolateral recess of the fourth ventricle (Fig. 3d, e).

Fibre dissection of the inferior cerebellar peduncle

Removal of the deep fibres of MCP exposes the centripetalfibres of the ICP traversing from lateral to medial the centralcore of cerebellum, with a slightly posterior direction towardsthe cortex of the vermis and to a lesser extent to the cortex ofthe cerebellar hemisphere (Fig. 3d, e). The superficial fibres ofICP wrap around the dentate nucleus and arch medially to-wards the vermis. A characteristic white matter prominence iscreated by the fibres of ICP crossing the dentate nucleus. Thedeep fibres of ICP proceed in a groove located at the junctionof the dentate nucleus and the initial portion of the SCP(Fig. 3d, e). On the basis of the different orientation of bothwhite matter tracts on the medial side of the peduncular mass,they could be progressively dissected and differentiated. Thefibres of trigeminal nerve are observed ventromedial to theICP and posterior to the lateral and medial lemnisci. At theanterior portion of white core of the cerebellum, the fibres ofICP form the posterior boundary of parabrachial recess, whichis a triangular pouch lined by the SCP on its medial side andby the MCP on its lateral side.

Fibre dissection of the superior cerebellar peduncle

Removal of the ICP fibres exposes the SCP radiation, whicharises from the dentate, globose and emboliform nuclei(Fig. 3f, g). The dentate nucleus consists of well-defined,island-like almost parallel bars of gray matter that are sep-arated from each other by shallow grooves filled with whitematter. In close relation to the hilus of dentate nucleus,delicate efferent fibres converge to form the SCP. On thesuperolateral surface of the fourth ventricle, the dentatenucleus, covered only by the ependyma and by a tiny layerof pontocerebellar fibres, produces a discrete prominence,the dentate tubercle. The fastigial nucleus is positioned nextto the midline. The globose nuclei and the emboliformnucleus are situated in an intermediate position. The inter-mediate segment of SCP emerges as distinct fibre bundlefrom the white core of cerebellum and ascends towards themesencephalon where it progressively sinks after passingbelow the fibres of the lateral lemniscus, which bordercaudally the lemniscal trigone (Fig. 3h–j).

Relationship between the cerebellar peduncles and otherfascicles

Ventral spinocerebellar tract The ventral spinocerebellartract, which consists of fibres originating from the cells ofposterior gray column of the same and opposite side, con-veys proprioceptive information to the cerebellum. Dissec-tion of the ventral spinocerebellar tract was difficult becauseof its small size and could be not dissected accurately. Theventral spinocerebellar tract runs through the pontine retic-ular formation and turns dorsolaterally at the rostral end ofthe pons [18]. This small afferent bundle courses over thedorsolateral surface of SCP and passes rostral to the fibres oftrigeminal nerve to enter the cerebellum.

Lateral lemniscus The lateral lemniscus is the central audi-tory tract from the cochlear nuclei towards the inferiorcolliculus and the inferior quadrigeminal brachium. Thefibres of lateral lemniscus, which are the continuation ofthe trapezoid body, ascend from the tegmental part of thepons where they are located laterally to the medial lemnis-cus and dorsally to the deep stratum of pontocerebellarfibres. In their course towards the inferior colliculus, thefibres of lateral lemniscus turn dorsolaterally until theyoccupy a position on the superolateral aspect of the SCPmarking the transition between the cisternal and the intra-tegmental part of the peduncle (Fig. 3h–j).

Medial lemniscus The medial lemniscus is a broad bundleof longitudinal fibres, which arise from the nuclei gracile,and cuneatus of the opposite side. These fibres conveysensory impulses from the muscles, joints and tendons, as

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well some elements of tactile sensibility. This bundle islocated ventromedially in the tegmental part of the ponsand shifts progressively to the lateral portion of the tegmen-tum of the mesencephalon displaced by the red nucleus(Fig. 3h–j). Due to this dorsolateral displacement, the me-dial lemniscus is ventral to the SCP in the rostral part of thepons and becomes laterally placed to the SCP at the level ofthe inferior colliculus where it lies at the ventrolateral borderof the tegmentum close to the substantia nigra (Fig. 3j).

Several observations about the spatial relationships of theintracerebellar segment of cerebellar peduncles can bemade. First, in all 10 cerebellar hemispheres that weredissected, the pontocerebellar fibres of MCP covered thewhite matter tracts of inferior and superior cerebellarpeduncles running with horizontal or slightly oblique direc-tion. Second, progressive dissection of the MCP superior tothe apparent origin of the trigeminal nerve in the direction ofthe deep layer of pontocerebellar fibres will produce an alleydirected towards the basilar pons limited ventrally by thecorticospinal tract and dorsally by the medial and laterallemnisci. Third, in all specimens, the tonsillar pedunclewas attached to the infradentate bundle of the MCP, which,in turn, was posterior to the initial part of the ICP radiation.Fourth, the dentate nucleus at the level of superolateralrecess is covered by a tiny layer of pontocerebellar fibreson its ventricular side and is medial and inferior to the ICPradiation.

Discussion

Nomenclature of cerebellar peduncles

Surgical exposure of cerebellar peduncles is a critical com-ponent of many neurosurgical approaches for neoplastic andvascular lesions located in the posterior fossa. Surgicalapproaches must be tailored to the site of the pathologicalfindings with a thorough understanding of the anatomy ofthis region. Microsurgical anatomy of cerebellar peduncleshas been described by Matsushima et al. [13] and by Rhoton[22], but a segmental nomenclature has not been establishedin neurosurgical literature. In addition, controversies remainregarding the course of the cerebellar peduncles at the levelof the white core of the cerebellum because of the admixtureof peduncular fibres, which assume complex 3D relation-ships. In 1986, Tomita subdivided the intracerebellar seg-ment of peduncles into three portions (i.e. brain stemportion, ventricular portion and cerebellar portion) by usingtwo arbitrary reference lines superimposed on a cross sectionof the brainstem and the cerebellum at the midpontine level[26]. Tomita’s report did not consider the intracerebellar seg-ments of peduncles as separate structures and described thethree distinct bundles in the white core of cerebellum as a

single cerebellar peduncle [26]. Tomita’s classification is use-ful for understanding the location and extension of a cerebellarlesion, but is anatomically inaccurate. In this report, we pro-pose a nomenclature, which describes the segments of thecerebellar peduncles according to a detailed understandingof the compartments through which they travel. In addition,by applying the operating microscope to Klinger’s method offibre dissection, we could dissect the white core of the cerebel-lum and demonstrate the intracerebellar course of peduncles.Our dissections disclosed a constant course of peduncularfibres inside the white core of the cerebellum. The pontocer-ebellar fibres of MCP course with a posteromedial directionand pass over and laterally the bundles of the inferior andsuperior cerebellar peduncles. The centripetal fibres of ICPafter a sharp turn in the roof of the lateral recess pass mediallyto the MCP fibres and wrap around the fibres of SCP and the

Fig. 3 2D (a, b, d, f, h, j) and 3D (c, e, g, i) illustrations of stepwisefibre dissection of the right hemisphere and cerebellar peduncles. The2D illustrations are labeled to facilitate understanding of the sameillustration in 3D. The 3D images should be viewed with red and blueanaglyph glasses a Extensive dissection of the lateral aspect of thebrain reveals the corona radiata which joins the internal capsule, thesagittal stratum and the mediobasal temporal region. The cerebellargray matter has been removed, and the basilar pons has been dissected.The pontocerebellar fibres merge together distally to the apparentorigin of the CN V where they form the middle cerebellar peduncle,which courses superficial and laterally to the inferior and superiorcerebellar peduncles. b The middle cerebellar peduncle has been par-tially removed (asterisk) while preserving its deep layer of pontocer-ebellar fibres, which spread around the prominence, created by thedentate nucleus. A bundle of pontocerebellar fibres running below thedentate nucleus (the infradentate bundle, arrows) joins with the tonsil-lar peduncle. c 3D illustration of the figure labeled in b. d The middlecerebellar peduncle has been transected and its fibres removed toexpose the centripetal fibres of the inferior cerebellar peduncle, whichreach the cortex of the vermis and to a lesser extent the cortex of thehemisphere. In addition, the postero-lateral fibres of the inferior cere-bellar peduncle have been removed to expose the parallel bars of graymatter of the dentate nucleus. e 3D illustration of the figure labeled ind. f the radiation of the inferior cerebellar peduncle has been partiallytransected (arrowheads) to fully expose the superior cerebellar pedun-cle, which arises from the dentate nucleus and ascends towards themesencephalon where it sinks after passing below the fibres of thelateral leminscus. g 3D illustration of the figure labeled in f. h Supero-lateral view of another specimen. The white matter of the right cere-bellum has been dissected, and a sagittal section of the basilar part ofthe pons has been made to demonstrate the relationship of the pyrami-dal tract with the medial and lateral lemnisci. i 3D illustration of thefigure labeled in h. j Enlarged view of h. The fibres of the laterallemniscus run toward the inferior colliculus on the superolateral aspectof the superior cerebellar peduncle and mark the transition between thecisternal and the intrategmental part of the peduncle. Ant., anterior;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;Int., internal; Intracer., intracerebellar; Lat., lateral; Lemn., lemniscus;Med., medial; Mid., middle; Nucl., nucleus; Pall., pallidus; Ped., pe-duncle; Plex., plexus; Pyram., pyramidal; Rad., radiata; Sag., sagittal;Seg., segment; Spinocer., spinocerebellar; Subs., substantia; Sup.,superior

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dentate nucleus, directed towards the cortex of the vermis.Removal of fibres of ICP exposes the centrifugal bundle ofSCP, which ascends towards the mesencephalon inferior theICP fibres and inferomedial the MCP bundle. Lesions of cer-ebellar peduncles are usually described generically in the liter-ature, indicating the peduncle affected without reporting theexact lesion location [10, 26]. The proposed nomenclatureallows localizing precisely a pathological process in the cere-bellar peduncles. Careful anatomical description of a peduncu-lar lesion is relevant since it dictates the surgical approach. Forexample, a cavernous malformation of the cisternal portion ofICP requires a midline suboccipital craniotomy and dissectionof the inferior extension of the cerebellomedullary fissure, theso-called medullotonsillary space [14]. On the other hand, acavernous malformation of the ventricular portion of the ICPrequires exposure of the lateral recess with elevation of thetonsil and division of the tela chorioidea using the telovelarapproach [6, 7, 16, 32]. Thanks to the technological advancesin magnetic resonance imaging, the precise location of a pe-duncular lesion can now be preoperatively identified. In addi-tion, the development of diffusion tensor (DT) tractographyallows the study of the intrinsic structure of cerebellum and thecreation of maps of white matter connectivity [1, 25]. The 3Drelationships of the intracerebellar segments of peduncles dis-closed in our dissections are similar to those obtained with DTtractography [1, 25]. 3D anatomical knowledge of the whitematter pathways of the cerebellum acquired with fibre dissec-tion improves the spatial understanding of tractographic recon-structions of cerebellar peduncles, especially when there iscompression and displacement of bundles in the presence ofpathological processes.

Cerebellar peduncles, clinical relevance and surgicalapproaches

To reach lesions in and around the cerebellar peduncles,surgeons must use strategies to avoid transgressing thepeduncular fibres and the cerebellar nuclei, since devastat-ing morbidity has been historically reported to occur. TheMCP is located on the cisternal surface of the large pedun-cular mass where all peduncles converge and may be injuredduring operations on lesions involving the cerebellomesen-cephalic and pontocerebellar fissures. Lesions of the MCPinduce ataxia, hypotonia and dysmetria on the same side ofthe lesion similar to that caused by injury of the lateral partof the hemisphere [2, 13]. In fact, clinical experience sug-gests that the MCP tolerates small neurotomies to accesspeduncular lesions that do not reach the surface (i.e. intrinsiclesions) [19]. The incision must be made on the dorsalsurface of the MCP parallel and longitudinal to respect thepontocerebellar fibres [19]. Recently, transgression of theMCP has been proposed to resect intrinsic lesions of thebasilar pons with relatively low morbidity [5]. The lateral

transpeduncular approach requires a small neurotomy rostralto the apparent origin of the trigeminal nerve and gentledissection along the pontocerebellar fibres [5]. According toour results, when such an approach is directed towards thedeep layer of pontocerebellar fibres, the anatomical bound-aries to be respected are the corticospinal tract ventrally, thetrigeminal nerve caudally and the medial and lateral lemnisciposteriorly in the tegmental pars of the pons. The lateraltranspeduncular approach is suited for intrinsic cavernousmalformations of the basilar pons in symptomatic patients [5].

The ICP can be damaged when approaching pathologicalprocesses involving the medullotonsillar space and the lateralrecess of the fourth ventricle. Experimental sectioning of theICP induces disturbances of the equilibrium with truncalataxia, staggering gait and tendency to fall towards the sideof the lesion [20]. These disturbances are analogous to thoseproduced by lesion of the flocculonodular lobe [13, 20].Similarly, the consequence of surgical removal of tumorsattached to the floor of the lateral recess can be temporarydisequilibrium [6]. The use of natural clefts in the cerebello-medullary fissure to avoid sacrifice of normal cerebellar tissue(i.e. the transvermian approach) was initially described byYasargil who entered the fourth ventricle through the “tonsil-louveal” sulcus, along the medial division of the posteriorinferior cerebellar artery [30, 31]. Subsequently, refinementsof the transcerebellomedullary fissure approach have beendescribed by different authors [14, 16]. The “lateral recessopeningmethod” proposed byMatsushima et al. [14] providesexposure of the ventricular portion of the ICP elevating thetonsil, cutting the unilateral taenia and extending the telaropening laterally towards the lateral recess. This approachwas duplicated with minor modifications by Ziyal et al. [32]and by Jean et al. [6] with satisfactory results in managementof tumors in the lateral recess. Recently, Lawton et al. [10]proposed a supratonsillar trajectory through the tonsillobiven-tral fissure to resect cavernous malformations of the ICP. Thisapproach relies on extraventricular route, requires inferome-dial retraction of the tonsil and transgresses the tonsillar pe-duncle to reach the ICP [10]. Our fibre dissection indicatesthat the supratonsillar approach exposes the initial part of theradiation of the ICP, at the level where its centripetal fibresrunning from the roof of the lateral recess arch mediallycrossing the dentate nucleus. In fact, such an approach risksinjury of the dentate nucleus, which is located just above thetonsillar peduncle. If the dentate nucleus is damaged, equili-bratory disturbances, intention tremor, dyskinesia and dysto-nia can occur [4, 9].

Lesions of the SCP induce symptoms similar to thoseof the dentate nucleus. The symptoms are generally mildand transient in case of partial sectioning of the peduncle[28].

The paramedian supracerebellar approach first described byYasargil [29] for aneurysms of the superior cerebellar artery

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provides access to the cisternal surface of the intermediatesegment of the SCP. Dissecting along the tentorial surface ofthe cerebellum, 2 to 3 cm from the midline, allows opening thecerebellomesencephalic cistern and exposure of the SCP justafter retraction of the quadrangular lobule [29]. Pathologicalconditions of the SCP extending into the fourth ventricle re-quire an intraventricular ruote to obtain full exposure of thepathological process. The “lateral wall opening method” de-scribed by Matsushima et al. [14] provides exposure of thelateral wall of the fourth ventricle, which is composed ofcerebellar peduncles forming themedial (or ventricular) surfaceof the large peduncular mass (superior and inferior cerebellarpeduncles). This approach permits access to the superolateralrecess and exposure of the dentate tubercle, which is locatedanterior to the lateral margin of the inferior medullary velum.Our fibre dissections indicate that at this level, only the epen-dyma and a tiny layer of pontocerebellar fibres cover theinferior surface of the dentate nucleus, which is located inferiorto the ICP radiation. In fact, if a lesion involves the peduncularcomplex, the approach through the lateral wall should bechosen only in case of ependymal representation, in order tolessen procedure-associated morbidity by avoiding transgres-sion of the dentate nucleus.

Limitations of the study

The main limitation of this study was the lack of a detailedmorphometric description of peduncular bundles. Thisshortcoming stems from the tissue dehydration due to for-malin fixation using Klinger’s technique, with resultantinaccurate morphometric data. In addition, fibre dissectiontechnique revealed a constant topographic anatomy of pe-duncular fibres inside the white core of cerebellum, but didnot disclose the precise origin and termination of the fibresof each fasciculus, which depends on the gray matter.

Conclusion

The Klinger’s dissection technique has proven valuable inunderstanding the intrinsic anatomy of the cerebellum andthe spatial relationship of its peduncles. A practical termi-nology for segmental anatomy of cerebellar peduncles thatis of surgical significance has been provided. Applying thedetailed knowledge of the white matter tracts to preoperativeplanning of surgical procedures around the cerebellarpeduncles may improve the surgical strategy and decreasethe morbidity for complete removal of tumors and vascularmalformations in this region.

Acknowledgments We thank Nicola Benedetto Ph.D., M.D., for theillustrations of cerebellar peduncles.

References

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3. Foville ALF (1844) Traité Complet de l’Anatomie, de la Physio-logie et de la Pathologie du Système Nerveux Cérébrospinal.Fortin, Masson et Cie, Paris

4. Fraioli B, Guidetti B (1975) Effects of stereotactic lesions of thedentate nucleus of the cerebellum in man. Appl Neurophysiol 38(2):81–90

5. Hebb MO, Spetzler RF (2010) Lateral transpeduncular approach tointrinsic lesions of the rostral pons. Neurosurgery 66(Suppl 1):ONS26–ONS29

6. Jean WC, Abdel Aziz KM, Keller JT, van Loveren HR (2003)Subtonsillar approach to the foramen of Luschka: an anatomic andclinical study. Neurosurgery 52(4):860–866

7. Jittapiromasak P, Sabuncouglu H, Deshmukh P, Spetzler RF, PreulMC (2010) Accessing the recesses of the fourth ventricle: compar-ison of tonsillar retraction and resection in telovelar approach.Neurosurgery 66(Suppl 1):ONS30–ONS40

8. Krieg WJS et al (1966) Functional neuroanatomy, 3rd edn. BrainBooks, Evanston

9. Larsell O (1937) The cerebellum. A review and interpretation.Arch Neurol Psychiatry 38:580–607

10. Lawton MT, Quinones-Hinojosa A, Jun P (2006) The supratonsil-lar approach to the inferior cerebellar peduncle: anatomy, surgicaltechnique, and clinical application to cavernous malformations.Neurosurgery 59:ONS-244–ONS-252

11. Ludwig E, Klinger J (1956) Atlas Cerebri Humani. Karger, Basel12. Luys JB (1865) Recherches sur le Système Nerveux Cérébro-

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the fourth ventricle: part 1. Microsurgical anatomy. Neurosurgery11:631–667

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18. Nieuwenhuys R, Voogd J, van Huijzen C (2008) The humancentral nervous system. Springer, Berlin

19. Ogata N, Yonekawa Y (1997) Paramedian supracerebellar ap-proach to the upper brain stem and peduncolar lesions. Neurosur-gery 40:101–105

20. Pickel VM, Krebs H, Bloom FE (1973) Proliferation ofnorepinephrine-containing axons in rat cerebellar cortex after pe-duncle lesions. Brain Res 59:169–179

21. Ranson SW, Clark SL (1957) The anatomy of the nervous system.Saunders, Philadelphia

22. Rhoton AL Jr (2000) Cerebellum and fourth ventricle. Neurosur-gery 47(3Suppl):S7–S27

23. Ribas GC, Bento RF, Rodrigues AJ (2001) Anaglyphic three-dimensional stereoscopic printing: revival of an old method foranatomical reporting. J Neurosurg 95:1057–1066

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24. Riley HA (1960) An atlas of basal ganglia, brain stem and spinalcord. Hafner, New York

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26. Tomita T (1986) Surgical management of cerebellar pedunclelesions in children. Neurosurgery 18:568–575

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Comments

Antonio Bernardo, New York, USAThe authors have performed a detailed, richly illustrated anatomical

study of the cerebellar peduncles. The elegant 3D photography helps tounderstand the intricate anatomy of the region. Mastering the complexanatomy of the cerebellar peduncles and their relationship with adjacentstructures and overlying cerebellar lobules is required in order to attemptthe exposure of the fourth ventricle. Several studies have already inves-tigated the structure and functions of the cerebellum and its connections,providing beautiful 2D photography. A significant problem with thismethod is the inherent conceptual limitation of conveying or teaching3D relationships via 2D images. The ability to visualize and understandanatomical spatial relationships is crucial in surgical planning, and the useof stereoscopic projection is invaluable for this purpose. The elegant 3Drepresentation provided by the authors helps to improve surgeons’ con-ceptual grasp of the complex anatomy of the region.

Guilherme Carvalhal Ribas, São Paulo, BrazilDespite having been based only in five specimens and being more

descriptive than analytical (in the sense that it does not evaluate/describe anatomical variations and/or measure structures) as most ofthe surgical anatomy articles, and in spite of the density of the topicitself (complex cerebellar and brainstem nuclei and tracts), the articledefinitely describes very well the surgical anatomy pertinent to thesestructures, and the 3D illustrations, as usually, enhance very much itscomprehension.

The didactic division of the cerebellar peduncles into topographicsegments here proposed is very appropriate for posterior fossa micro-neurosurgery, and the text is very well subdivided. Regarding theirnaming, maybe the intermediate segment of the superior cerebellarpeduncle (SCP) could be designated as SCP intraventricular segment,

as adopted for the equivalent segment of the inferior cerebellar pedun-cle, which, in our understanding, is a more “surgical” term that wouldenhance its comprehension.

Also regarding denominations, now related to the current utilizationof different types of stereoscopic images, maybe the expression “three-dimensional (3D) relationships” could be changed to “spatial relation-ships” or to “tridimensional relationships”, leaving the expression“three-dimensional (3D)” only to designate generically stereoscopicimages. Congratulations for your excellent article.

João Paulo C. de Almeida and Evandro de Oliveira, São Paulo, BrazilWe would like to congratulate Perrini et al. for the excellent de-

scription of the anatomical nuances of the cerebellar peduncles. Theauthors present in a detailed fashion the microsurgical anatomy of thecerebellar peduncles and their white fibres using the Klinger’s methodof white dissection with the support of the operating microscope. Thehigh-quality 3D images presented adequately demonstrate such com-plex anatomy, facilitating the comprehension of the manuscript.

As an original contribution, the authors describe the complex anat-omy of the intracerebellar segments of the peduncles considering thepathway of the fibres (superior, middle or inferior peduncle) andpropose a detailed classification of the segments of the peduncles.According to such classification, the superior cerebellar peduncle isdivided in three segments: intracerebellar, intermediate and intrateg-mental; the middle cerebellar peduncle in two segments: cisternal andintracerebellar; and the inferior cerebellar peduncle in three segments:cisternal, ventricular and intracerebellar. Such classification, as theauthors comment, may help in the decision of the surgical approachfor cavernomas and arteriovenous malformations affecting thepeduncles. It is important to remember, however, that the surgical routefor brainstem cavernomas must remain the area wherein the lesionabuts the pial or ependymal surface.

The authors have added a significative contribution to the literatureregarding the microsurgical anatomy of the brainstem and cerebellarpeduncles. For the neurosurgeons interested in vascular malformationsand brainstem surgery, it represents an interesting guide for the surgicalplanning of such complex procedures.

Toshio Matsushima, Saga, JapanMy congratulations to Dr. Paolo Perrini and the authors for this

paper which shows well-done anatomical study of the cerebellarpeduncles by using a fibre dissection technique. Each peduncle isexplained being divided into a few segments.

When I studied the anatomy of the fourth ventricle and developedtranscerebellomedurally fissure approach, we did not think of incisingthe brainstem at all (1, 2, 3, 4). After development of MRI, however,many cases of cavernoma have been found as a cause of pontinehemorrhage, and now neurosurgeons try to attack an intrinsic lesionin 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 haveshown by an illustration which portion of the brainstem should have beenincised and which direction of an incision should be selected in order tominimize the postoperative neurological deficits, though I understand thatthis study had limitation. Recently cavernoma in the pons is removed notonly through the floor of the fourth ventricle but also through the lateralwall of the pons including the middle cerebellar peduncle (5). It is becausethe injury of the middle cerebellar peduncle develops lower morbidity thanthat of the floor of the fourth ventricle. In conclusion again my congrat-ulations to Dr. Perrini for this well-done paper.

References1. Kawashima M, Matsushima T, Nakahara Y, Takase Y, Masuoka

J, Ohata K (2009) Trans-cerebellomedullary fissure approach withspecial reference to lateral route. Neurosurg Rev 32:457–464

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2. Matsushima T, Fukui M, Inoue T, Natori Y, Baba T, Fujii K(1992) Microsurgical and magnetic resonance imaging anatomy of thecerebello-medullary fissure and its application during fourth ventriclesurgery. Neurosurgery 30:325–330

3. Matushima T, Inoue T, Inamura T, Natori Y, Ikezaki K, Fukui M(2001) Transcerebellomedullary fissure approach with special refer-ence to methods of dissecting the fissure. J Neurosurg 94:257–264

4. Matsushima T, Abe H, Kawashima M, Inoue T (2012) Exposureof the wide interior of the fourth ventricle without splitting the vermis:importance of cutting procedures for the tela choroidea. Neurosurg RevDOI 10.1007/s10143-012-0384-3

5. Ohue S, Fukushima T, Friedman A, Kumon Y, Ohnishi T (2010)Retrosigmoid suprafloccular transhorizontal fissure approach for resec-tion of brainstem cavernous malformation. Neurosurgery 66(ONSSuppl 2): ons306–ons313

Helmut Bertalanffy, Hannover, GermanyThe authors are to be commended for this detailed anatomical de-

scription of the cerebellar peduncles using the white matter dissectiontechnique. A detailed anatomical knowledge is always an importantprerequisite for safe surgery in this area, and this nicely illustrated article

contributes to our understanding of the complex anatomy of the cerebel-lum and the three cerebellar peduncles. However, concentrating withanatomical studies solely upon the neural tissue after having removedthe arachnoid membrane and vascular structures does not completelyreflect the clinical situation at surgery. My experience with primarilyintrinsic brainstem lesions comprises over 250 surgical cases treated forcavernous malformations and gliomas. Only a part of these lesions werereadily visible on the surface of the brainstem and thus directly accessible.In a great number of cases, the surface of the brainstem showed atexposure either an apparently normal aspect or perhaps a bulging ordiscoloration in case of an intraaxial hemorrhage. In all these cases, Ihad to penetrate the pial surface at some point and enter into the brainstemto reach the underlying pathological lesion. I am convinced that choosingthe optimal location for this entry point was of crucial importance for thesurgical result. In my experience, the selection of the entry point into thebrainstem was not only dictated by the location of the intrinsic fibresystem and nuclei but also by the (quite variable) vascular anatomy onthe surface of the brainstem. Particularly the area of the cerebellomesen-cephalic fissure contains an abundant vascular network. I was very carefulin preserving perforating arteries supplying the brainstem and superficialdraining veins as much as possible, which also influenced my choice ofthe optimal entry point into the brainstem.

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