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n e u r o c i r u g i a . 2 0 1 7;28(3):111–123

www.elsev ier .es /neuroc i rugia

NEUROCIRUGÍA

Clinical Research

3D anatomy of cerebellar peduncles based on fibremicrodissection and a demonstrationwith tractography!,!!

Ruben Rodríguez-Menaa,b,∗, José Piquer-Bellocha,b, José Luis Llácer-Ortegaa,b,Pedro Riesgo-Suáreza,b, Vicente Rovira-Lilloa,b

a Hospital Universitario de la Ribera, Alzira, Valencia, Spainb Cátedra de Neurociencias – Fundación NISA-CEU, Valencia, Spain

a r t i c l e i n f o

Article history:Received 10 August 2016Accepted 30 October 2016Available online 16 March 2017

Keywords:CerebellumInferior cerebellar peduncleMiddle cerebellar peduncleSuperior cerebellar peduncleFibre microdissection techniqueTractography

a b s t r a c t

Objective: To perform an anatomical and radiological study, using fibre microdissection anddiffusion tensor tractography (DTT), to demonstrate the three-dimensionality of the supe-rior, middle and inferior cerebellar peduncles.Material and methods: A total of 15 brain-stem, 15 cerebellar hemispheres, and 5 brainhemispheres were dissected in the laboratory under the operating microscope with micro-surgical instruments between July 2014 and July 2015. Brain magnetic resonance imagingwas obtained from 15 healthy subjects between July and December of 2015, using diffusion-weighted images, in order to reproduce the cerebellar peduncles on DTT.Results: The main bundles of the cerebellar peduncles were demonstrated and delineatedalong most of their trajectory in the cerebellum and brain-stem, noticing their overallanatomical relationship to one another and with other white matter tracts and the greymatter nuclei the surround them, with their corresponding representations on DTT.Conclusions: The arrangement, architecture, and general topography of the cerebellar pedun-cles were able to be distinguished using the fibre microdissection technique. This knowledgehas given a unique and profound anatomical perspective, supporting the correct represen-tation and interpretation of DTT images. This information should be incorporated in theclinical scenario in order to assist surgeons in the detailed and critical analysis of lesionsthat may be located near these main bundles in the cerebellum and/or brain-stem, and

! Please cite this article as: Rodríguez-Mena R, Piquer-Belloch J, Llácer-Ortega JL, Riesgo-Suárez P, Rovira-Lillo V. Anatomía de lospedúnculos cerebelosos en 3D basada en microdisección de fibras y demostración a través de tractografía. Neurocirugia. 2017;28:111–123.!! Part of this paper was the basis of an oral presentation at the Spanish Neurosurgery Society (SENEC)/Portuguese Neurosurgery Society(SPNC) International Congress in Estoril, Portugal, in May 2016.

∗ Corresponding author.E-mail addresses: [email protected], [email protected] (R. Rodríguez-Mena).

2529-8496/© 2016 Sociedad Espanola de Neurocirugıa. Published by Elsevier Espana, S.L.U. All rights reserved.

Author's Personal Copy

112 n e u r o c i r u g i a . 2 0 1 7;28(3):111–123

therefore, improve the surgical planning and achieve a safer and more precise microsurgicaltechnique.

© 2016 Sociedad Espanola de Neurocirugıa. Published by Elsevier Espana, S.L.U. All rightsreserved.

Anatomía de los pedúnculos cerebelosos en 3D basada en microdisecciónde fibras y demostración a través de tractografía

Palabras clave:CerebeloPedúnculo cerebeloso inferiorPedúnculo cerebeloso medioPedúnculo cerebeloso superiorTécnica de microdisección defibrasTractografía

r e s u m e n

Objetivo: Realizar un estudio anatómico de microdisección de fibras y radiológico mediantetractografía basada en tensor de difusión (DTT) para demostrar tridimensionalmente lospedúnculos cerebelosos superiores, medios e inferiores.Material y métodos: Bajo visión microscópica y con el uso de instrumental microquirúr-gico en el laboratorio, se disecaron 15 troncoencéfalos, 15 hemisferios cerebelosos y 5hemisferios cerebrales humanos, entre julio de 2014 y julio de 2015. Se obtuvieron imá-genes de resonancia magnética cerebrales realizas a 15 sujetos sanos entre julio y diciembrede 2015, empleando secuencias potenciadas en difusión para el trazado de los pedúnculoscerebelosos y su reproducción mediante DTT.Resultados: Se demostraron y describieron anatómicamente las principales fibras de lospedúnculos cerebelosos a lo largo de gran parte de su trayectoria en el cerebelo y tron-coencéfalo, identificando las relaciones entre sí y con otros haces de sustancia blanca ynúcleos de sustancia gris que los rodean, con la correspondiente representación medianteDTT.Conclusiones: Mediante la técnica de microdisección se apreció la disposición, arquitecturay organización topográfica general de los pedúnculos cerebelosos. Este conocimiento haaportado una perspectiva anatómica única y profunda que ha favorecido la representacióny correcta interpretación de las imágenes de DTT. Esta información debe ser trasladada a lapráctica clínica para favorecer el análisis crítico y exhaustivo por parte del cirujano ante lapresencia de lesiones que puedan localizarse cercanas a este grupo de haces en el cerebeloy/o troncoencéfalo, y, en consecuencia, mejorar la planificación quirúrgica y alcanzar unatécnica microquirúrgica más segura y precisa.

© 2016 Sociedad Espanola de Neurocirugıa. Publicado por Elsevier Espana, S.L.U. Todoslos derechos reservados.

Introduction

The cerebellum constitutes the posterior part of the meten-cephalon and can be divided into 2 fundamental parts: theflocculonodular lobe and the corpus cerebelli. The latter con-sists of the anterior lobe and the posterior lobe (also knownas the middle lobe). The cerebellum is connected to the restof the brainstem through 3 pairs of projection fibre tractsknown as cerebellar peduncles: the superior cerebellar pedun-cles, with efferent fibres leading towards the midbrain andthalamus, involved in the coordination of muscle activity; themiddle cerebellar peduncles, with afferent cerebellopontinefibres which mainly lead towards the neocerebellum and forman essential circuit in the cerebellar movement control sys-tem (movement planning or programming); and the inferiorcerebellar peduncles, with both efferent and afferent fibreswhich connect it to the medulla oblongata, linked to trans-mission of proprioceptive information, and tied to movementand position in relation to gravity, as well as motor learning.1–4

Histological staining techniques applied to anatomicalstudy have improved understanding of the organisation of thewhite matter in the central nervous system. However, from asurgical perspective, the fibre dissection technique, reportedwidely in the literature,5–14 represents the best method toacquire accurate and precise knowledge of the inner struc-tures of the brain.

Moreover, advances in neuroimaging through the intro-duction and development of diffusion tensor imaging (DTI),based on magnetic resonance imaging (MRI),15,16 have enabledidentification in vivo since their first studies of some detailsof the organisation of the main white matter nerve path-ways in human beings, in both healthy brains and brainswith disease.17–19 This promising technology and mathemat-ical models are becoming increasingly sophisticated withthe development of diffusion tensor tractography (DTT),20,21

thereby enabling individual delineation and assessmentin vivo of the main white matter tracts. This is essentialfor neuroscientific studies and in the clinical practice ofneurosurgery.22–37


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All this has motivated the conduct of an essentiallyanatomical laboratory study using the nerve fibre microdis-section technique with the main objective of demonstratingthe topography and relationships of the main projection fibresystems of the human brain: the superior, medial and infe-rior cerebellar peduncles. This study offers a microsurgicalperspective of the configuration of the cerebellum which issupplemented with the demonstration of these systems bymeans of MRI DTT performed in healthy subjects.

Material and methods

The anatomical study was performed in the neuroanatomylaboratory at Hospital Universitario de la Ribera (Alzira,Spain) from July 2014 to July 2015. There, multiple humanbrain specimens—15 brainstems, 15 cerebellar hemispheresand 5 cerebral hemispheres—were examined and dissectedusing the fibre dissection technique, widely reported in theliterature.10,12–14,38 To do this, the specimens were removedfrom the cranial cavity, stripped of dura mater and placed ina 10% formaldehyde solution for at least 2 months. After that,they were carefully stripped of pia mater, arachnoid materand blood vessels. Next, the specimens were frozen at −10 ◦Cto −15 ◦C for 7–10 days. Thereafter, they were submerged inwater until they thawed (2–3 h). At that point, they were readyfor anatomical dissection. They were preserved during the dis-section process in a 5% formaldehyde solution.

In order to progressively follow anatomical planes anddetail and identify even the thinnest fibres, bundles of whitematter were systematically microdissected using microscopicvision (6–40×) and the following instruments: scalpel with15 and 11 mm blades, microsurgery scissors, microdissectionforceps of different sizes, fine aspirators and, on occasion,fine-pointed wooden spatulas (<1 mm thick and 3 mm wide).Dissection started on the superior aspect and lateral bor-der of the cerebellum, from the most superficial structuresto the deepest structures, accompanied by dissection of theanterolateral surface of the midbrain and pons, and finally cul-minated in dissection of the inferior aspect of the cerebellum.During the different steps, each specimen was photographedusing a Nikon D3000 camera (with an AF-S VR Micro-Nikkor105 mm f/2.8 G IF-ED lens), Nikon Corp, Sendai, Japan, and2 free wireless flashes. A tripod with a built-in pan and tilthead was also used to perform 2 captures of the same imagefrom 2 different perspectives and thus prepare 3-dimensionalimages. The images were fused in an anaglyph to create three-dimensional photographs using the software program AdobePhotoshop CS6 version 13.0 × 64 for Macintosh.

The second part consisted of a radiological study with DTTimages obtained from brain MRIs performed with a 1.5-TeslaPhilips Achieva device on 15 healthy subjects from July toDecember 2015. The fascicles chosen in tractography weretraced with enhanced diffusion sequences using DTV.II SRtoolbox software (Hospital Universitario de la Ribera RadiologyDepartment). This allowed tractographies with 30 directions(b = 1.000; voxel = 2 × 2 × 2 mm) to be prepared. The techniquebased on selection of regions of interest (ROIs) reported byCatani et al.21 was applied. This was essentially guided byclassic anatomy books1,2,39–41 and the knowledge obtained in

the anatomical phase. Thus, three-dimensional volumes ofthe white matter projection fascicles selected—the superior,medial and inferior cerebellar peduncles—were created.

Results

Anatomy and dissection of the superior surface andlateral border of the cerebellar hemisphere and brainstem

The superior surface of the cerebellum is also known as thetentorial surface due to its relationship to the tentorium cere-belli. The anteromedial portion of this surface constitutes itsapex, formed by the anterior part of the vermis, the culmen,the highest point of the cerebellum. The part of the cerebellarhemisphere corresponding to this surface includes the qua-drangular, simple and superior semilunar lobules, while thevermis includes the culmen, declive and folium. The tento-rial or primary fissure, between the quadrangular and simplelobules in the hemisphere and the culmen and declive inthe vermis, divides this surface into an anterior lobe and alarger posterior lobe. The larger and deeper horizontal fis-sure separates the superior and inferior semilunar lobes andis identified on the anterior surface and lateral border ofthe cerebellar hemisphere, extending up to the foramen ofLuschka in the cerebellopontine cistern (Fig. 1).

Initial dissection of the superior surface and lateral borderof the cerebellum consists of removing the cerebellar cortexwhich covered the anterior lobe (the lingula, the centrallobule together with the wing of the central lobule, and theculmen together with the quadrangular lobule) and partof the posterior lobe (the declive together with the simplelobule, and the folium together with the superior semilunarlobule), thus exposing the narrow sheets of white matterwhich constitute the cerebellar folia as projections from thedeep white matter of the cerebellum. After dissecting thewhite matter of the cerebellar folia, we identified superficialradiations mainly from the middle cerebellar peduncle, whichcourse and project in a posterior direction both laterally andmedially, to show terminations in most of the lobules of thecerebellum, minus the nodule and the flocculus. The middlecerebellar peduncle, which contains more fibres, originatesfrom transverse pontine fibres largely from the contralateralpontine nuclei, which travel obliquely on the lateral surfacewithin the pons, crossed by the fibres of the trigeminal nerve,to form part of the floor of the cerebellopontine angle beforeentering the cerebellum, thus positioning itself lateral to thesuperior and inferior cerebellar peduncles, with no directrelationship to the cavity of the fourth ventricle.

After removing deeper fibres of the middle cerebellarpeduncle, mainly in the depth of the quadrangular lobule, thefibres of the inferior cerebellar peduncle, whose bundles havea characteristic arrangement and pathway, are observed. Thewhite matter of the centre of the cerebellum crosses from lat-eral to medial to continue dorsomedially around the hilum ofthe dentate nucleus and proceed mainly towards the vermis.The rostral border of the inferior cerebellar peduncle is thenseen anterior to the level of the union of the superior cerebel-lar peduncle with the dentate nucleus. Similarly, dissectionof the deep fibres of the middle cerebellar peduncle exposed


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Fig. 1 – Tentorial or superior surface (A), suboccipital orinferior surface (B) and petrosal or anterior surface (C) of thecerebellum. Abbreviations with white letters refer tofissures. bil: biventer lobule; ca: cerebellar amygdala; cel:central lobule; cu: culmen; de: declive; flc: flocculus; isl:inferior semilunar lobule; mo: medulla oblongata; pf:primary fissure; pon: pons; py: medullary pyramid; qul:quadrangular lobule; sl: simple lobule; ssl: superiorsemilunar lobule; uv: uvula.

a thin capsule of fibres covering the superior surface of thedentate nucleus (Fig. 2A).

On the lateral surface of the midbrain tegmentum, a thinand superficial layer of fibres forming the tectospinal tractis identified behind the lateral midbrain sulcus and anteriorto the fibres of the superior cerebellar peduncle. The tec-tospinal tract is an efferent bundle from the superior colliculusthat descends and continues towards the pontine tegmentum.When this tract is removed, a group of fibres is exposed thatascends obliquely, superficially and ventrally to the fibres ofthe superior cerebellar peduncle, some of which reach theipsilateral inferior colliculus while others continue below thebrachium of the inferior colliculus. These fibres, from posterior

and medial to anterior and lateral, correspond to the laterallemniscus, the spinothalamic tract and some fibres from thedorsolateral portion of the medial lemniscus, which consti-tutes the most superficial portion of their trajectories throughthe brainstem, occupying the area known as the lemniscaltrigone.3,41 The lateral lemniscus terminates in the ipsilat-eral inferior colliculus, while the spinothalamic tract and themedial lemniscus turn dorsally and ascend in the depth of thebrachium of the inferior colliculus towards their final destina-tions in the thalamus. From the pontomesencephalic sulcus,dissection continued on the anterior surface of the pons. Thisenabled determination of how the corticospinal tract divideslongitudinally into several bundles which interdigitate withthe transverse pontine fibres connecting the pontine nuclei tothe middle cerebellar peduncle (Fig. 2A).

Dissecting part of the fibres of the inferior cerebellar pedun-cle and all other fibres comprising the capsule of the dentatenucleus allows the superior surface of this nucleus along withthe fibres of the superior cerebellar peduncle to be distin-guished. The dentate nucleus consists of well-defined islets ofgrey matter forming nearly parallel bars, separated by superfi-cial sulci which contain white matter. The fibres which departfrom this nucleus come together in its hilum and combinewith those originating in the globular and emboliform nucleito form the superior cerebellar peduncle, located in the depthof the culmen and central lobule of the vermis as well as partof the quadrangular lobule and the wing of the central lobuleof the cerebellar hemisphere. The superior cerebellar pedun-cle is arranged medial to the medial and inferior cerebellarpeduncles and continues on a pathway that ascends in ananterior and superior direction, initially as part of the lateralwall of the fourth ventricle, to later contribute, along with thesuperior medullary velum and its contralateral counterpart, toforming the ceiling of the fourth ventricle. It ascends towardsthe interior of the midbrain tegmentum under the fibres ofthe lateral lemniscus and inferior colliculus (Fig. 2B–D, G–I).The inferior cerebellar peduncle ascends dorsolaterally in themedulla oblongata, dorsal to the olive, lateral to the gracile andcuneate tubercles, and deep to the medullary striae and dorsalcochlear nucleus in the lateral recess of the fourth ventricle,laterally covered by the flocculus, to form part of the lateralwall of the fourth ventricle. On its ascent, the inferior cere-bellar peduncle is intimately related to intrapontine fibres ofthe facial and trigeminal nerves in its ventromedial portion. Italso intersects with fibres from the middle cerebellar pedun-cle, where it changes direction to proceed backwards obliquelyand enter the cerebellum, mainly between the superior andmiddle cerebellar peduncles (Fig. 2E and F).

Anatomy and dissection of the inferior surface of thecerebellar hemisphere and posterior surface of thebrainstem

The main hemispheric structures on the inferior or suboc-cipital surface of the cerebellum are the biventer lobules andthe cerebellar amygdalae, as well as the uvula on the mid-line. The fissures that surround the cerebellar amygdala anddelimit its free borders—the cerebellomedullary fissure, theamygdalar–biventral fissure and the fissure that separates itfrom the uvula—are recognised (Fig. 1B and Fig. 3A). The right


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Fig. 2 – Progressive dissection on the superior surface and lateral border of the cerebellar hemisphere and brainstem.Abbreviations with white letters refer to sulci and fissures. (A) Dissection on the superior surface and lateral border of thecerebellum exposes the superior cerebellar peduncles (scp), middle cerebellar peduncles (mcp) and inferior cerebellarpeduncles (icp). (B–D) Advanced dissection, enabling observation of the relationships between the cerebellar peduncles andthe dentate nucleus (dn) (lateral, posterolateral and posterior view, respectively). Fibres belonging to the medial and laterallemnisci (lle) and in the basilar portion of the pons and the corticospinal tract (cst) unfolded in several bundles are identifiedon the lateral surface of the midbrain tegmentum. (E and F) Part of the ascent of the inferior cerebellar peduncle (icp) is seenon the anterolateral surface of the brainstem. G–I correspond to images B–D in 3D, respectively (anaglyph glasses in red andcyan must be used to visualise them properly). bico: brachium of the inferior colliculus; cp: cerebral peduncle; cst:corticospinal tract; cu: culmen; de: declive; dn: dentate nucleus; flc: flocculus; ico: inferior colliculus; icp: inferior cerebellarpeduncle; lle: lateral lemniscus; lms: lateral midbrain sulcus; mcp: middle cerebellar peduncle; ol: olive of the medullaoblongata; pf: primary fissure; pg: pineal gland; pon: pons; py: medullary pyramid; qul: quadrangular lobule; sco: superiorcolliculus; scp: superior cerebellar peduncle; sl: simple lobule; smv: superior medullary velum; ssl: superior semilunarlobule; tl: temporal lobule; tp: thalamic pulvinar; ver: vermis of the cerebellum; III: oculomotor nerve; IV: trochlear nerve; V:trigeminal nerve; VII-VIII: facial–vestibulocochlear nerves.

amygdala is dissected by separating the fibres from its super-olateral portion. Through these fibres, known as the peduncleof the cerebellar amygdala, it inserts into and connects to therest of the cerebellar hemisphere.42 This exposes the infe-rior medullary velum, the tela choroidea with the choroidplexus and the telovelar junction, forming the inferior partof the ceiling of the fourth ventricle. The structures of thecerebellar vermis (uvula and nodule in depth, from whichthe inferior medullary velum arises) may be clearly visualised(Fig. 3B and F). Next, the left cerebellar amygdala and bothtelae choroideae were dissected, largely exposing the cavityof the fourth ventricle and both lateral recesses, as well as the

posterolateral surface of the brainstem, mainly the medullaoblongata. The inferior medullary velum extends as a sheetof white matter to each side of the nodule; its convex bordercontinues with the white matter of the cerebellum, specificallythrough the so-called peduncle of the flocculus, at the level ofthe outer margin of the lateral recess.4,42 The inferior cere-bellar peduncle ascends from the posterolateral surface of themedulla oblongata to later form part of the lateral border of theIV ventricle, as well as the anterior and superior margins of thelateral recess, where it will maintain contact with fibres of themedial and superior cerebellar peduncles while proceedingposteromedially towards the cerebellar hemisphere on the


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Fig. 3 – (A–E) Systematic dissection of the inferior or suboccipital surface of the cerebellum exposing the cavity of the fourthventricle and the relationships to the cerebellar peduncles and dentate nucleus (dn). F–I correspond to images B–E in 3D,respectively. ca: cerebellar amygdala; chp: choroid plexus; dcn: dorsal cochlear nucleus; dn: dentate nucleus; dt: dentatetubercle; flc: flocculus; icp: inferior cerebellar peduncle; imv: inferior medullary velum; lr: lateral recess; mcp: middlecerebellar peduncle; mo: medulla oblongata; scp: superior cerebellar peduncle; tch: tela choroidea; uv: uvula; IX-X:glossopharyngeal and vagus nerves; IV-v: fourth ventricle.

same side. The superior cerebellar peduncles are observedconstituting the lateral walls of the superior portion of thefourth ventricle. The dentate tubercle, a prominence of thedentate nucleus, is located in the region of the lateral recess,close to the lateral border of the inferior medullary velum,which is superior and lateral to the vestibular area and lat-eral to the inferior cerebellar peduncle, as well as medial tothe peduncle of the cerebellar amygdala (Fig. 3C and G).

On the superior surface of the cerebellar hemisphere weobserved the fibres of the middle cerebellar peduncle follow-ing a pathway towards the midline, where finally the majorityof them would cross to the contralateral hemisphere. However,when we removed the folia from the right biventer and infe-rior semilunar lobules, we revealed a set of fibres belonging tothe middle cerebellar peduncle which advances curvilinearlybelow the dentate nucleus in a posterior direction towardsthe periphery, without crossing the midline. The flocculus,together with its connection to the inferior medullary velumthrough the peduncle of the flocculus, as well as the site ofinsertion of the amygdala into the cerebellar hemisphere, mayeasily be seen (Fig. 3D and H). Finally, dissecting the white

matter of the right cerebellar hemisphere in greater depthexhibits the grey matter of the inferior surface of the dentatenucleus, thereby showing its relationships to the cerebellarpeduncles and the IV ventricle (Fig. 3E and I).

DTT of the cerebellar peduncles

A better and clear perception of the three-dimensionalarrangement of the fibres of the 3 pairs of cerebellar pedun-cles, acquired through the microdissections performed, wasthe fundamental pillar for identifying them properly whenstudying brain MRI DTI axial sequences, especially in thosezones that are the most constant and have the greatestanatomical distinction. This enabled more rigorous selec-tion of the corresponding ROIs during tracking on thecolour DTI map. Thus reproduction and subsequent triplanardemonstration through tractography images of the supe-rior, medial and inferior cerebellar peduncles were achieved,thereby providing additional qualitative and descriptiveinformation.


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Superior cerebellar peduncleThe area of the dentate nucleus, corresponding to the originand therefore to the initial portion of the superior cerebel-lar peduncle recognised in the axial slices of the colour DTImap, was selected as the first ROI. The highest portion wasidentified approximately 1 mm below the ipsilateral inferiorcolliculus, just after entering the midbrain tegmentum, whichconstituted the second ROI. Along its ascent on the ceilingof the fourth ventricle (cerebellopontine level), approximately7 mm equidistant from the first 2 ROIs and 5 mm from the mid-line, the third ROI, corresponding to the midpoint of its path,was selected. Tractography of the superior cerebellar pedun-cle illustrated the known pathway from the cerebellar greynuclei to their destination in the thalamus. However, it wasnot possible to demonstrate its decussation in the midbraintegmentum. In this case, the fibres of both peduncles ascendedto approach the midline without coming into contact withthose on the contralateral side at the height of the red nucleus.Therefore, the tractographical phenomenon known as kissingwas not shown (Fig. 4). Identifying an ROI at the site of thedecussation of the superior cerebellar peduncles reproducederratic fibres, potentially related to the central tegmental tract,very close in a posterolateral position to the red nucleus, oralso from the ventral tegmental decussation, which includesdescending rubrospinal fibres deriving from the superior cere-bellar peduncle.2,43,44

Middle cerebellar peduncleTo represent the cerebellopontine fibres, a 3 mm axial sliceinferior to the emergence of the trigeminal nerve was usedand 2 ROIs were selected corresponding to the area of themiddle cerebellar peduncle on each side, from its start justlateral to the emergence of the trigeminal nerve in the ponsto its entry into the cerebellum (occupying an area of approx-imately 15 mm on its anteroposterior axis). As occurred in themicrodissections, accurate demonstration of cerebellopontinefibres from contralateral pontine nuclei was not possible in theradiological phase; in its place both middle cerebellar pedun-cles were simultaneously demonstrated and the continuityand connection of their fibres through the midline, sugges-tive of the contralateral origin of many of them, were observed(Fig. 5).

Inferior cerebellar peduncleThe search for the inferior cerebellar peduncle started in thedorsolateral and inferior portion of the medulla oblongata. Itsidentification was clearer starting from the height of the oliveof the medulla oblongata, ascending to constitute the corpusrestiforme on the superior part of the medulla oblongata,where the first ROI was selected (around 8 mm superior tothe obex, 2 mm under the lateral recess and occupying thearea from 5 to 8 mm lateral to the posterior medial sulcus).We followed it towards the cerebellum and located the con-fluence of the large peduncular mass on the lateral walls ofthe fourth ventricle, to later advance and continue towardsthe inside of the cerebellum, where the second ROI wasselected (approximately 1–2 mm superior and anterior to theipsilateral dentate nucleus). Thus the tractography sequencesshow the main connection between the medulla oblongata

Fig. 4 – Demonstration of the superior cerebellar pedunclesand their thalamocortical projections through DTT imageson different brain MRI planes.

and the cerebellum through the inferior cerebellar peduncle,continuing in front of and above the dentate nucleus to spreadout mainly in the vermal and paravermal region of the ante-rior lobule of the cerebellum (Fig. 6A and B). Finally, the set offibres of the 3 cerebellar peduncles was represented throughtractography, which exhibited the relationships, arrangementand organisation of these bundles of white matter on theaxial, coronal and sagittal brain MRI planes (Fig. 6C and D).

The limitations of the study include the characteristic tech-nical limitations related to the equipment and software usedin this study, such as the lack of quantitative information withrespect to size, fibre volume, number of fibres in a tract, frac-tion of anisotropy and apparent diffusion coefficient, as wellas the impossibility of accurately selecting the same ROIs indifferent subjects. All this had an impact on the analysis ofthe tractography results and motivated focusing the objectiveon achieving radiological reproduction of the fibre bundlesstudied during the laboratory phase, for demonstration pur-poses only.


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Fig. 5 – Demonstration of the middle cerebellar pedunclesthrough DTT images on different brain MRI planes.

Discussion

Historical–anatomical account of the study of thecerebellar peduncles based on fibre dissection

The first representations of the superior and middle cerebellarpeduncles, among other central nervous system structures,emerged in 1543 with the publication of De Humani CorporisFabrica by Andrea Vesalius (1514–1564).45 In his atlas Neu-rographia universalis (1685), the French anatomist RaymondVieussens (1641–1715) described and represented, althoughimprecisely and with low-quality images, the cerebellarpeduncles, especially the medial and inferior peduncles, aswell as their connections to the brainstem.46 Franz JosephGall (1758–1828), in collaboration with his student JohannC. Spurzheim (1776–1832), strengthened the study of theprojection fibres, and his anatomical studies, published in1810, identify good illustrations of the middle cerebellarpeduncles.9

The studies of Herbert Mayo (1796–1852) stand out, fortheir era, due to the better dissections and illustrationsof the superior, medial and inferior cerebellar peduncles,where the main relationships between them and to otherneighbouring tracts are distinguished (Fig. 7). Subsequently,other anatomists, such as Friedrich Arnold (1803–1890), AchilleL. Foville (1799–1878) and JB Luys (1828–1895) contributedinformation on the white matter of the cerebellum and brain-stem with great detail and spectacular images.5,8,47 Later on, inthe middle of the 20th century, Joseph Klingler (1888–1963) andhis teacher, Ludwig, published their masterpiece, Atlas CerebriHumani, which displayed a wide variety of detailed dissections,including dissections of the cerebellum and brainstem.10

Recently, with the development of the microscope, the tech-nique has been rescued and interest has been awakened in thestudy of fibre dissection,12,13 including the region of the cere-bellum, oriented more towards microsurgical anatomy.48–51

Anatomy of the surface of the cerebellum and itsrelationship to the dissection of the cerebellar peduncles

On the superior surface of the cerebellum are the culmen,declive and folium, which form part of the vermis, and thequadrangular, simple and superior semilunar lobules, whichform part of the cerebellar hemispheres, respectively. Thesedissections confirmed the close relationship of the 3 cere-bellar peduncles to this surface. Thus, fibres of the middlecerebellar peduncle, in an anteroposterior and lateromedialdirection, are found in the depth of the quadrangular and sim-ple lobule. Many of these follow a curve that projects towardsmost of the cerebellar lobules, thereby constituting part of thefinal destination of the cortico-ponto-cerebellar afferences.In an anterior and medial direction, the fibres of the infe-rior cerebellar peduncle which pass in front of the dentatenucleus towards the vermis and paravermis were identified.A group of fibres from the inferior cerebellar peduncle crossesthe midline while others continue ipsilaterally; however, dur-ing microdissections, the intimate relationship between someof these fibres and those of the middle cerebellar pedunclemakes them very difficult to differentiate. In the most anteriorportion of the depth of the superior surface (quadrangular andsimple lobules), approximately 5 mm from the midline on eachside, the superior cerebellar peduncles are arranged obliquelyfrom inferior and posterior to superior and anterior, as partof the ceiling of the fourth ventricle, along with the superiormedullary velum, proceeding towards the posterior aspect ofthe midbrain and continuing medial to the fibres of the laterallemniscus, covered by the inferior colliculi (Figs. 1A and 2).Akakin et al.48 separated the fibres of the middle cerebellarpeduncle which run in the depth of the superior surface ofthe cerebellum in 2 groups: the fibres in the first group are ori-ented parallel to the midline and are called corticocerebellarfibres, and the fibres in the second group project parallel tothe dentate nucleus towards the superior and inferior semilu-nar lobules and are called cerebellopontine fibres. However,in this microdissection study, it was not possible to discerna clear separation between the two groups of fibres, and soapplication of this nomenclature, which can even create acertain amount of topographical and anatomical confusion,was avoided.


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Fig. 6 – Demonstration of the inferior cerebellar peduncles (A and B) and jointly of the 3 cerebellar peduncles (C and D)through DTT images on different brain MRI planes.

The anterior surface of the cerebellum is related on itssuperior part to the cerebellopontine angle and foramen ofLuschka through the cerebellopontine fissure, which containsa superior brachium and an inferior brachium which comeinto direct contact with the middle cerebellar peduncle onits path towards the cerebellum to later be covered by theapex of the fissure, where the two brachia meet. The lat-eral recess and the foramen of Luschka open towards themedial portion of the inferior brachium of the cerebellopon-tine fissure, where the flocculus, the choroid plexus and thecranial nerve pairs—facial, vestibulocochlear, glossopharyn-geal and vagus—are identified. Thus, during its ascendingcourse the inferior cerebellar peduncle is closely related tothe anterior and superior border of the lateral recess, being

partially covered by the flocculus (which projects towards thecistern of the cerebellopontine angle) and by the most ante-rior border of the biventer lobule, both forming part of theposterior, superior and lateral border of this recess. As wedescended on the anterior surface, we found the complexcerebellomedullary fissure as a continuation of the cerebel-lopontine fissure, close to the inferior portion of the floor ofthe fourth ventricle. On the anterior wall of this fissure wemainly observed the fibres of the inferior cerebellar pedun-cle and, behind them, the biventer lobule and the ipsilateralcerebellar amygdala, leaving the inferior medullary velum andthe tela choroidea in a more medial location on the ceiling ofthe fourth ventricle (Figs. 1C and 2E,F). On the inferior sur-face of the cerebellum we identified the folium, the tuber, the

Fig. 7 – (A and B) Historical illustration by Herbert Mayo, with special distinction between the fibres of the 3 pairs ofcerebellar peduncles. Source: Mayo.11


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pyramid and the uvula as structures of the vermis, the supe-rior and inferior semilunar and biventer lobules, and thecerebellar amygdala as structures of the cerebellar hemi-sphere, respectively (Figs. 1B and 3A). The lateral surface of theamygdala is in contact with the biventer lobule and separatedfrom it through the amygdalar–biventral or retroamygdalarfissure; in the depth we identified fibres that proceed mainlyfrom the middle cerebellar peduncle, which run inferior to thedentate nucleus, in close relationship to the so-called pedun-cle of the amygdala, which connects it from its superior andlateral border to the rest of the cerebellar hemisphere.

Therefore, the fibres of the middle cerebellar peduncle weredemonstrated wrapping the dentate nucleus in a superiorand inferior direction: those that pass the superior surfaceof the cerebellar hemisphere form a curve, emitting radia-tions towards multiple hemispheric regions, including somethat are oriented towards the midline, part of which willpotentially cross towards the contralateral hemisphere; thosethat continue on the inferior surface do so predominantly inan anteroposterior oblique direction on the cerebellar amyg-dalae while remaining in the same hemisphere, similar to thatreported by other authors48 (Fig. 3). However, microdissectionof peduncular fibres in the area close to the lateral recess didnot enable appropriate separation of the limits between thosethat ascend as part of the inferior cerebellar peduncle fromthose corresponding to the inferior radiations of the middlecerebellar peduncle. Unlike Perrini et al.,50 when we followedthe fibres of the inferior cerebellar peduncle, we did not clearlyidentify radiations that continue under the ipsilateral dentatenucleus. This is consistent with data from classic literaturethat indicate their major ascending trajectory above and infront of this nucleus.1–3,52

Cerebellar peduncles and surgical implications

When surgically approaching the cerebellum, together withthe cavity of the fourth ventricle, their relationships to thegrey-matter structures (dentate nucleus) and white-matterstructures (cerebellar peduncles) found inside must be takeninto account. As in the cerebrum, the normal cortex andcerebellar white matter, mainly peduncular fibres, should bepreserved to the extent possible when resecting lesions insideor neighbouring them. The morbidity inherent to violatingthem (due to inappropriate dissection or retraction, or evenpartial retraction) requires implementation of strategies thatattempt to protect their integrity during surgery.

The middle cerebellar peduncle is most vulnerable to beingaffected during approaches to the cerebellopontine fissure(retrosigmoid or suboccipital lateral craniotomy towards theregion of the cerebellopontine angle), in both their suprafloc-cular and infrafloccular variants.53–56 Lesion of this pedunclecauses ataxia and dysmetria during voluntary movementsof ipsilateral limbs and hypotonia similar to those thatappear when the lateral part of the cerebellar hemisphere isaffected.57,58 When accessing the inside of the middle cere-bellar peduncle and the lateral portion of the pons, incisionand dissection must be done preferably in a horizontal direc-tion, lateral to the emergence of the trigeminal nerve andfollowing the parallel anatomical trajectory of their cerebel-lopontine fibres,59,60 in an attempt to preserve their integrity.

As the fibres of the middle cerebellar peduncle go deeper, thecorticospinal tract will be located in an anterior and medialdirection in the basilar portion of the pons, while the fibres ofthe medial and lateral lemnisci will be located in a medialdirection in the depth of the pontine tegmentum and theinferior cerebellar peduncle will be located in a medial andcaudal direction (mainly its spinocerebellar fibres). Extendingdissection through the inferior portion of the cerebellopontinefissure and its continuation with the superolateral border ofthe cerebellomedullary fissure exposes the dorsolateral sur-face of the medulla oblongata, low cranial nerve pairs andlateral border of the inferior cerebellar peduncle, recentlyreported as a route of access to resect lesions affecting thispeduncle.61

On the inferior surface of the cerebellar hemisphere, therelationships between the cerebellar amygdala and the biven-ter lobule are significant for the supra-amygdalar approachthrough the amygdalar–biventral fissure, proposed by Lawtonto resect arteriovenous malformations in the inferior cere-bellar peduncle.62 This approach requires retraction of theamygdala and may affect the fibres that connect it to the cere-bellar hemisphere. However, it is recognised as a favourableroute to access both the medial fibres of the inferior cerebel-lar peduncle as they pass through the ceiling of the lateralrecess of the fourth ventricle and those of the middle cere-bellar peduncle which cross the inferior border of the dentatenucleus. This nucleus, which is found just above and there-fore has a close relationship to the peduncle of the amygdala,may be lesioned during dissection and cause mainly balanceabnormalities and intention tremor in limbs.63

Studies by Matsushima et al.58 emphasised the micro-surgical anatomy of the fourth ventricle and its approachthrough the tela choroidea and the inferior medullary velum.Yasargil4 reported entering the fourth ventricle through thesulcus between the amygdala and the uvula, along the medialdivision of the posteroinferior cerebellar artery. Subsequently,the concept of the “transcerebellomedullary” approach wasmodified by detailing its benefits and limitations.63–66

Although the 3 cerebellar peduncles converge on the lateralwalls and the ceiling of the fourth ventricle, the direct prox-imity of the superior and inferior cerebellar peduncles to theinside of the cavity of the fourth ventricle confers upon thema higher risk of being lesioned during surgical approaches tothis region. Thus, in the approach to the cerebellomedullaryfissure, initial dissection of the space between the amygdalaand the posterolateral surface of the medulla oblongata, aswell as lateral dissection through the opening of the telachoroidea to reach and expose the lateral recess, render theinferior cerebellar peduncles more vulnerable. Opening theinferior medullary velum to gain access to higher areas ofthe ventricular ceiling exposes the superior cerebellar pedun-cles, especially above the height of the lateral recesses anddentate tubercle, thereby making them more prone to beinglesioned during dissection of lesions in this area. Damage tothe fibres of the superior cerebellar peduncle causes ipsilateralintention tremor, dysmetria and decomposition of movement,while damage to the inferior cerebellar peduncle causes bal-ance abnormalities similar to those caused by impairment ofthe flocculonodular lobe, with truncal ataxia, unstable gait anda tendency to fall towards the same side of the lesion.58


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Finally, the superior cerebellar peduncles also have ahigher risk of being affected during approaches to the cis-tern of the cerebellar–mesencephalic fissure. Special mentionis made of the paramedian infratentorial supracerebellarapproach, reported by Yasargil4,67,68 and widely used foraneurysm disease of the superior cerebellar artery, arteri-ovenous malformations and tumour lesions involving thesuperior surface of the cerebellum, the dorsolateral regionof the midbrain and the pineal and parapineal region, aswell as more lateral variations of this approach reportedby other authors.69–71 Dissection along the superior sur-face of the cerebellum, 2 or 3 cm from the midline, enablesopening of the cerebellar–mesencephalic cistern and subse-quent exposure of the superior cerebellar peduncle just afterretracting the quadrangular lobule, a place in which it mayeasily be lesioned. Transtentorial interhemispheric posterior(transtentorial occipital) approaches67,72–75 allow access to theipsilateral half of the cerebellar–mesencephalic fissure withexposure of the pineal and parapineal region, the dorsolateralregion of the midbrain and part of the ceiling of the fourthventricle, including the superior cerebellar peduncle.

Tractography and microdissection of the cerebellarpeduncles

The development of diffusion tensor-based DTI and trac-tography techniques more than a decade ago representedan extraordinary achievement.15,43 The information obtainedthrough DTI and thus from tractography images possessesconsiderable value, providing visualisation and qualitativeand quantitative characterisation of the major routes of whitematter.26,27,29,76–79 Its incorporation as a tool in the preoper-ative study of patients with brain lesions is becoming moreand more common, with the corresponding responsibility thatit represents for neurosurgeons to tackle an appropriate andcritical interpretation of its results.

As the fibre microdissection technique was adopted, thelaboratory study enabled observation of the fundamentalmacroscopic and microscopic arrangement of the 3 pairs ofpeduncles that connect the cerebellum to the rest of thehindbrain and forebrain, which are intimately related to thegrey matter nuclei and other surrounding tracts. It should beremembered that dissection of one system of fibres generallyresults in destruction of another, and that clearly demarcat-ing small fibre bundles as well as identifying their origin ortermination may become an arduous task, despite the avail-ability of microsurgical instruments and high magnification,as this study showed. However, it was possible to show themand follow their main path in the cerebellum and brainstem aswell as conceive of their course and main spatial relationshipsto one another and to other parenchymatous structures. Thisknowledge is difficult to acquire solely through study of histo-logical illustrations, which are common and widely reportedin the literature.

This three-dimensional anatomical knowledge unique towhite matter is particularly beneficial for neurosurgeonsinvolved in the study and treatment of patients with intrinsiclesions of the central nervous system, including the cerebel-lum and the brainstem, the main subject of this study, asit increases precision at the time of reconstruction in vivo

through tractography of these bundles. Therefore, the twotechniques complement and enrich one another, despite theirshared limitations: difficulty distinguishing areas where fibresintersect, difficulty determining the cortical and subcorticalorigins and terminations of tracts, and lack of anatomicalaccuracy when attempting to delimit contiguous tracts witha similar trajectory.

Finally, it should be noted that the study of “normal-ity” (both anatomical and tractographical) in relation to thearrangement of the main projection fibres, including the cere-bellar peduncular fibres, may be translated to the clinicalpractice setting, being helpful when performing clinical andradiological analysis of a patient with an intrinsic lesion of theposterior fossa (highlighting tumours and cavernomas) andfacilitating understanding of the relationships between thelesion and the surrounding healthy tissue, including poten-tial changes in the spatial configuration of these bundles—allwith the objective of a better indication, planning, strategy andmicrosurgical technique to achieve maximum resection of thelesion while avoiding damage to these functional structuresand minimising morbidity.

Conclusions

The microdissection technique enabled observation of thegeneral topographical arrangement, architecture and orga-nisation of the superior, medial and inferior cerebellarpeduncles, crossing and connecting the cerebellum to thebrainstem, and determination of their relationships to oneanother, to intrinsic neighbouring neural structures and tothe surface of the cerebellum and brainstem. This knowl-edge contributed a unique, in-depth anatomical perspectivethat promoted the representation and proper interpretationof DTT images. This information should be translated to clini-cal practice to promote comprehensive critical analysis by thesurgeon when there are lesions that may be located close tothis group of bundles in the cerebellum and/or brainstem andthus improve surgical planning and achieve a safer and moreprecise surgical technique.

Conflicts of interest

The authors declare that they have no conflicts of interest.

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