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Cerebellar anatomy as applied to
cerebellar microsurgical resections
Anatomia cerebelar aplicada à microcirurgia cerebelar ablativa
Alejandro Ramos1, Feres Chaddad-Neto2, Hugo Leonardo Dória-Netto3, José Maria de Campos-Filho3,
Evandro Oliveira4



Abstract
Objective: To define the anatomy of dentate nucleus and cerebellar peduncles, demonstrating the surgical application of anatomic landmarks
in cerebellar resections. Methods: Twenty cerebellar hemispheres were studied. Results: The majority of dentate nucleus and cerebellar pe-
duncles had demonstrated constant relationship to other cerebellar structures, which provided landmarks for surgical approaching. The lat-
eral border is separated from the midline by 19.5 mm in both hemispheres. The posterior border of the cortex is separated 23.3 mm from the
posterior segment of the dentate nucleus; the lateral one is separated 26 mm from the lateral border of the nucleus; and the posterior segment
of the dentate nucleus is separated 25.4 mm from the posterolateral angle formed by the junction of lateral and posterior borders of cerebellar
hemisphere. Conclusions: Microsurgical anatomy has provided important landmarks that could be applied to cerebellar surgical resections.
Key words: cerebellum, anatomy, neurosurgery.

Resumo
Objetivo: Definir a anatomia do núcleo denteado e dos pedúnculos cerebelares, demonstrando a aplicação dos marcos anatômicos em cirurgias
cerebelares. Métodos: Foram estudados 20 hemisférios cerebelares. Resultados: A maioria dos núcleos denteados e pedúnculos cerebelares
demonstraram relação anatômica constante com outras estruturas cerebelares, fato que proporcionou o estabelecimento de marcos anatômi-
cos específicos a serem utilizados em acessos cirúrgicos. O bordo lateral do núcleo denteado é separado da linha média em 19,5 mm em ambos
os hemisférios cerebelares. O bordo posterior do córtex é separado do segmento posterior do núcleo denteado por 23,3 mm. O bordo lateral do
córtex é separado do bordo lateral do núcleo por 26 mm e o segmento posterior do núcleo denteado é separado por 25,4 mm do ângulo poste-
rolateral, que é formado pela junção dos bordos lateral e posterior do hemisfério cerebelar. Conclusões: O estudo da anatomia microcirúrgica
proporcionou o estabelecimento de marcos anatômicos importantes que podem ser utilizados durante cirurgias cerebelares ablativas.
Palavras-Chave: cerebelo, anatomia, neurocirurgia.




    The cerebellum is an exquisite anatomic structure with-                    with the final objective of performing better operations with less
in the human brain, which needs to be considered from the                      damage to the cerebellar nucli and important deep pathways.
surgical standpoint because of its functional importance and
common pathologies that affect this area1. It is possible to
reach the cerebellum avoiding damaging neural structures by                        METHODS
approaches which target tentorial, petrosal, or suboccipital
surfaces. Each has its microsurgical particularities in order to                   The dentate nucleus, cerebellar peduncles and their rela-
reach the desired region and preserve neural structures2.                      tionship with others cerebellar structures were studied in 20
    In this article, we have presented the microsurgical anatomy of            adult cerebellar hemispheres, 12 male and 8 female corpses,
the suboccipital and supracerebellar approaches to the cerebellar              obtained from São Paulo death verification service using X3
surfaces using comprehensives anatomic and functional relations                to X40 magnifications.



Neurosurgeon Fellow of Microanatomy Laboratory in Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil;
1


Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo; Coordinator of Microanatomy Laboratory in
2

Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil;
Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil;
3


Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo; Director of Microanatomy Laboratory in
4

Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil.
Correspondence: Hugo Leonardo Dória Netto; Instituto de Ciências Neurológicas; Praça Amadeu Amaral 27 / 5º andar; 01327-010 São Paulo SP - Brasil;
E-mail: hldoria@hotmail.com
Conflict of interest: There is no conflict of interest to declare.
Received 11 July 2011; Received in final form 07 December 2011; Accepted 14 December 2011


                                                                                                                                                         441
Histological and functional considerations                     tentorium and posteriorly limited by the lateral sinus and lat-
      The cerebellum has a special cytoarchitecture, which           erally by the sigmoid sinus; the division between the lateral
  makes it unique3. Histologically the cortex presents three         and sigmoid sinus is located at the junction with the supe-
  layers of cells that involve a central white substance.            rior petrosal sinus. The tentorial surface has two incisures in
  These layers include the molecular, the Purkinje, and the          the midline: the anterior one is related to the brain stem and
  granular cells. The only efferent cells are the Purkinje ones      the posterior incisure is related to the falx cerebelli. There are
  that end in the central nucleus playing an inhibition ac-          two fissures on the tentorial surface, which divide this sur-
  tion. The layer in contact with the white substance is con-        face into anterior, middle, and posterior parts. The anterior
  stituted of granular cells. Two different kinds of afferents       fissure is the tentorial one and the posterior fissure is the
  cerebellar fibers arrive to the cerebellar cortex: the fibers      postclival one. The vermian surface is the most superior part
  that interconnect the caudal olives with the purkinje cells        of this surface.
  (olivocerebellar tract) and the myelinic fibers that come               The posterior inferior or suboccipital surface is located
  to an end in the granular layer (pontocerebellar, spinocer-        down the lateral sinus and inferomedially to the sigmoid si-
  ebellar, and vestibulocerebellar tracts)4.                         nus6. The falx cerebelli extends from the tentorial surface above
      The Purkinje cells are the main afferents of the cerebellar    to the inferior part of the middle suboccipital surface, the falx
  nucleus and most of the efferent fibers from the cerebellum        overlies a vertical depression that is medially formed by the
  come from these nuclei; there are four nuclei in the cerebel-      vermis, laterally by the medial aspects of the cerebellar hemi-
  lum, which includes from medial to lateral, the fastigial, glo-    spheres and continues inferiorly with the vallecula cerebelli.
  bose, emboliform, and dentate nucleus1,2. The cerebellum can       When it is viewed from a posterior position, the only part
  be longitudinally subdivided as follows: a midline zone, con-      of the vermis that is uncovered on this surface is at the side
  taining axons projecting to the fastigial nucleus and connect-     where the pyramid meets the uvula, located down this sur-
  ing with the vestibular nucleus and reticular formation; an        face. There are two fissures on the suboccipital surface that
  intermedial zone, projecting to the nucleus interpositus (glo-     divide it in superior, middle, and inferior parts. The superior
  bose and emboliform) and connecting with the contralateral         fissure is the petrosal and the inferior is the suboccipital one.
  red nucleus and thalamic nucleus with impulses to the cere-        The tonsils are the most prominent hemispheric structures
  bral cortex; and a lateral zone, containing axons to the dentate   of the suboccipital surface, located inferomedially. The ton-
  nucleus, which course to the contralateral thalamic nucleus        sils are ovoid structures, which have a middle vertical size of
  that transmits impulses to the cerebral cortex. Functionally,      13.5 mm (range from 10 to 18 mm) and a wide size of 7.8 mm
  this nucleus controls a different type of movements: the fas-      (range from 5 to 10 mm). The tonsils have an implantation
  tigial controls posture and gait; the nucleus interpositus con-    base to the suboccipital surface of the cerebellum at the su-
  trols segmental reflexes and assists the initiation of move-       perior lateral border and they are superoanteriorly related to
  ments; and the dentate nucleus controls fine dexterity. One        the inferior medullary velum and tela choroidea, laterally to
  of the main important features of the cerebellum is its con-       the biventral lobule, superolaterally to the tellovelotonsilar
  trol on the automatic excitation of antagonist muscles at the      cleft, posteriorly and inferiorly to the cistern magna, medially
  end of the movement with simultaneous inhibition of the ag-
  onist muscles, which initiated the movement5.
      Afferent fibers from the brain stem project to the cerebel-
  lum by the inferior, middle, and superior cerebellar peduncle.
  Afferent fibers from the medulla carry the anterior and pos-
  terior spinocerebellar tract that project to the cerebellum by
  the superior and inferior cerebellar peduncles. The pontine
  fibers from the pontine nucleus project to the cerebellum
  by the middle cerebellar peduncle. The cerebello vestibular
  fibers, from the vestibular nucleus, project to the cerebel-
  lum by the inferior cerebellar peduncle. Most of the effer-
  ent fibers from the cerebellum go to the superior cerebellar
  peduncle4,5.

      Anatomic considerations
      Anatomically, the cerebellum can be considered as a
                                                                     Fig 1. Suboccipital surface view. The vallecula extends
  three-surface triangle: tentorial, suboccipital, and petrosal
                                                                     between the tonsils and communicates through the foramen
  surfaces2. The posterior-superior or tentorial surface is the      of Magendie with the fourth ventricle. 1: tonsil; 2: vallecula; 3:
  most regular of all surfaces. It is surrounded superiorly by the   uvula; 4: PICA.



442     Arq Neuropsiquiatr 2012;70(6):441-446
to the vallecula cerebelli, superomedially to the uvula, and        vein of Galen; the veins of the cerebellomedullary fissure and
anteriorly to the medulla2,7 (Fig 1).                               inferior cerebellar peduncle drain into the petrosal veins; the
    The tentorial surface is related to the superior cerebel-       veins of the cerebellopontine fissure and of the middle cer-
lar artery, which arises at the pontomesecenphalic junc-            ebellar peduncle also drain through the petrosal ones3,6.
tion, encircles the brain stem, and is directed medially and
backward to the tentorial surface. The artery runs as a single
trunk up to the lateral pontomesencephalic segment, where              RESULTS
the artery commonly divides into two trunks: the superior
runs within the mesencephalic fissure, passes down to the                After our research, we could conclude that the lateral bor-
inferior colliculus, and continues posteromedially to the           der of the dentate nucleus is separated from the midline by
superior half of the fourth ventricle. The inferior trunk also      an average of 19.5 mm in the right hemisphere (range – from
runs within the anterior part of the mesencephalic fissure,         17 to 21 mm) and 19.5 mm in the left ones (range – from 14 to
but shortly, the artery turns superolaterally to the tentorial      23 mm), as seen in Fig 2.
surface. The branches of these trunks give off the precerebel-           The dentate nucleus has a unique shape. It is oriented in
lar arteries which course medially from the mesencephalic           craniocaudal direction and from lateral to medial. It is help-
fissure to the superior peduncle and dentate nucleus. The           ful to consider the dentate nucleus with upper and lower sur-
anterior inferior cerebellar artery (AICA) arises at the ante-      faces, and three segments. The upper surface is related medi-
rior pontine level; passes around the cerebellopontine fis-         ally to the superior cerebellar peduncle and faces the vermis
sure and goes to the pontomedullar segment, dividing into           at the junction of the cumen and declive. The upper surface
two trunks. The rostral trunk passes between the facial and         is bordered laterally, anteriorly, and posteriorly by the fibers
vestibulocochear nerves and around the superior part of the         of the middle cerebellar peduncle. At the basal surface, the
flocculus to supply the middle peduncle. The caudal trunk           dentate nucleus is related anteriorly to the caudal segment of
passes below the flocculus near the IX and X nerves to sup-         the flocculus, medially to the telovelotonsillar cleft and pos-
ply the petrosal surface. The posterior inferior cerebellar         teromedially to the superior pole of the tonsil and the lateral
artery (PICA) arises at the anterior medullary level, passes        border of the uvula in its posterolateral third (Fig 3).
around the medulla, crosses the inferior cerebellar peduncle,            The distance from the posterior extreme of the uvula to
enters the cerebellomedullar fissure, where it is closely re-       the posterior segment of the dentate nucleus is on average
lated to the inferior half of the fourth ventricle, and exits the   16.2 mm (range – from 13 to 20 mm). The posterior border
fissure to supply the suboccipital surface8.                        of the cortex is separated on an average of 23.3 mm (range –
    The veins of the cerebellum are divided into superficial        from 20 to 29 mm) from the posterior segment of the dentate
and deep. The superficial group is divided into tentorial,          nucleus; the lateral border of the cortex is separated on an
petrosal, and suboccipital veins. The tentorial surface veins       average of 26 mm (range – from 15 to 32 mm) from the lat-
are drained by the superior hemispheric and vermian veins,          eral border of the nucleus; and the posterior segment of the
which empty into the vein of Galen and the tentorial sinuses.       dentate nucleus is separated on an average of 25.4 mm (range
The petrosal surface veins are drained by the anterior hemi-
spheric veins, which empty mainly into the superior petrosal
sinus. The suboccipital surface veins are drained by the inferi-
or hemispheric and inferior vermian veins, which commonly
empty into the tentorial sinuses. The deep veins are divided
into: the vein of the cerebellomesecephalic fissure that is re-
lated to the superior half of the roof of the fourth ventricle;
the vein of the cerebellomedullary fissure that is related to
the inferior half of the roof; and the vein of the cerebellopon-
tine fissure that is related to the laterals walls of the fourth
ventricle. The veins of the three peduncles also course within
these fissures.
    The vein of the superior cerebellar peduncle courses in
the cerebellomesencephalic fissure; the one from the middle
cerebellar peduncle courses in the anterior part of the cere-
bellopontine fissure; and the one from the inferior cerebellar
peduncle courses in the cerebellomedullary fissure. In gener-       Fig 2. Basal surface of the cerebellum. The left and right
                                                                    cerebellar hemispheres have been removed to expose the
al terms, the vein of the cerebellomesencephalic fissure and        dentate nucleus and its relationship with the tonsils. 1: uvula;
the vein of the superior cerebellar peduncle drain into the         2: dentate nucleus; 3: tonsil; 4: vallecula.



                                                                                        Ramos A et al. Cerebellar surgical resections   443
– from 17 to 31 mm) from the posterolateral angle, which is          and the lateral zone is the cortex. This is based on similar
  formed by the junction of the lateral and posterior borders of       structures related in each zone9.
  the cerebellar hemisphere (Fig 4).                                       The cerebellum is connected to the brain stem by three
      The distance from the inferior pole of the tonsil to the lev-    large cerebellar peduncles, each peduncle displays a special
  el of the basal surface of the dentate nucleus is approximately      shape that creates a particular stratification in the cerebel-
  19.4 mm on the right side (range – from 18 to 22 mm) and             lar hemisphere; the relations between the peduncles, the cer-
  19.4 mm (range – from 16 to 25 mm) on the left one, as seen          ebellar cortex and the cerebellar nuclei are extremely impor-
  in Figs 5 and 6.                                                     tant to access the cerebellum10.
      From the basal suboccipital surface to the tentorial one,            The white matter of the cerebellum forms a central core,
  the association fibers of the white matter start to form thick       which receives afferent fibers from the cortex; these fibers
  laminae or lobular peduncles at 10 mm (range – from 0.8              create laminae of white matter that comes from the cor-
  to 1.4 mm) from the superior pole of the tonsil. The cortex          tex to the central core. The pathways and the central core
  of the cerebellum is not divided into gyri, but instead into         have variable shapes in each cerebellar hemisphere, but the
  numerous folia. According to Lange, the cortical portion of
  the cerebellum forms about 67% of the total surface area.
  In this study, the lateral border of the cerebellar cortex is
  separated on an average of 14.8 mm (range – from 10 to
  25  mm) at the level of the dentate nucleus, from the sub-
  cortical white matter or lobular peduncle; and the posterior
  border of the cerebellar cortex is separated on an average of
  15.4 mm (range – from 0.8 to 24 mm), from the subcortical
  white matter (Fig 7).


      DISCUSSION

      From a surgical perspective, it is helpful to consider the
  cerebellar hemispheres as a three-component structure that
  can be divided into median, paramedian, and lateral zones.           Fig 4. Suboccipital surface view of the cerebellum. Notice that
  The median zone extends from the lateral border of the ver-          the distance from the middle line to the lateral border of the
                                                                       dentate nucleus is 19.5 mm and 38º is the angle of separation
  mis to the lateral one of the dentate nucleus; the paramedian
                                                                       from the middle line to avoid the dentate nucleus during the
  zone extends from the lateral border of the dentate nucleus          surgical resections. Also, the distance from the middle line to
  to the junction of the white matter substance and the cortex;        the lateral border of the tonsil is approximately 16 mm.




  Fig 3. Basal surface of the cerebellar hemisphere. The left          Fig 5. Suboccipital surface view of the cerebellum. The distance
  cerebellar hemisphere and the tonsil have been removed               from the middle line to the lateral border of the dentate nucleus
  to expose the uvula and their relationship with the superior         is approximately 19.5 mm and the distance from the inferior
  pole of the tonsil and the dentate nucleus. 1: dentate nucleus;      pole of the tonsil to the level of the basal surface of the
  2: uvula; 3: flocculus; 4: middle cerebellar peduncle; 5: superior   dentate nucleus is approximately 19.4 mm. Also, 16 mm is the
  pole place of the tonsil after removed.                              distance from the middle line to the lateral border of the tonsil.



444     Arq Neuropsiquiatr 2012;70(6):441-446
are always medial to the dentate nucleus and located in the
                                                                    median zone. The middle cerebellar peduncle has the widest
                                                                    posterolateral projection and it is almost always located in
                                                                    the paramedian zone; it follows a descendent course from
                                                                    the pons. The fibers of the middle cerebellar peduncle can be
                                                                    divided into superior, middle, and inferior. The superior part
                                                                    of the fibers crosses the inferior third of the superior pedun-
                                                                    cle and runs alongside the median aspect of the dentate nu-
                                                                    cleus. The middle part of the fibers course posterolaterally
                                                                    alongside the lateral segment of the dentate nucleus around
                                                                    the hemisphere. The inferior tract fibers of the middle ce-
                                                                    rebral peduncle follow a descendent course and are closely
                                                                    related to the fibers of the inferior cerebellar peduncle at the
                                                                    rostral pole of the dentate nucleus. The inferior cerebellar
Fig 6. The right cerebellar hemisphere has been sectioned
                                                                    peduncle ascends alongside the lateral recess and floor of
to show the different relationships of the dentate nucleus to
the nearby structures. The distance from the lateral border         the fourth ventricle with most of its fibers distributed mainly
of the dentate nucleus to the middle line is on an average of       to the rostral pole of the dentate nucleus, these tract fibers
19.5 mm; the distance from the inferior pole of the tonsil to the   are medially related to the dentate nucleus and are mainly
basal surface of the dentate nucleus is on average 19.4 mm
and 38º is on average the angle of separation from the middle
                                                                    located in the median zone. There is an extraordinary medi-
line to lateral border of the dentate nucleus.                      cal significance attached to the nuclei of the cerebellum and,
                                                                    among these, particularly  to the dentate nucleus3. The den-
                                                                    tate nucleus is the most lateral nucleus of the cerebellum and
                                                                    it is located in the median zone of the hemisphere. The high
                                                                    frequency, in which the cerebellum is operated, exposing the
                                                                    cerebellar hemispheres, increases the importance of thorough
                                                                    understanding of anatomical and functional features of the
                                                                    cerebellum and their relationship with the deep nucleus8,10.
                                                                         The suboccipital and supracerebellar approaches have
                                                                    been used for lesions in the suboccipital hemispheres and
                                                                    vermis and they have also been adapted for lesions located
                                                                    in the quadrigeminal cistern. In planning operative strate-
                                                                    gies to tumors of the cerebellum, arteriovenous malforma-
                                                                    tions (AVMs) and other pathologies, it is helpful to consider
                                                                    operative landmarks for localizing avoidable structures10-13. If
                                                                    we examine the suboccipital surface of the cerebellum care-
                                                                    fully, the best anatomic landmarks are the tonsils, uvula, and
                                                                    middle line11. The lateral border of the dentate nucleus is
Fig 7. Basal surface view of the right cerebellar hemisphere.
The cerebellar hemisphere has been partially sectioned to           separated on an average of 26 mm from the lateral border of
show the cortex and the subcortical area at the level of the        the cerebellum, 23 mm from the posterior border of the cer-
dentate nucleus. The lateral border of the cerebellar cortex        ebellum and 25 mm from the posterolateral angle. Therefore,
is separated on an average of 14.8 mm, at the level of the
                                                                    these parameters are actually the medial and posterior limits
dentate nucleus from the subcortical white matter; and the
posterior border of the cerebellar cortex is separated on an        of the resection and they are easily intraoperatively identi-
average of 15.4 mm from the subcortical white matter.               fied. If a line is traced from the posterosuperior angle of the
                                                                    uvula to the posterior part of the dentate nucleus, there is an
relations with the deep cerebellar nuclei and with the cortex       average distance of 16 mm and with 38º of separation from
are more constant. The cerebellar peduncles are connected           the middle line (range – from 30 to 42 grades), almost the en-
to the white matter within the ventral and posterolateral           tire dentate nucleus will stay above and medial to this line.
aspects of the cerebellum; the superior cerebellar peduncle              The best anatomic landmark for the superior limit of the re-
follows an ascendant trajectory to the mesencepahlon, its           moval is the tonsil and the telovelotonsillar cleft. Also, the den-
tract fibers run from the posterolateral segment of the hemi-       tate nucleus is approximately situated, lateral from the mid-
sphere to the superior pole of the dentate nucleus, bordering       dle line at the level of the posterosuperior angle of the uvula.
the lateral aspect of the ventricle roof and medially relating      However, during the resection, only the inferior pole of the ton-
to the superior medullary velum, their straight up bundles          sil is well-visualized. The inferior pole of the tonsil is separated



                                                                                         Ramos A et al. Cerebellar surgical resections   445
on an average of 19 mm from the basal surface of the dentate                      border of the nucleus is separated on an average of 18.5 mm
  nucleus, and the tonsil has a superolateral implantation base                     from the middle line. The nucleus is located at the junction
  that is at the middle level of the dentate nucleus. When viewed                   of the upright surface with the flat one. The distance from
  from its medial aspect, the lateral border of the dentate nucle-                  the dentate nucleus to the level of the tentorial surface is ap-
  us is separated on an average of 19 mm from the middle line,                      proximately 17 mm.
  and the basal surface of the dentate nucleus is located at the                        In conclusion, the thorough knowledge of cerebellum
  telovelotonsillar cleft. Thus, 19 mm from the middle line is ac-                  anatomy has a tremendous neurosurgical importance. When
  tually the middle limit of the hemispheric resection.                             dealing with the cerebellum, it is judicious to devise in ad-
      Difficulty on performing a tentorial surface resection is                     vance a comprehensive plan of surgical approach and expo-
  evident. Useful landmarks to be followed during this stage of                     sure that offers adequate response to all of the foreseeable
  surgery are the fissures and the vermis. The dentate nucle-                       postoperative complications, which may potentially preju-
  us is located anteriorly to the tentorial fissure and the lateral                 dice the patient’s optimal outcome.


  References

  1.	   Carpenter MB. Core text of Neuroanatomy. Baltimore: Williams &              8.	    Rhoton Al Jr. Microsurgical anatomy of posterior fossa cranial nerves.
        Wilkins; 1991.                                                                     In: Barrow DL (Ed). Surgery of the cranial nerves of the posterior fossa.
  2.	   Rhoton AL Jr. Cerebellum and Fourth ventricle. Neurosurgery                        Neurosurgical topics. Chicago: AANS; 1993: 1-103.
        2000;47(Suppl):S7-S27.                                                      9.	    Youmans JR. Neurological surgery. Philadelphia: WB Saunders; 1996.
  3.	   Lang J. Clinical anatomy of the posterior cranial fossa and its foramina.   10.	   Yasargyl MG. Microneurosurgery Sttugart: Gerog Thieme Verlag; 1984.
        New York: Stuttgart, Georg Thieme; 1991.                                    11.	   Matsushina T, Fukui M, Inoue T, Natori Y, Baba T, Fujii K. Microsurgical
  4.	   Machado A. Neuroanatomia Funcional. Estrutura e funções do                         and magnetic resonancia imagen anatomy of the cerebellomedulary
        cerebelo. São Paulo: Atheneu; 1981, p. 179-186.                                    fissure and its application during fourth ventricle surgery.
  5.	   Brazis PW, Masdeu J, Biller J. Localization in Clinical Neurology. New             Neurosurgery 1992;30:325-330.
        York: Little, Brown; 1996. p. 365-379.                                      12.	   Holmes G. The croonian lectures on the clinical symptoms of cerebellar
  6.	   Rhoton AL Jr. The Posterior             Fossa    Veins.   Neurosurgery             disease and their interpretation. Lancet 1992;2:59-65,111-115.
        2000;47(Suppl):S69-S92.                                                     13.	   Yasargyl MG. Microneurosurgery: CNS tumors-surgical anatomy,
  7.	   Mussi A, Rhoton AL Jr. Telovelar approach to the fourth ventricle:                 neurophatology, neuroradiology, neurophisiology, clinical considerations,
        microsurgical antomy. J Neurosurg 2000;92:812-823.                                 operability, treatment options. Stuttgart: Georg Thieme; 1994.




446     Arq Neuropsiquiatr 2012;70(6):441-446

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Cerebellar anatomy as applied to cerebellar microsurgical resections

  • 1. Article Cerebellar anatomy as applied to cerebellar microsurgical resections Anatomia cerebelar aplicada à microcirurgia cerebelar ablativa Alejandro Ramos1, Feres Chaddad-Neto2, Hugo Leonardo Dória-Netto3, José Maria de Campos-Filho3, Evandro Oliveira4 Abstract Objective: To define the anatomy of dentate nucleus and cerebellar peduncles, demonstrating the surgical application of anatomic landmarks in cerebellar resections. Methods: Twenty cerebellar hemispheres were studied. Results: The majority of dentate nucleus and cerebellar pe- duncles had demonstrated constant relationship to other cerebellar structures, which provided landmarks for surgical approaching. The lat- eral border is separated from the midline by 19.5 mm in both hemispheres. The posterior border of the cortex is separated 23.3 mm from the posterior segment of the dentate nucleus; the lateral one is separated 26 mm from the lateral border of the nucleus; and the posterior segment of the dentate nucleus is separated 25.4 mm from the posterolateral angle formed by the junction of lateral and posterior borders of cerebellar hemisphere. Conclusions: Microsurgical anatomy has provided important landmarks that could be applied to cerebellar surgical resections. Key words: cerebellum, anatomy, neurosurgery. Resumo Objetivo: Definir a anatomia do núcleo denteado e dos pedúnculos cerebelares, demonstrando a aplicação dos marcos anatômicos em cirurgias cerebelares. Métodos: Foram estudados 20 hemisférios cerebelares. Resultados: A maioria dos núcleos denteados e pedúnculos cerebelares demonstraram relação anatômica constante com outras estruturas cerebelares, fato que proporcionou o estabelecimento de marcos anatômi- cos específicos a serem utilizados em acessos cirúrgicos. O bordo lateral do núcleo denteado é separado da linha média em 19,5 mm em ambos os hemisférios cerebelares. O bordo posterior do córtex é separado do segmento posterior do núcleo denteado por 23,3 mm. O bordo lateral do córtex é separado do bordo lateral do núcleo por 26 mm e o segmento posterior do núcleo denteado é separado por 25,4 mm do ângulo poste- rolateral, que é formado pela junção dos bordos lateral e posterior do hemisfério cerebelar. Conclusões: O estudo da anatomia microcirúrgica proporcionou o estabelecimento de marcos anatômicos importantes que podem ser utilizados durante cirurgias cerebelares ablativas. Palavras-Chave: cerebelo, anatomia, neurocirurgia. The cerebellum is an exquisite anatomic structure with- with the final objective of performing better operations with less in the human brain, which needs to be considered from the damage to the cerebellar nucli and important deep pathways. surgical standpoint because of its functional importance and common pathologies that affect this area1. It is possible to reach the cerebellum avoiding damaging neural structures by METHODS approaches which target tentorial, petrosal, or suboccipital surfaces. Each has its microsurgical particularities in order to The dentate nucleus, cerebellar peduncles and their rela- reach the desired region and preserve neural structures2. tionship with others cerebellar structures were studied in 20 In this article, we have presented the microsurgical anatomy of adult cerebellar hemispheres, 12 male and 8 female corpses, the suboccipital and supracerebellar approaches to the cerebellar obtained from São Paulo death verification service using X3 surfaces using comprehensives anatomic and functional relations to X40 magnifications. Neurosurgeon Fellow of Microanatomy Laboratory in Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil; 1 Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo; Coordinator of Microanatomy Laboratory in 2 Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil; Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil; 3 Neurosurgeon of Instituto de Ciências Neurológicas (ICNE) and Hospital Beneficência Portuguesa of São Paulo; Director of Microanatomy Laboratory in 4 Hospital Beneficência Portuguesa of São Paulo, São Paulo SP, Brazil. Correspondence: Hugo Leonardo Dória Netto; Instituto de Ciências Neurológicas; Praça Amadeu Amaral 27 / 5º andar; 01327-010 São Paulo SP - Brasil; E-mail: hldoria@hotmail.com Conflict of interest: There is no conflict of interest to declare. Received 11 July 2011; Received in final form 07 December 2011; Accepted 14 December 2011 441
  • 2. Histological and functional considerations tentorium and posteriorly limited by the lateral sinus and lat- The cerebellum has a special cytoarchitecture, which erally by the sigmoid sinus; the division between the lateral makes it unique3. Histologically the cortex presents three and sigmoid sinus is located at the junction with the supe- layers of cells that involve a central white substance. rior petrosal sinus. The tentorial surface has two incisures in These layers include the molecular, the Purkinje, and the the midline: the anterior one is related to the brain stem and granular cells. The only efferent cells are the Purkinje ones the posterior incisure is related to the falx cerebelli. There are that end in the central nucleus playing an inhibition ac- two fissures on the tentorial surface, which divide this sur- tion. The layer in contact with the white substance is con- face into anterior, middle, and posterior parts. The anterior stituted of granular cells. Two different kinds of afferents fissure is the tentorial one and the posterior fissure is the cerebellar fibers arrive to the cerebellar cortex: the fibers postclival one. The vermian surface is the most superior part that interconnect the caudal olives with the purkinje cells of this surface. (olivocerebellar tract) and the myelinic fibers that come The posterior inferior or suboccipital surface is located to an end in the granular layer (pontocerebellar, spinocer- down the lateral sinus and inferomedially to the sigmoid si- ebellar, and vestibulocerebellar tracts)4. nus6. The falx cerebelli extends from the tentorial surface above The Purkinje cells are the main afferents of the cerebellar to the inferior part of the middle suboccipital surface, the falx nucleus and most of the efferent fibers from the cerebellum overlies a vertical depression that is medially formed by the come from these nuclei; there are four nuclei in the cerebel- vermis, laterally by the medial aspects of the cerebellar hemi- lum, which includes from medial to lateral, the fastigial, glo- spheres and continues inferiorly with the vallecula cerebelli. bose, emboliform, and dentate nucleus1,2. The cerebellum can When it is viewed from a posterior position, the only part be longitudinally subdivided as follows: a midline zone, con- of the vermis that is uncovered on this surface is at the side taining axons projecting to the fastigial nucleus and connect- where the pyramid meets the uvula, located down this sur- ing with the vestibular nucleus and reticular formation; an face. There are two fissures on the suboccipital surface that intermedial zone, projecting to the nucleus interpositus (glo- divide it in superior, middle, and inferior parts. The superior bose and emboliform) and connecting with the contralateral fissure is the petrosal and the inferior is the suboccipital one. red nucleus and thalamic nucleus with impulses to the cere- The tonsils are the most prominent hemispheric structures bral cortex; and a lateral zone, containing axons to the dentate of the suboccipital surface, located inferomedially. The ton- nucleus, which course to the contralateral thalamic nucleus sils are ovoid structures, which have a middle vertical size of that transmits impulses to the cerebral cortex. Functionally, 13.5 mm (range from 10 to 18 mm) and a wide size of 7.8 mm this nucleus controls a different type of movements: the fas- (range from 5 to 10 mm). The tonsils have an implantation tigial controls posture and gait; the nucleus interpositus con- base to the suboccipital surface of the cerebellum at the su- trols segmental reflexes and assists the initiation of move- perior lateral border and they are superoanteriorly related to ments; and the dentate nucleus controls fine dexterity. One the inferior medullary velum and tela choroidea, laterally to of the main important features of the cerebellum is its con- the biventral lobule, superolaterally to the tellovelotonsilar trol on the automatic excitation of antagonist muscles at the cleft, posteriorly and inferiorly to the cistern magna, medially end of the movement with simultaneous inhibition of the ag- onist muscles, which initiated the movement5. Afferent fibers from the brain stem project to the cerebel- lum by the inferior, middle, and superior cerebellar peduncle. Afferent fibers from the medulla carry the anterior and pos- terior spinocerebellar tract that project to the cerebellum by the superior and inferior cerebellar peduncles. The pontine fibers from the pontine nucleus project to the cerebellum by the middle cerebellar peduncle. The cerebello vestibular fibers, from the vestibular nucleus, project to the cerebel- lum by the inferior cerebellar peduncle. Most of the effer- ent fibers from the cerebellum go to the superior cerebellar peduncle4,5. Anatomic considerations Anatomically, the cerebellum can be considered as a Fig 1. Suboccipital surface view. The vallecula extends three-surface triangle: tentorial, suboccipital, and petrosal between the tonsils and communicates through the foramen surfaces2. The posterior-superior or tentorial surface is the of Magendie with the fourth ventricle. 1: tonsil; 2: vallecula; 3: most regular of all surfaces. It is surrounded superiorly by the uvula; 4: PICA. 442 Arq Neuropsiquiatr 2012;70(6):441-446
  • 3. to the vallecula cerebelli, superomedially to the uvula, and vein of Galen; the veins of the cerebellomedullary fissure and anteriorly to the medulla2,7 (Fig 1). inferior cerebellar peduncle drain into the petrosal veins; the The tentorial surface is related to the superior cerebel- veins of the cerebellopontine fissure and of the middle cer- lar artery, which arises at the pontomesecenphalic junc- ebellar peduncle also drain through the petrosal ones3,6. tion, encircles the brain stem, and is directed medially and backward to the tentorial surface. The artery runs as a single trunk up to the lateral pontomesencephalic segment, where RESULTS the artery commonly divides into two trunks: the superior runs within the mesencephalic fissure, passes down to the After our research, we could conclude that the lateral bor- inferior colliculus, and continues posteromedially to the der of the dentate nucleus is separated from the midline by superior half of the fourth ventricle. The inferior trunk also an average of 19.5 mm in the right hemisphere (range – from runs within the anterior part of the mesencephalic fissure, 17 to 21 mm) and 19.5 mm in the left ones (range – from 14 to but shortly, the artery turns superolaterally to the tentorial 23 mm), as seen in Fig 2. surface. The branches of these trunks give off the precerebel- The dentate nucleus has a unique shape. It is oriented in lar arteries which course medially from the mesencephalic craniocaudal direction and from lateral to medial. It is help- fissure to the superior peduncle and dentate nucleus. The ful to consider the dentate nucleus with upper and lower sur- anterior inferior cerebellar artery (AICA) arises at the ante- faces, and three segments. The upper surface is related medi- rior pontine level; passes around the cerebellopontine fis- ally to the superior cerebellar peduncle and faces the vermis sure and goes to the pontomedullar segment, dividing into at the junction of the cumen and declive. The upper surface two trunks. The rostral trunk passes between the facial and is bordered laterally, anteriorly, and posteriorly by the fibers vestibulocochear nerves and around the superior part of the of the middle cerebellar peduncle. At the basal surface, the flocculus to supply the middle peduncle. The caudal trunk dentate nucleus is related anteriorly to the caudal segment of passes below the flocculus near the IX and X nerves to sup- the flocculus, medially to the telovelotonsillar cleft and pos- ply the petrosal surface. The posterior inferior cerebellar teromedially to the superior pole of the tonsil and the lateral artery (PICA) arises at the anterior medullary level, passes border of the uvula in its posterolateral third (Fig 3). around the medulla, crosses the inferior cerebellar peduncle, The distance from the posterior extreme of the uvula to enters the cerebellomedullar fissure, where it is closely re- the posterior segment of the dentate nucleus is on average lated to the inferior half of the fourth ventricle, and exits the 16.2 mm (range – from 13 to 20 mm). The posterior border fissure to supply the suboccipital surface8. of the cortex is separated on an average of 23.3 mm (range – The veins of the cerebellum are divided into superficial from 20 to 29 mm) from the posterior segment of the dentate and deep. The superficial group is divided into tentorial, nucleus; the lateral border of the cortex is separated on an petrosal, and suboccipital veins. The tentorial surface veins average of 26 mm (range – from 15 to 32 mm) from the lat- are drained by the superior hemispheric and vermian veins, eral border of the nucleus; and the posterior segment of the which empty into the vein of Galen and the tentorial sinuses. dentate nucleus is separated on an average of 25.4 mm (range The petrosal surface veins are drained by the anterior hemi- spheric veins, which empty mainly into the superior petrosal sinus. The suboccipital surface veins are drained by the inferi- or hemispheric and inferior vermian veins, which commonly empty into the tentorial sinuses. The deep veins are divided into: the vein of the cerebellomesecephalic fissure that is re- lated to the superior half of the roof of the fourth ventricle; the vein of the cerebellomedullary fissure that is related to the inferior half of the roof; and the vein of the cerebellopon- tine fissure that is related to the laterals walls of the fourth ventricle. The veins of the three peduncles also course within these fissures. The vein of the superior cerebellar peduncle courses in the cerebellomesencephalic fissure; the one from the middle cerebellar peduncle courses in the anterior part of the cere- bellopontine fissure; and the one from the inferior cerebellar peduncle courses in the cerebellomedullary fissure. In gener- Fig 2. Basal surface of the cerebellum. The left and right cerebellar hemispheres have been removed to expose the al terms, the vein of the cerebellomesencephalic fissure and dentate nucleus and its relationship with the tonsils. 1: uvula; the vein of the superior cerebellar peduncle drain into the 2: dentate nucleus; 3: tonsil; 4: vallecula. Ramos A et al. Cerebellar surgical resections 443
  • 4. – from 17 to 31 mm) from the posterolateral angle, which is and the lateral zone is the cortex. This is based on similar formed by the junction of the lateral and posterior borders of structures related in each zone9. the cerebellar hemisphere (Fig 4). The cerebellum is connected to the brain stem by three The distance from the inferior pole of the tonsil to the lev- large cerebellar peduncles, each peduncle displays a special el of the basal surface of the dentate nucleus is approximately shape that creates a particular stratification in the cerebel- 19.4 mm on the right side (range – from 18 to 22 mm) and lar hemisphere; the relations between the peduncles, the cer- 19.4 mm (range – from 16 to 25 mm) on the left one, as seen ebellar cortex and the cerebellar nuclei are extremely impor- in Figs 5 and 6. tant to access the cerebellum10. From the basal suboccipital surface to the tentorial one, The white matter of the cerebellum forms a central core, the association fibers of the white matter start to form thick which receives afferent fibers from the cortex; these fibers laminae or lobular peduncles at 10 mm (range – from 0.8 create laminae of white matter that comes from the cor- to 1.4 mm) from the superior pole of the tonsil. The cortex tex to the central core. The pathways and the central core of the cerebellum is not divided into gyri, but instead into have variable shapes in each cerebellar hemisphere, but the numerous folia. According to Lange, the cortical portion of the cerebellum forms about 67% of the total surface area. In this study, the lateral border of the cerebellar cortex is separated on an average of 14.8 mm (range – from 10 to 25  mm) at the level of the dentate nucleus, from the sub- cortical white matter or lobular peduncle; and the posterior border of the cerebellar cortex is separated on an average of 15.4 mm (range – from 0.8 to 24 mm), from the subcortical white matter (Fig 7). DISCUSSION From a surgical perspective, it is helpful to consider the cerebellar hemispheres as a three-component structure that can be divided into median, paramedian, and lateral zones. Fig 4. Suboccipital surface view of the cerebellum. Notice that The median zone extends from the lateral border of the ver- the distance from the middle line to the lateral border of the dentate nucleus is 19.5 mm and 38º is the angle of separation mis to the lateral one of the dentate nucleus; the paramedian from the middle line to avoid the dentate nucleus during the zone extends from the lateral border of the dentate nucleus surgical resections. Also, the distance from the middle line to to the junction of the white matter substance and the cortex; the lateral border of the tonsil is approximately 16 mm. Fig 3. Basal surface of the cerebellar hemisphere. The left Fig 5. Suboccipital surface view of the cerebellum. The distance cerebellar hemisphere and the tonsil have been removed from the middle line to the lateral border of the dentate nucleus to expose the uvula and their relationship with the superior is approximately 19.5 mm and the distance from the inferior pole of the tonsil and the dentate nucleus. 1: dentate nucleus; pole of the tonsil to the level of the basal surface of the 2: uvula; 3: flocculus; 4: middle cerebellar peduncle; 5: superior dentate nucleus is approximately 19.4 mm. Also, 16 mm is the pole place of the tonsil after removed. distance from the middle line to the lateral border of the tonsil. 444 Arq Neuropsiquiatr 2012;70(6):441-446
  • 5. are always medial to the dentate nucleus and located in the median zone. The middle cerebellar peduncle has the widest posterolateral projection and it is almost always located in the paramedian zone; it follows a descendent course from the pons. The fibers of the middle cerebellar peduncle can be divided into superior, middle, and inferior. The superior part of the fibers crosses the inferior third of the superior pedun- cle and runs alongside the median aspect of the dentate nu- cleus. The middle part of the fibers course posterolaterally alongside the lateral segment of the dentate nucleus around the hemisphere. The inferior tract fibers of the middle ce- rebral peduncle follow a descendent course and are closely related to the fibers of the inferior cerebellar peduncle at the rostral pole of the dentate nucleus. The inferior cerebellar Fig 6. The right cerebellar hemisphere has been sectioned peduncle ascends alongside the lateral recess and floor of to show the different relationships of the dentate nucleus to the nearby structures. The distance from the lateral border the fourth ventricle with most of its fibers distributed mainly of the dentate nucleus to the middle line is on an average of to the rostral pole of the dentate nucleus, these tract fibers 19.5 mm; the distance from the inferior pole of the tonsil to the are medially related to the dentate nucleus and are mainly basal surface of the dentate nucleus is on average 19.4 mm and 38º is on average the angle of separation from the middle located in the median zone. There is an extraordinary medi- line to lateral border of the dentate nucleus. cal significance attached to the nuclei of the cerebellum and, among these, particularly  to the dentate nucleus3. The den- tate nucleus is the most lateral nucleus of the cerebellum and it is located in the median zone of the hemisphere. The high frequency, in which the cerebellum is operated, exposing the cerebellar hemispheres, increases the importance of thorough understanding of anatomical and functional features of the cerebellum and their relationship with the deep nucleus8,10. The suboccipital and supracerebellar approaches have been used for lesions in the suboccipital hemispheres and vermis and they have also been adapted for lesions located in the quadrigeminal cistern. In planning operative strate- gies to tumors of the cerebellum, arteriovenous malforma- tions (AVMs) and other pathologies, it is helpful to consider operative landmarks for localizing avoidable structures10-13. If we examine the suboccipital surface of the cerebellum care- fully, the best anatomic landmarks are the tonsils, uvula, and middle line11. The lateral border of the dentate nucleus is Fig 7. Basal surface view of the right cerebellar hemisphere. The cerebellar hemisphere has been partially sectioned to separated on an average of 26 mm from the lateral border of show the cortex and the subcortical area at the level of the the cerebellum, 23 mm from the posterior border of the cer- dentate nucleus. The lateral border of the cerebellar cortex ebellum and 25 mm from the posterolateral angle. Therefore, is separated on an average of 14.8 mm, at the level of the these parameters are actually the medial and posterior limits dentate nucleus from the subcortical white matter; and the posterior border of the cerebellar cortex is separated on an of the resection and they are easily intraoperatively identi- average of 15.4 mm from the subcortical white matter. fied. If a line is traced from the posterosuperior angle of the uvula to the posterior part of the dentate nucleus, there is an relations with the deep cerebellar nuclei and with the cortex average distance of 16 mm and with 38º of separation from are more constant. The cerebellar peduncles are connected the middle line (range – from 30 to 42 grades), almost the en- to the white matter within the ventral and posterolateral tire dentate nucleus will stay above and medial to this line. aspects of the cerebellum; the superior cerebellar peduncle The best anatomic landmark for the superior limit of the re- follows an ascendant trajectory to the mesencepahlon, its moval is the tonsil and the telovelotonsillar cleft. Also, the den- tract fibers run from the posterolateral segment of the hemi- tate nucleus is approximately situated, lateral from the mid- sphere to the superior pole of the dentate nucleus, bordering dle line at the level of the posterosuperior angle of the uvula. the lateral aspect of the ventricle roof and medially relating However, during the resection, only the inferior pole of the ton- to the superior medullary velum, their straight up bundles sil is well-visualized. The inferior pole of the tonsil is separated Ramos A et al. Cerebellar surgical resections 445
  • 6. on an average of 19 mm from the basal surface of the dentate border of the nucleus is separated on an average of 18.5 mm nucleus, and the tonsil has a superolateral implantation base from the middle line. The nucleus is located at the junction that is at the middle level of the dentate nucleus. When viewed of the upright surface with the flat one. The distance from from its medial aspect, the lateral border of the dentate nucle- the dentate nucleus to the level of the tentorial surface is ap- us is separated on an average of 19 mm from the middle line, proximately 17 mm. and the basal surface of the dentate nucleus is located at the In conclusion, the thorough knowledge of cerebellum telovelotonsillar cleft. Thus, 19 mm from the middle line is ac- anatomy has a tremendous neurosurgical importance. When tually the middle limit of the hemispheric resection. dealing with the cerebellum, it is judicious to devise in ad- Difficulty on performing a tentorial surface resection is vance a comprehensive plan of surgical approach and expo- evident. Useful landmarks to be followed during this stage of sure that offers adequate response to all of the foreseeable surgery are the fissures and the vermis. The dentate nucle- postoperative complications, which may potentially preju- us is located anteriorly to the tentorial fissure and the lateral dice the patient’s optimal outcome. References 1. Carpenter MB. Core text of Neuroanatomy. Baltimore: Williams & 8. Rhoton Al Jr. Microsurgical anatomy of posterior fossa cranial nerves. Wilkins; 1991. In: Barrow DL (Ed). Surgery of the cranial nerves of the posterior fossa. 2. Rhoton AL Jr. Cerebellum and Fourth ventricle. Neurosurgery Neurosurgical topics. Chicago: AANS; 1993: 1-103. 2000;47(Suppl):S7-S27. 9. Youmans JR. Neurological surgery. Philadelphia: WB Saunders; 1996. 3. Lang J. Clinical anatomy of the posterior cranial fossa and its foramina. 10. Yasargyl MG. Microneurosurgery Sttugart: Gerog Thieme Verlag; 1984. New York: Stuttgart, Georg Thieme; 1991. 11. Matsushina T, Fukui M, Inoue T, Natori Y, Baba T, Fujii K. Microsurgical 4. Machado A. Neuroanatomia Funcional. Estrutura e funções do and magnetic resonancia imagen anatomy of the cerebellomedulary cerebelo. São Paulo: Atheneu; 1981, p. 179-186. fissure and its application during fourth ventricle surgery. 5. Brazis PW, Masdeu J, Biller J. Localization in Clinical Neurology. New Neurosurgery 1992;30:325-330. York: Little, Brown; 1996. p. 365-379. 12. Holmes G. The croonian lectures on the clinical symptoms of cerebellar 6. Rhoton AL Jr. The Posterior Fossa Veins. Neurosurgery disease and their interpretation. Lancet 1992;2:59-65,111-115. 2000;47(Suppl):S69-S92. 13. Yasargyl MG. Microneurosurgery: CNS tumors-surgical anatomy, 7. Mussi A, Rhoton AL Jr. Telovelar approach to the fourth ventricle: neurophatology, neuroradiology, neurophisiology, clinical considerations, microsurgical antomy. J Neurosurg 2000;92:812-823. operability, treatment options. Stuttgart: Georg Thieme; 1994. 446 Arq Neuropsiquiatr 2012;70(6):441-446