Abstract
Surgery of the posterior fossa represents a technical challenge because of the proximity of the vessels of the cerebellum. If the arterial vascularization of the cerebellum is well known, the main arterial variations and the whole venous vascularization are probably under recognized. We describe the vascular organization and the main variations through photographs of colored latex perfused brains, obtained with a surgical microscope. The arterial vascularization of the cerebellum is based on three arteries which all originate from the vertebrobasilar system: the superior cerebellar artery (SCA), the anterior and inferior cerebellar artery (AICA), and the posterior and inferior cerebellar artery (PICA). The main arterial variations involve essentially the origin of these vessels. Concerning the SCA, its origin depends on the embryology. The AICA can arise from a common trunk AICA-PICA. It can be sometimes doubled and rarely absent. The PICA also can arise from a common trunk AICA-PICA and sometimes from the extradural segment of the vertebral artery. Concerning the venous organization, we distinguish the superficial and deep veins. The superficial veins drain the cerebellar cortex and transit on the surface of the cerebellum. The deep veins refer to the veins transiting in the fissures between the cerebellum and the brainstem. All these veins terminate as bridging veins that we can divide in three groups: a superior group emptying into the great vein, a posterior group emptying into the transtentorial sinus, and a lateral group ending into the superior petrosal sinus. The surgical implications are discussed.
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Introduction
Surgery of the cerebellum represents a technical challenge because of the proximity of the brainstem, the cranial nerves, and the vessels in the posterior fossa. Contrary to brainstem and cranial nerves which are already well understood, a good knowledge of the vascularization of the cerebellum and its variations seems mandatory before performing surgery in this area.
Materials and Methods
Twenty-five formalin-fixed human heads were perfused with red- and blue-colored latex. Additional fixed, but non-injected, brains were used for morphological study. The brains were removed some days later, and the cerebellum was examined using a Wild Leitz surgical microscope with a D-80 Nikon photographic attachment set. We examined the arteries and veins of the cerebellum.
Anatomical Description
We start with the morphology of the cerebellum, followed by a description of the arteries and veins with particular attention paid to the vascular variations.
Reminder: Morphology of the cerebellum (anterior view, superior view, and inferior view)
The posterior cranial fossa includes the cerebellum and the brainstem. The cerebellum is attached laterally to the brainstem through the cerebellar peduncles and through the superior and inferior medullary velum which cover the fourth ventricle on the midline.
Anterior view
The anterior view allows us to reveal the cerebellopontine angle (Fig. 1). Each cerebellar hemisphere is divided by a horizontal fissure which is referred to as a horizontal fissure or petrosal fissure. Above this fissure, we can see from medially to laterally the quadrangular lobule, the simple lobule, and the superior semilunar lobule; under this fissure, from laterally to medially, we can identify the inferior semilunar lobule, the gracile lobule, the biventral lobule, and the cerebellar tonsillar partially hidden by the brainstem. The flocculus stays at the medial part of the horizontal fissure.
Laterally, we can see the apparent origin of the cranial nerves from the brainstem.
Superior view
The superior view shows the tentorial surface of the cerebellum (Fig. 2). Laterally, we find the hemisphere segmentation in lobules, as described previously, located above the horizontal fissure. In the midline, we observe vermian lobules from anterior to posterior: the lingula, the central lobule, the culmen, the declive, and the folium.
Inferior view
The inferior view shows the inferior vermian lobules on the midline: from posterior to anterior folium, tuber, pyramid, and uvula (Fig. 3). Laterally, we find the hemispheric segmentation as described above and the cerebellomedullary fissure.
Arteries of the Cerebellum
We can distinguish three cerebellar arteries: the superior cerebellar artery (SCA), the anterior inferior cerebellar artery (AICA), and the posterior inferior cerebellar artery (PICA). These arteries all originate from the vertebrobasilar arterial system (Figs. 4 and 5).
SCA
The SCA is the most constant vessel and commonly arises from the basilar trunk (Figs. 6 and 7). Its origin depends on the embryology. Sometimes the SCA originates from the junction of the basilar tip and the first segment of the posterior cerebral artery (P1) (Fig. 8) or directly from P1 (Fig. 9) with a symmetrical or asymmetrical aspect [1–3].
The aspect of the basilar tip depends on the site of fusion of the posterior division of the ICA. The more caudal the fusion is, the more frequent the duplicate origin of the SCA becomes (Fig. 10).
When the SCA originates from the basilar artery, it passes below the third cranial nerve, and when it comes from P1, it can pass above the oculomotor nerve [3]. Classically, the SCA transits under the third cranial nerve and the fourth cranial nerve before joining the lateral side of the pontomesencephalic junction (Figs. 5 and 6). After crossing the trigeminal nerve, above or under, the SCA splits into two branches: the medial and the lateral branches which transit along the free edge of the tentorium. Both these arteries join the cerebellomesencephalic fissure (Fig. 11).
The medial branch leads to two branches: a medial branch for the mesencephalon, the superior and inferior colliculi and the cerebellar cortex, and a lateral branch for the vermis and the superolateral cortex of the cerebellar hemisphere (Figs. 12, 13, and 14).
The medial branch vascularises by descending branches, the superior vermis and the neighboring part of the surface of the cerebellar hemisphere; it also sends rami running along the superior cerebellar peduncles and reaching the dentate nucleus and can contribute to some other deep nuclei (globulus, emboliform, and fastigial) (Figs. 13, 14, and 15).
The lateral branch vascularises the most lateral part of the superior cerebellar cortex, i.e., the quadrangular, simple, and semilunar lobules (Fig. 16). The perforating arteries supplying the deep nuclei can arise from the SCA main trunk, but also from the medial and lateral branches of the first division.
It is important to notice that there are some anastomosis between the SCA and the AICA (Fig. 14) and between the SCA and the PICA as described below.
Aica
The AICA arise from the basilar trunk in 99 % of cases and classically from the lower third (75 % of cases). It can also arise close to the vertebrobasilar junction in 9 % of cases (Fig. 5).
This vessel is also called the cerebellolabyrinthine artery because it gives off the labyrinthine artery in 90 % of cases [1–6].
Sometimes we may observe a common trunk for AICA and PICA arising from the basilar artery (Fig. 17). There is often also an accessory PICA (Fig. 17) or accessory AICA (Fig. 18).
Rarely, there is no AICA (4 % of cases): the AICA comes from a common trunk arising from the vertebral artery or directly from the PICA (Fig. 19).
In some cases, there is a duplicate AICA with a small branch giving off the labyrinthine artery and the vascularisation of the flocculus and a larger branch supplying the semilunar and biventral lobule (Fig. 20).
The AICA transits then above or below the sixth nerve. It can perforate the sixth nerve or passes between two rootlets of the nerve (Fig. 21).
After crossing the sixth nerve, AICA joins the cerebellopontine angle and the facial and cochleovestibular nerves.
It can also pass between [7] (Fig. 22), below (Fig. 23) or above (Fig. 24), the facial and cochleovestibular nerves.
At this level, the AICA gives off the labyrinthine and the subarcuate arteries. The labyrinthine artery follows and supplies the vestibulocochlear and the facial nerves (Fig. 25). It enters the internal auditory canal and terminates by giving rise to vestibular, cochlear and vestibulocochlear arteries.
The AICA then bifurcates into two branches. The bifurcation takes place before (in two-thirds of cases) or after (in one-third of cases) crossing the facial and cochleovestibular nerves [3]. We distinguish the rostrolateral branch and the caudomedial branch (Fig. 26).
The rostrolateral branch transits laterally above the horizontal fissure and the flocullus in front of the middle cerebellar peduncle, before combining with the superior lip of the cerebellopontine fissure and the adjacent petrosal cerebellar surface (Fig. 26).
The caudo medial branch transits below the flocculus and gives off cortical branches for the petrosal surface around the horizontal fissure. It then penetrates in the inferior cerebello medullary fissure where it transits along the foramen of Lushka and then goes back on to the anterior petrosal surface of the cerebellar hemisphere ending by giving rise to cortical arteries (Fig. 26).
The AICA usually supplies the anterior surface of the simple, superior, and inferior semilunar lobules as well as the flocculus, the choroid plexuses of the lateral ventricular recess, and the middle cerebellar peduncle; in fact, as we have seen above, its caliber as well its cerebellar vascular territory are quite variable.
We typically notice some anastomoses between the rostral branch and the SCA and between the caudal branch and the PICA.
We can see a lack of division in some cases (Fig. 27). In this case, the AICA transits along the horizontal fissure.
Pica
The PICA usually stems from the vertebral artery 2 cm from the vertebral artery dural entrance (Fig. 28). The origin of the PICA is in reality variable: it can arise from a common trunk AICA-PICA of the basilar artery (as described above), from the extradural vertebral artery at the level of C1–C2 (or even C2–C3), from the ascending phayngeal artery, and from the proatlantal artery or from the ascending cervical artery [1–4, 8–16].
The PICA crosses the last cranial nerves, passing above, between, under, or through the ninth, tenth, eleventh, and twelfth cranial nerves [9] (Figs. 21 and 29).
At this level, the PICA gives rise to perforating branches for the lateral part of the medulla and the olive, sharing the area with the branches coming from the basilar artery, the AICA, and the vertebral artery. It is important to note that there are no perforators arising from the vertebral artery before the PICA origin (Fig. 30), except in the case of common AICA-PICA, or extradural PICA in which the VA gives off the perforators for the anterior and lateral aspect of the medulla (Fig. 31).
After crossing the last cranial nerves, the PICA transits on the lateral aspect of the medulla and in front of the anterior surface of the tonsilla, before describing its first caudal loop (Fig. 32). Sometimes, the first caudal loop is very extended and overflows significantly within the cisterna magna (Figs. 33 and 34).
The PICA then follows an ascending vertical route between the tonsilla and the dorsal surface of the medulla and reaches the superior medullary velum and the choroid plexus where it makes a second loop. It gives at this point the choroidal artery which supplies the tela choroidea and the choroid plexus (Fig. 35).
After this second loop, the PICA bifurcates into two branches on the medial side of the tonsilla (Fig. 36): the vermian branch (vermian trunk) for pyramid, uvula, nodule, and inferior part of the biventral lobule; and the tonsillo hemispheric branch (lateral trunk) for the superior part of the biventral lobule, the inferior part of the semilunar lobule and the tonsilla. The vermis can be vascularised bilaterally by the same PICA if the controlateral supplier is a common trunk AICA-PICA.
Tonsillo hemispheric branches and vermian branches terminate their transit on the cerebellar cortex (Figs. 4 and 37). The vermian cortical branches arise from the medial trunk and the tonsilar and hemispheric branches arise from the lateral trunk.
The cortical arteries originating from PICA establish anastomosis with the cortical branches of the SCA (Fig. 38).
Veins of the Cerebellum
We can describe two groups of veins: the superficial veins, which drain the cortical surface of the cerebellum, and the deep veins. All these veins terminate as bridging veins [2, 17, 18].
Superficial Veins
Tentorial surface
The superior cortical surface of the cerebellum is drained by the superior vermian veins and the superior hemispheric veins (Figs. 39 and 40). These veins empty into the great vein of Galen in the midline (Fig. 39) and in the transtentorial medial and lateral sinuses laterally which combine with the transverse and straight sinus (Figs. 41 and 42). The transtentorial sinus also drains the inferior surface of the temporal and occipital lobe (Fig. 42). From their cortical route to the transtentorial sinuses, the superior hemispheric veins form bridging veins (Fig. 41).
Suboccipital surface
The posterior inferior cortical surface of the cerebellum is drained by the inferior hemispheric veins and the inferior vermian veins. The hemispheric veins do not empty directly in the transverse sinus but via the transtentorial sinuses (Fig. 43). The inferior vermian veins typically empty in the straight sinus directly or via the medial transtentorial sinuses (Fig. 44). The inferior hemispheric vein can also combine with the inferior vermian veins before together merging with the straight sinus (Figs. 34 and 45). All these veins form bridging veins too.
Petrosal surface
The anterior cortical surface of the cerebellum is drained by the anterior hemispheric veins (AHV) (Figs. 46, 47, 48, and 49). We distinguish the middle AHVs which drain the cortex of the horizontal fissure, the inferior AHVs which drains the inferior part of the petrosal surface, and the superior AHVs which drain the superior part of the petrosal surface. These veins converge in the cerebellopontine fissure and in front of the middle cerebellar peduncle to form the vein of the cerebellopontine fissure. In this area, it receives the venous drainage from the brainstem through the vein of the middle cerebellar peduncle before combining with the superior petrosal vein (Figs. 49 and 50). The superior petrosal vein then empties in the superior petrosal sinus, also forming a bridging vein (Fig. 50).
The superior petrosal vein can be duplicated with a medial superior petrosal vein draining the brainstem and a lateral superior petrosal vein draining the cerebellum (Fig. 51).
Deep Veins
We use the term deep veins to refer to the veins transiting in the fissures between the brainstem and the cerebellum. We distinguish three groups of deep veins: the veins of the cerebellomesencephalic fissure, the veins of the cerebellopontine fissure, and the veins of the cerebello medullary fissure.
Veins Transiting in the Cerebellomesencephalic Fissure
We distinguish two groups of veins transiting in the cerebellomesencephalic fissure: the superomedial empties into the great vein of Galen and the superolateral empties into the superior petrosal vein. These two venous drainage groups are connected by the lateromesencephalic vein (Fig. 52).
The superomedial group is made up of the vein of the superior cerebellar peduncle and the supra cerebellar veins.
The vein of the superior cerebellar peduncle arises from the superior cerebellar peduncle and transits along the lateral face of the lingula. It then becomes the vein of the cerebellomesencephalic fissure (Fig. 53) and empties into the vein of Galen or into the superior vermian vein (Fig. 53).
The group of supracerebellar veins is made up of the tectal vein, the superior vermian vein, the culminal vein, the central veins which drain the superior part of the vermis, and the tectum (Figs. 54, 55, and 14).
The pontotrigeminal vein represents the superolateral group.
This vein transits along the superior cerebellar peduncle, passes above the trigeminal nerve, and combines with the vein of the cerebellopontine fissure to form the superior petrosal vein before terminating in the superior petrosal sinus (Fig. 11). Before the junction, it receives the superior hemispheric vein. There are often anastomoses between the ponto trigeminal vein and the lateromesencephalic vein on the medial extremity.
Veins Coursing in the Cerebellopontine Fissure
We distinguish two veins traveling along the cerebellopontine fissure:
The vein of the cerebellopontine fissure drains the petrosal surface of the cerebellum and comes from the junction of the stems of the anterior hemispheric vein. It drains into the superior petrosal sinus through the superior petrous vein. This vein can often be joined by the vein of the middle cerebellar peduncle and the ponto trigeminal vein to form a trunk that drains into the superior petrosal vein (Figs. 46, 47, 56).
The vein of the middle cerebellar peduncle comes from the fusion of the vein of the pontomedullary sulcus and the lateral medullary vein or the vein of the inferior cerebellar peduncle. It then transits along the lateral sides of the middle cerebellar peduncle, in the anterior part of the cerebellopontine fissure. It drains directly into the superior petrosal sinus or combines with other stems like the vein of the cerebellopontine fissure before together draining into the superior petrosal sinus (Figs. 47 and 56).
Veins Coursing in the Cerebello Medullary Fissure
We can distinguish the vein of the cerebellomedullary fissure and the vein of the inferior cerebellar peduncle.
The vein of the cerebello medullary fissure comes from the lateral side of the uvula of the vermis and transits along the junction of the inferior medullary velum and the tela choroidea, then under the lateral recesses of the fourth ventricle as far as the cerebellopontine angle (Figs. 57 and 58). This vein drains the inferior aspect of the cerebellum and notably the dentate nucleus (Fig. 59). It then merges with the transverse medullary vein and terminates in the anterior hemispheric vein (Fig. 60).
The vein of the inferior cerebellar peduncle transits along the inferior cerebellar peduncle. It comes from the posterior side of the medulla laterally to the foramen of Magendie. It passes below the lateral recesses and combines with the vein of the cerebellomedullary fissure (Figure 57). Inferiorly, the veins of the inferior cerebellar peduncle from each side may create anastomoses with the median posterior medullary vein by merging on the midline under the foramen of Magendie. The median posterior medullary vein can also create anastomoses with sinus converging on the jugular foramen or in an occipito marginal sinus through a bridging vein (Fig. 58).
Bridging Veins
All the veins of the cerebellum terminate as bridging veins which we can classify in three groups: a superior group emptying into the great vein (vein of Galen), a posterior group emptying into the transtentorial sinus, and a lateral group ending in the superior petrosal sinus (Figs. 39 and 42).
Discussion
As discussion, we propose to clarify some points concerning the anatomical variations of the cerebellar arterial vascularization and the technical aspect from the venous point of view for the posterior fossa approach.
We point out the variability of the arterial cerebellar vascularization concerning the deep nuclei and the cortex.
The medial branch of the SCA classically supplies the dentate nucleus which can also receive tributaries from the PICA; on the other hand, the PICA vascularises some other deep nuclei (globulus, emboliform, and fastigial) to which the SCA can also make contributions.
The lateral branch of the SCA vascularises the most lateral part of the superior cerebellar cortex (quadrangular, simple, and semilunar lobules) in balance with the AICA and the PICA.
Each half of the inferior part of the vermis is supplied by its homolateral PICA but the whole of the vermis can be supplied by one PICA if the contralateral PICA is an AICA-PICA.
Cerebellar veins have huge anastomosis on the cerebellar surface with possibilities for example of inferior vermian veins draining superiorly towards the trans tentorial sinuses and the tent with the superior vermian and hemispheric veins or inferior hemispheric cerebellar veins draining laterally and anteriorly towards the superior petrosal vein. From a surgical point of view, a good knowledge of veins is also absolutely necessary for the posterior fossa approach, firstly, to avoid a massive hemorrhage by a lesion of the bridging veins draining notably the superior hemispheric and superior vermian veins which can be torn off during a supracerebellar approach, as well as the transtentorial sinuses in a transtentorial approach.
For the supracerebellar approach, the superior hemispheric and vermian veins must be coagulated along the tent to protect the venous anastomosis on the cerebellar surface and avoid a venous infarct.
During pontocerebellar angle surgery, it’s better to protect the petrosal vein which obviously drains the brainstem and the cerebellum but also the supratentorial brain via the lateromesencephalic vein when the last part of the basal vein of Rosenthal is missing.
Conclusion
If the arterial vascularization of the cerebellum is usually well known by neurosurgeons, the main arterial variations and the whole venous vascularization are probably insufficiently recognized. Nevertheless, these notions are essential for operating in this area and notably in case of cisternal and ventricular surgery, where the main arterial trunks and bridging veins are localized.
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Delion, M., Dinomais, M. & Mercier, P. Arteries and Veins of the Cerebellum. Cerebellum 16, 880–912 (2017). https://doi.org/10.1007/s12311-016-0828-3
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DOI: https://doi.org/10.1007/s12311-016-0828-3