Functional Cerebral Venous Anatomy: A Perspective on Venous Collaterals Part II, Infratentorial Venous System

Authors: Takahiro Ota

Abstract

The infratentorial veins are densely packed in a smaller space compared to the supratentorial veins and have many variations, such as disconnections and anastomoses. Knowledge of the functional venous anatomy of the posterior fossa is becoming increasingly important in neurointerventional procedures. The basic brainstem veins are longitudinal and transverse veins. The venous drainage of the brainstem and cerebellum follows 3 superior (Galenic), anterior (petrosal), and posterior (torcular). Knowledge of the basic venous anatomy of the brainstem and cerebellum is essential for understanding the routes and patterns of venous drainage under pathological conditions, particularly in arteriovenous shunts. This review describes posterior fossa venous development and the functional venous anatomy of the posterior fossa, mainly the veins of the brainstem, cerebellum, and the emissary veins.

There are 3 routes for draining the brainstem and cerebellum. ^1^ , ^2^ , ^3^ Anterior drainage (superior petrosal drainage) drains the archicerebellum, which is the basic drainage of the cerebellum through the embryological ventral metencephalic vein (trigeminal vein). Superior drainage (Galenic drainage) drains the paleocerebellum, and posterior drainage (torcular drainage) drains the neocerebellum. There are abundant transverse (transverse pontine veins) and longitudinal (anterior pontomesencephalic, anterior medullary, and anastomotic lateral mesencephalic veins) anastomoses between the 3 drainage routes, superficially. Similar to the cerebrum, the cerebellum contains superficial and deep venous systems. Venous drainage from the cerebellar hemisphere and the vermis is superficial. ^4^ The subependymal veins around the fourth ventricle drain to the precentral cerebellar vein and the vein of the lateral recess of the fourth ventricle, both of which also receive superficial cerebellar veins. The subependymal veins below the floor of the fourth ventricle drain anteriorly through the anterior and lateral transpontine veins (Figure 1).

This review describes posterior fossa venous development and the functional venous anatomy of the posterior fossa, mainly the veins of the brainstem, cerebellum, and emissary veins. This review is based on the reports of great predecessors who have knowledge and insight into the development of cerebral veins, starting with Padget ^5^ and followed by Okudera et al ^6^ , ^7^ , Huang et al, ^3^ , ^8^ Lasjaunias et al, ^9^ and others. ^1^ , ^10^ In addition, there is a detailed examination by Rhoton ^2^ from a microsurgical perspective. It is helpful to understand the pathophysiology by considering the venous system as 1 system and examining the hemodynamic balance and dominance within it.

Posterior Fossa Venous Development

During embryonic development, the first vein to appear in the posterior fossa is the primitive ventral metencephalic vein, which is the first vein to connect with the alar plate of the metencephalon (which will develop into the future cerebellum). ^11^ This vein drains the anterior aspect of the brainstem and cerebellum.

In the hindbrain, numerous primary transverse pial‐arachnoid veins are first identified on the dorsolateral surface of the neural tube, which connects to the dural plexus and is reduced to 3 trigeminal, vagal, and hypoglossal. The ventral myeloencephalic (vagal) vein of the human embryo anastomoses caudally with the spinal vein and cranially with the ventral metencephalic (trigeminal) vein. Subsequently, secondary ventral longitudinal anastomoses (forming the anterior pontomesencephalic and anterior medullary veins [AMVs]) develop parallel to the basilar artery between these primary transverse veins. Later, the pial tributaries of these transverse veins are joined by secondary longitudinal anastomoses, and these, in turn, are irregularly connected in a similar fashion across the midline. ^5^ , ^11^ The late developmental pattern and timing of this longitudinal venous system explain the tendency of ventral longitudinal veins to have variations, such as duplication and disconnection.

The ventral metencephalic vein eventually becomes the petrosal vein. The proximal end of the ventral metencephalic vein becomes incorporated into the petrous crest to form the superior petrosal sinus. Petrosal drainage plays an important role in draining the lateral pons, cerebellar primordium, and the lateral aspect of the expanded choroid plexus of the fourth ventricle. The inferior petrosal sinus (IPS) is derived from the proximal end of the ventral myelencephalic vein.

With the development of the cerebellar hemispheres, the veins of the posterior group, derived from the dorsal metencephalic veins, become prominent and receive the superior and inferior tributaries. The veins of the posterior group drain into the straight sinus either directly or indirectly through the tentorial venous plexuses. ^3^

Veins on the Brainstem

The veins on the surface of the brainstem are divided into longitudinal and transverse veins based on their direction of flow. The longitudinal vein is continuous with the basal vein of Rosenthal (BVR) cranially and caudally to the spinal vein. The transverse vein connects to the longitudinal veins laterally. Many veins on the surface of the brainstem drain into the petrosal vein; however, bridging veins (emissary veins) to the posterior part of the cavernous sinus, IPS, sigmoid sinus, and marginal sinus have also been identified (Figures 2, 3).

Longitudinal Veins

Longitudinal veins can be divided into ventral midline, ventral anterolateral, lateral, and dorsal veins. Many of these veins are interconnected via the transverse veins.

Ventral Midline

The anterior pontomesencephalic vein (APMV) and the AMV are longitudinal venous channels running along the anterior surface of the brainstem. The APMV is connected to the basal vein via the peduncular vein superiorly and is often continuous with the AMV, inferiorly. ^9^ The APMV eventually drains laterally into the petrosal vein and superior petrosal sinus. Disconnection is often observed in the pontine segment of the APMV, which is connected to the craniocaudal side via the lateral APMV and transpontine veins. Transverse anastomoses, such as the transverse pontine and bridging veins, communicate with the cavernous, superior petrosal, and suboccipital cavernous sinuses. There are many variations in their anastomoses. ^12^ The AMV usually runs in the midline along the anterior surfaces of the pons and medulla and connects to the APMV and vein of the pontomedullary sulcus cranially and the anterior spinal vein inferiorly. This longitudinal venous channel communicates with the adjacent dural sinuses via the transverse pontine and/or the bridging veins. ^13^

Therefore, several variations in the APMV–AMV system can occur depending on the degree of regression and development of the primary transverse and secondary longitudinal veins.

In cases of dural arteriovenous fistulas potentially draining via the APMV–AMV system, the development of the APMV–AMV system and its bridging veins may be related to symptoms. ^12^

Ventral Anterolateral

The lateral APMV extends from the anterior surface of the cerebral peduncle to the anterolateral surface of the ventral pontine. This is complementary to the APMV. It either joins the APMV medially or connects to the transverse pontine vein and flows into the petrosal vein. Preolivary vein (lateral AMV) runs along the anterolateral (preolivary) sulcus between the medulla oblongata and olive above and joins the vein of the anterior medullary sulcus, cranially to the vein of the pontomedullary sulcus. It has numerous connections with AMVs and retro‐olivary veins via the transmedullary veins.

Lateral

Any vein running in or adjacent to the lateral mesencephalic sulcus may generically be called the lateral mesencephalic vein. ^3^ The lateral pontomesencephalic vein (lateral mesencephalic vein) belongs to the Galenic draining group; it courses vertically on the lateral aspect of the cerebral peduncle and drains either superiorly or inferiorly, superiorly to the third segment of the BVR or inferiorly into the brachial tributary of the petrosal vein. The lateral pontomesencephalic vein frequently connects the supratentorial BVR to the petrosal vein of the infratentorial venous system, representing an important anastomotic pathway for venous drainage between the supratentorial and infratentorial compartments.

The lateral mesencephalic vein is the most important venous outlet of the BVR and may provide an important salvage outlet for venous drainage toward the BVR and superior petrosal sinus in cases of compromised deep venous systems.

Lateral pontine vein (vein of the middle cerebellar peduncle) belongs to the petrosal draining group and runs along the lateral pontine sulcus. It receives tributaries from the venous outflow of the middle cerebellar peduncle and caudally, from the lateral medullary vein or the retro‐olivary vein, and joins the petrosal vein cranially. Caudally it merges with the vein of the pontomedullary sulcus.

Retro‐olivary vein is a vein that runs along the retro‐olivary sulcus, located behind the olive nucleus. It flows cranially into the lateral pontine vein either directly or via the vein of the pontomedullary sulcus. In the anteroposterior view of the angiogram, the retro‐olivary vein is located at the outer edge of the medulla oblongata. Multiple anastomoses are noted between the retro‐ and preolivary veins and between the preolivary and median AMVs.

The lateral medullary vein (vein of the restiform eminence) runs parallel to the retro‐olivary vein along the posterolateral sulcus. It flows cranially into the lateral pontine vein either directly or via the vein of the pontomedullary sulcus. It communicates with the retro‐olivary vein anteriorly via the transverse medullary vein and with the vein of the inferior cerebellar peduncle posteriorly. A bridging vein from the lateral medullary vein to the venous sinuses (inferior petrosal, sigmoid, and marginal sinuses) around the jugular foramen may also be present. In some cases, it forms a common trunk with the pre‐ and retro‐olivary veins and flows into the lateral pontine vein. If the common trunk runs along the vagal nerve toward the venous sinuses around the jugular foramen, it is called the inferior petrosal vein (vagal vein).

The vein of the pontomedullary sulcus, the pre‐and retro‐olivary veins, and the lateral medullary vein often unite to form a single trunk that flows into the lateral pontine vein along with the vein of the lateral recess of the fourth ventricle.

Dorsal

The median superior collicular vein from the superior colliculus, the median inferior collicular vein from the inferior colliculus, and the intercollicular vein running between the superior and inferior colliculi unite to form the quadrigeminal vein. The quadrigeminal vein runs backward and upwards to join the precentral cerebellar vein near its junction with the greater cerebral vein. The collicular vein sometimes joins with the lateral pontomesencephalic and pineal veins.

Transverse Veins

Peduncular vein (interpeduncular vein) runs along the anterior aspect of the cerebral peduncle and receives venous drainage from the veins of the hypothalamus, inferior thalamic vein, and veins from the midbrain. It communicates medially with the posterior communicating vein and the median APMV, and laterally with the second segment of the BVR. Bridging veins ventral to the posterior portion of the cavernous sinus and the transitional portion of the IPS may be observed.

Posterior communicating vein runs transversely in the interpeduncle cistern and connects with the right and left peduncular veins and the median APMV.

Vein of the pontomesencephalic sulcus runs along the pontomesencephalic sulcus. It rarely runs through the entire length of the sulcus and often connects the median and lateral APMVs transversely. It may be connected to the lateral pontomesencephalic vein also.

Transverse pontine veins collect blood from a network of small veins ventral to the pons. They then drain laterally into the petrosal veins, establishing connections between the median and lateral APMVs, as well as the petrosal and lateral pontomesencephalic veins. There are 2 or 3 transverse pontine veins (superior, middle, and inferior transverse pontine veins) on the anterior aspect of the pons. The middle transverse pontine vein at the level of the midpons is the most prominent and joins the median APMV to the petrosal vein. The transverse pontine vein in the anteroposterior view of the angiogram shows lateral morphology of the pons.

Vein of the pontomedullary sulcus runs along the pontomedullary sulcus, which is the transitional area located ventral to the pons and medulla oblongata. It communicates with the longitudinal veins of the pons and medulla oblongata.

Transverse medullary vein is a vein that traverses the ventral and lateral surfaces of the medulla oblongata. However, it rarely extends far enough to establish a connection between the median AMV and the lateral medullary vein. It is often found only on the surface of the pyramid or olive, with 1 or 2 of each. Numerous transverse connections have been identified between the various longitudinally running medullary veins.

Bridging veins may be observed extending from the transverse pontine vein ventrally toward the posterior cavernous sinus and the transition zone of the IPS and from the vein of the pontomedullary sulcus and transverse medullary vein ventrally to the sigmoid sinus and marginal sinus.

Cerebellar Veins

The veins on the surface of the cerebellum have a slightly complex course; however, they are composed of longitudinal veins that run vertically to the cerebellar sulci and transverse veins that run parallel to the cerebellar sulci, similar to the veins on the surface of the brainstem. ^2^ , ^3^ , ^9^ , ^14^ There are various classifications of cerebellar veins, and if they are divided into the superficial and deep venous systems, the precentral cerebellar vein and vein of the lateral recess of the fourth ventricle belong to the deep venous system, and the rest belong to the superficial venous system (Figure 1). However, from a developmental perspective, it is easier to understand their normal anatomy by classifying them according to their drainage sites. These are divided into 3 groups. (1) the superior group, which drains the cerebellar upper surface (cranial side of the primary fissure) facing the cerebellar tentorium; (2) the inferior group, which drains the cerebellar lower surface (caudal side of the primary fissure) facing the vault of the posterior cranial fossa; and (3) the anterior group, which drains the cerebellar anterior surface facing the posterior surface of the pyramidal bone. If we look at the relationship between the classification by drainage site and outflow route, the superior group forms the Galenic draining group for those in the front and the tentorial draining groups for those in the back and side. The inferior group forms the tentorial draining group, and the anterior group the petrosal draining group (Figures 4, 5).

Superior Group

Precentral Cerebellar Vein (Vein of the Cerebellomesencephalic Fissure)

The precentral cerebellar vein is a single midline vessel that typically enters the vein of Galen. The brachial tributary of the precentral cerebellar vein (the vein of the superior cerebellar peduncle) runs medially across the superior cerebellar peduncle from the deep lateral portion of the precentral cerebellar fissure toward the posterior superior cerebellar peduncle. It joins with its counterpart from the opposite side at the center of the fissure to form the precentral cerebellar vein. The brachial tributary of the precentral cerebellar vein communicates with the brachial tributaries of the petrosal vein (pontotrigeminal vein), which drains the upper part of the middle cerebellar peduncle. The colliculocentral point and the brachial and parenchymal tributaries of the precentral cerebellar vein indirectly mark the position of the roof of the upper part of the fourth ventricle. The superior cerebellar vein receives blood from the precentral cerebellum and the superior vermian veins.

Superior vermian vein (Galenic draining group) is a single large trunk formed by several small tributaries that drain the superior aspect of the superior vermis and the adjacent part of the cerebellar hemisphere. The superior vermian vein originates from the superior hemispheric vein and runs upward and forward along the superior aspect of the cerebellar hemisphere. The precentral cerebellar and superior vermian veins define the superior border of the superior vermis on the lateral angiogram.

Multiple superior hemispheric veins run posteriorly and inferiorly on the superior surface of the cerebellar hemispheres and open to the torcular Herophili and transverse sinus, either directly or via the tentorial sinus. The superior hemispheric veins may also converge into the tentorial sinus after merging with the inferior hemispheric veins that have reached the superior cerebellar surface.

The superior hemispheric tributaries of the precentral cerebellar vein, superior vermian vein, vein of the great horizontal fissure, and the superior hemispheric veins are interconnected.

Inferior Group

The posterior lobe of the cerebellar vermis and the surrounding cerebellar hemispheres are drained by the left and right inferior vermian veins.

Inferior vermian vein is the most important vein in this group. It is formed by the union of the superior and inferior retrotonsillary tributaries and enters the straight or transverse sinuses, sometimes after a short course within the tentorium. It has a median paramedian location in the anteroposterior view on the angiogram.

Inferior hemispheric veins are the inferior veins of the cerebellar hemispheres. Most of them run posteriorly upward and enter the transverse sinus either directly or via the tentorial sinus. However, some of them reach the superior surface of the cerebellum, join the superior hemispheric vein, and then drain into the tentorial sinus. Laterally, they may flow into the superior petrosal sinus via the tentorial sinus and may also connect with the inferior hemispheric tributary of the vein of the great horizontal fissure.

Anterior Group

This group consists of several tributaries that converge to a single trunk represented by the petrosal vein, which is a large but very short venous channel that enters the superior petrosal sinus. Petrosal vein is formed by the remnants of the metencephalic vein and receives numerous tributaries from the anterior aspect of the cerebellum and brainstem before draining into the superior petrosal sinus. The petrosal vein is often well identified, especially in the anterolateral view of the angiogram. It is an important vein in the venous outflow route in the same area, as observed in cases of dural arteriovenous malformation.

The vein of the great horizontal fissure, comprising the anterior hemispheric vein and the vein of the cerebellopontine fissure courses anteromedially through the anterior half of the great horizontal fissure situated between the superior and inferior surfaces of the cerebellar hemispheres. It ultimately drains into the petrosal vein after receiving the superior and inferior hemispheric tributaries along its course. Some of the hemispheric tributaries around the great horizontal fissure do not directly join the vein of the great horizontal fissure. Instead, they independently drain into various vessels, including the anterior lateral marginal vein, superior petrosal sinus, IPS, transverse sinus, and sigmoid sinus rather than into the vein of the great horizontal fissure.

Brachial vein (brachial tributary of the petrosal vein and pontotrigeminal vein) refers to the veins that drain the periphery of the lateral precentral cerebellar fissure, specifically the region above the superior and middle cerebellar peduncles. Among the brachial veins, those that course in a lateral downward direction from the upper to the anterior surface of the middle cerebellar peduncle and subsequently join the petrosal vein are called the brachial tributaries of the petrosal vein. These veins belong to the petrosal‐draining group. Conversely, the brachial tributaries of the precentral cerebellar veins are those that traverse the superior cerebellar peduncle proceeding inward and backward to converge with the precentral cerebellar fissure, where they unite with their counterpart on the opposite side, to form the precentral cerebellar vein. Therefore, the brachial veins communicate between the petrosal and Galenic draining groups. In addition, the brachial tributary of the petrosal vein communicates with the lateral pontomesencephalic vein at the level of the lateral mesencephalic sulcus.

Vein of the lateral recess of the fourth ventricle (vein of the posterolateral fissure and vein of the cerebellomedullary fissure) collects veins from the subependymal region of the fourth ventricle. It originates at the upper pole of the cerebellar tonsil, where the transverse and lateral supratonsillar veins join. From there it courses forward along the cerebellomedullary fissure, and drains into the petrosal vein or directly into the superior petrosal sinus or IPS. It is sometimes called the vein of the cerebellomedullary fissure because it does not traverse the lateral recess of the cerebellum.

Thus, the veins of the great horizontal fissure, transverse pontine vein, brachial vein, vein of the lateral recess of the fourth ventricle, and lateral pontine vein usually converge toward the anterior angle of the cerebellum, where they form a single stem, the petrosal vein. ^3^

Emissary Vein

Emissary veins serve as connections between the intracranial and extracranial venous systems. They are characteristically thin walled with a valveless structure. In the posterior fossa, several emissary veins connect the dural sinuses and extracranial veins. During the early stages of development, these emissary veins carry venous return from the extracranial tissues to the primitive venous sinuses. ^7^ , ^15^ , ^16^ As the chondrocranium forms at their base, the emissary veins pass through the emissary foramina and subsequently reverse their blood flow direction, to flow from the intracranial toward the extracranial. Drainage of the dural sinuses of the posterior fossa into the extracranial venous system may occur through the mastoid, anterior and posterior condyloids, and occipital emissary veins. The hypoglossal emissary vein drains into the ventral myeloencephalic vein from the upper cervical spinal cord. The posterior condylar emissary vein originates from the tail of the superior jugular bulb or the sigmoid sinus and communicates with the suboccipital venous plexus through the condylar canal. The anterior condylar vein communicates with the marginal sinus and anterior condylar confluence or internal jugular vein via the hypoglossal canal. The mastoid emissary vein communicates with the sigmoid sinus, posterior auricular vein, and occipital vein through the mastoid foramen. The hypoglossal, condylar, and mastoid emissary veins play a crucial role as collateral pathways connecting intracranial veins with veins around the vertebral body. The IPS at its distal end also functions as an emissary vein, connecting the cavernous sinus with the jugular vein. ^9^ The tail of the IPS originates from the ventral myelencephalic vein and passes through the pars nervosa of the jugular foramen to reach the anterior condylar confluence or directly communicates with the internal jugular vein.

The petrosquamous sinus originates from the dorsolateral side of the transverse sinus and runs along the boundary between the squamous and petromastoid parts of the temporal bone before flowing into the retromandibular vein via the postglenoid foramen. ^17^ A venous channel that passes through the petrous apex communicates with both the IPS and inferior petro‐occipital vein.

Emissary veins are sometimes used as an abnormal route for venous outflow, in addition to their normal function as collateral pathways that connect intracranial and extracranial veins. ^18^ Emissary veins or their surroundings may also be associated with dural arteriovenous fistulas in areas lacking dural venous sinus. Dural arteriovenous fistulas in the region of the hypoglossal canal are likewise related to the emissary veins in the region of hypoglossal canal. These diseases can be viewed from a similar perspectives. ^19^

Conclusion

The infratentorial veins are classified into 3 groups according to their drainage superior (Galenic), anterior (petrosal), and posterior (tentorial). The area of their tributaries for each route are neither strictly defined nor mutually connected. Between the Galenic and petrosal draining groups, the brachial vein and superior hemispheric tributary play a role in the connection, and between the petrosal and tentorial draining groups, the superior and inferior hemispheric tributaries and the supratonsillar tributaries serve the same purpose. Between the Galenic and tentorial draining groups, the superior hemispheric tributary, supraculminate vein, and declival vein also contribute. Although there are many variations in the running course and connecting pattern of the infratentorial veins, understanding the basic pattern of infratentorial venous angioarchitecture can be beneficial for neurointerventionalists when interpreting 3‐dimensional angiography or cone‐beam computed tomography.

Sources of Funding

No specific grant from funding agencies in the public, commercial, or not‐for‐profit sectors was received.

Disclosures

None.