Abstract
The development of neuroimaging has allowed clinicians to improve clinicoanatomic correlations in patients with strokes.Brainstem and cerebellum structures are well delineated on MRI, but there is a lack of standardization in their arterial supply. We present a system of 12 brainstem and cerebellum axial sections, depicting the dominant arterial territories and the most important anatomic structures. These sections may be used as a practical tool to determine arterial territories on MRI, and may help establish consistent clinicoanatomic correlations in patients with brainstem and cerebellar ischemic strokes.
NEUROLOGY 1996;47: 1125-1135
The advent of neuroimaging has allowed clinicians to make precise clinicoanatomic correlations before death of the patient. A knowledge of arterial territories is needed to achieve accurate localization of ischemic lesions on CT and MRI. A few studies have provided schematic drawings of the distribution of arterial territories of the brainstem and cerebellum. [1-4] Some of them were purely radiologic; [4] others were pathologic. [1] This report is designed to present arterial territories in a form directly applicable to CT or MRI slices in clinical practice. Its aim is to help establish reproducible clinicoanatomic correlations in patients with brainstem and cerebellar strokes. Subsequent reports will focus on arterial territories of the hemispheres and arterial border zones.
Our report displays the arterial supply and the most important anatomic structures of the human brainstem and cerebellum. The arterial territories have been drawn using (1) the map of brainstem territories from the anatomic studies of Duvernoy, [5,6] which divide supply into anteromedial, anterolateral, lateral, and posterior arterial groups; and (2) the pathologic studies by Amarenco et al. [1,7-10] and the injection studies of Marinkovic et al. [11] of the supply from the three main cerebellar arteries. The organization of the arterial supply is shown on anterior, posterior, and lateral views of brainstem and cerebellum in Figure 1, Figure 2, Figure 3, Figure 4.
Figure 1. Anterior view showing the general arrangement of the brainstem and cerebellar arteries (Modified from Duvernoy [6]). A = medulla; B = pons; C = midbrain; D = cerebellum. Main arterial trunks: 1 = vertebral artery; 2 = anterior spinal artery; 3 = posterior inferior cerebellar artery; 4 = basilar artery; 5 = anterior inferior cerebellar artery; 6 = superior cerebellar artery; 7 = posterior cerebral artery; 8 = collicular artery; 9 = posteromedial choroidal artery; 10 = anterior choroidal artery. Arteries of the anterior and lateral aspects of the brainstem: 11 = anteromedial group of medullary arteries; 12 = anterolateral group of medullary arteries; 13 = lateral group of medullar arteries (arteries of the lateral medullary fossa), a = inferior rami, b = middle rami, c = superior rami; 14 = anteromedial group of pontine arteries, penetrating the basilar sulcus (14), penetrating the interpeduncular fossa (14 prime) (inferior rami of the interpeduncular fossa), penetrating the foramen cecum (14 double prime); 15 = anterolateral group of pontine arteries; 16 = lateral group of pontine arteries originating from the superior lateral pontine (16 prime) and the inferior lateral pontine (16 double prime) arteries and from the anterior inferior cerebellar artery; 17 = anteromedial group of mesencephalic arteries (middle rami of the interpeduncular fossa); 18 = thalamoperforating arteries (superior rami of the interpeduncular fossa); 19 = anterolateral group of midbrain arteries. Arteries of the anterior aspect of the cerebellum: 20 = branches of the superior cerebellar artery; 21 = branches of the anterior inferior cerebellar artery; 22 = branches of the posterior inferior cerebellar artery.
Figure 2. Posterior view of medulla and pons after removal of the cerebellum by sections of the cerebellar peduncle. A = posterior aspect of the lower medulla; A prime = posterior aspect of the upper medulla; B = posterior aspect of the pons (superior cerebellar peduncle); C = inferior colliculus; 1 = posterior inferior cerebellar artery; 2 = posterior spinal artery; 3 = posterior group of medullary arteries supplying the lower medulla; 4 = posterior group of medullary arteries supplying the upper medulla; 5 = superior cerebellar artery, lateral branch; 6 = superior cerebellar artery, medial branch; 7 = posterior group of pontine arteries (arteries of the superior cerebellar peduncle).
Figure 3. Right lateral view of the midbrain showing the general arrangement of the midbrain arteries (Modified from Duvernoy [6]). A = interpeduncular fossa; B = mamillary body; C = cerebral peduncle; D = lateral surface of the midbrain; E = superior colliculus; F = inferior colliculus; G = superior cerebellar peduncle; 1 = basilar artery; 2 = superior cerebellar artery, 2 prime = medial branch, 2 double prime = lateral branch; 3 = posterior cerebral artery; 4 = collicular artery; 5 = posteromedial choroidal artery; 6 = anterior choroidal artery; 7 = anteromedial group of midbrain arteries (middle group of interpeduncular arteries); 8 = anterolateral group of midbrain arteries; 9 = lateral group of midbrain arteries; 10 = posterior group of midbrain arteries; 11 = posterior group of pontine arteries (arteries of the posterior cerebellar peduncle).
Figure 4. Sagittal section of the pons showing the paths of different pontine arteries. A = pontine ventral (basilar) part; B = pontine tegmentum; 1 = basilar artery; 2 = the lower part of the pontine tegmentum, vascularized by ascending arteries; 3 = the middle part of the pontine tegmentum, vascularized by arteries with a straight path; 4 = the upper part of the pontine tegmentum, vascularized by descending arteries.
We developed 12 serial sections (4 mm thick) based on a bicommissural plane passing through the center of the anterior and posterior commissures (sections I to XII). These sections are modified views from previous work by Duvernoy. [6] The right side of the sections shows the anatomic structures mentioned in Table 1. The arterial territories appear in the left side of the sections.
Table 1. Anatomic structures of sections I to XII
Arterial supply of brainstem and cerebellum.
Brainstem.
Main arterial trunks supplying the brainstem include the vertebral artery, anterior spinal artery, posterior inferior cerebellar artery, basilar artery, anterior inferior cerebellar artery, superior cerebellar artery, posterior cerebral artery, posterior communicating artery, and anterior choroidal artery. The collaterals of these arteries are divided into four arterial groups (anteromedial, anterolateral, lateral, and posterior), which supply the brainstem structures. [5] At each level of the brainstem, the origin of arterial supply varies.
1. Arterial groups to the medulla.
(1) Anteromedial and anterolateral groups arising from the vertebral and anterior spinal arteries. (2) Lateral group (rami of the lateral medullary fossa) arising from the posterior inferior cerebellar artery (inferior rami), the vertebral artery (middle rami), the basilar artery, and anterior inferior cerebellar artery (superior rami). (3) Posterior group arising from the posterior inferior cerebellar artery for the upper part of the posterior aspect of the medulla, and from the posterior spinal artery for the lower part.
2. Arterial groups to the pons.
(1) Anteromedial and anterolateral groups arising from the basilar artery, entering the foramen cecum, the basilar sulcus, and the interpeduncular fossa. (2) Lateral group arising from the anterior inferior cerebellar artery (entering the parenchyma in the pontomedullary sulcus) and arising from the lateral pontine arteries (entering the brachium pontis). (3) Posterior group arising from the superior cerebellar artery (medial and lateral branches). Probably due to the large development of the ventral part of the pons in humans, the arterial supply of the pontine tegmentum can be divided into three levels (see Figure 4). At the lowest tegmental level the artery entering the foramen cecum and the pontomedullary sulcus (superior rami of the lateral medullary fossa) supplies the tegmentum along its ascending path. At the middle tegmental level the arteries reach the tegmentum by a direct and straight path. At the upper tegmental level, the arteries entering the interpeduncular fossa (inferior rami) reach the tegmentum through a descending path.
3. Arterial groups to the midbrain.
Five arterial trunks supply the arterial midbrain groups, from below to above, the superior cerebellar artery (mainly the medial branch), the collicular artery, the posteromedial choroidal artery, the posterior cerebral artery, and the anterior choroidal artery (see Figure 3). Due to their anatomic relationship with the anterior, lateral, and posterior aspects of the midbrain, these arterial trunks have specific involvement in the anteromedial, anterolateral, lateral, and posterior groups of midbrain arteries. The posterior cerebral artery provides the only supply to the anteromedial group (middle rami of the interpeduncular fossa). The collicular and posteromedial choroidal arteries are the main source of the anterolateral and lateral groups; the posterior group is supplied by the superior cerebellar, collicular, and posteromedial choroidal arteries. Note that the anterior choroidal and posterior cerebral arteries may participate in the upper anterolateral group.
Cerebellum.
The cerebellar arterial supply depends on three long arteries (see Figure 1). The posterior inferior cerebellar artery gives rise to two branches and vascularizes the inferior vermis and the inferior and posterior surfaces of the cerebellar hemispheres. The anterior inferior cerebellar artery supplies the anterior surface of the simple, superior, and inferior semilunar lobules as well as the flocculus and the middle cerebellar peduncle. The superior cerebellar artery divides into medial and lateral branches and vascularizes the superior half of the cerebellar hemisphere and vermis as well as the dentate nucleus. These three cerebellar arteries also take part in the vascularization of the brainstem (see above). The territory of the superior cerebellar artery often includes the upper part of the pontine tegmentum. The posterior inferior cerebellar artery takes part in the lateral and posterior arterial groups of the medulla. The anterior inferior cerebellar artery supplies the middle cerebellar peduncle and often the lower part of the pontine tegmentum.
Discussion.
The bicommissural plane used in this work passes through the center of the anterior and posterior commissures. This plane differs slightly from the bicommissural line of Talairach, [12] which is drawn through the superior edge of the anterior commissure and the inferior edge of the posterior commissure. According to Salamon et al., [13] the center-to-center bicommissural line is easier to find on MRI sagittal views than Talairach's line. Moreover, potential errors in determining the bicommissural plane, due to a variation in size of the anterior commissure, are reduced. [14] The neuro-orbital plane recommended by Cabanis et al. [15] could be specifically adapted to the sectional anatomy of the brainstem, but it is not routinely applicable to the rest of the brain. On CT, the external reference of the bicommissural plane used in our study is the suborbitomeatal line passing at the lower margin of the orbital opening and in the center of the external acoustic meatus, although the correlation between external cranial and intracerebral structures appears to be imprecise. [6]
Since pioneer works by Duret, [16] Stopford, [17,18] and Foix and Hillemand, [19] the arterial supply of brainstem and cerebellum has also been assessed using injection studies by Gillilan, [20,21] Khan, [22] or Stephens and Stilwell. [23] Numerous classifications of the brainstem arteries have been proposed. The classification we chose here is that of Lazorthes et al., [24] who divided the superficial arteries into anterior (paramedian for Foix and Hillemand), lateral (short circumferential for Foix and Hillemand) and posterior (long circumferential for Foix and Hillemand), according to their point of penetration into the parenchyma. For the arteries of the anterior group, we used the subdivision proposed by Duvernoy. [5,6] This classification divides anterior arteries into anteromedial and anterolateral groups. Each of the anteromedial, anterolateral, lateral, and posterior groups supplies corresponding territories in the brainstem. Arterial anastomoses always exist for the leptomeningeal (pial) segment of arteries, for example, in the cerebral peduncles and among the thalamoperforating arteries. [5,25] As for other parts of the brain in general, arterial anastomoses rarely occur in deep structures. Anastomoses of pial arteries are less frequent in the cerebellar cortex than in the cerebral cortex. [11,26] Figure 5
We must emphasize that the arterial groups have a variable extension at different levels of the brainstem. For example, the size of the posterior group is progressively reduced in the upper medulla, disappears in the lower pons, and reappears in the upper pons and midbrain. Consequently, the nuclei and tracts that extend into the brainstem may be supplied by several groups. For example, the nucleus of the solitary tract and spinal trigeminal nucleus and tract are supplied by the posterior group at their lower part and by the lateral group at their upper part. In the midbrain, the anteromedial (supplying the red nucleus, oculomotor nuclei, and fibers), anterolateral (supplying the crus cerebri and the substantia nigra, a part of the medial lemniscus), and posterior (supplying the colliculi and the periacqueductal gray matter) groups have large territories, but the lateral group has a more limited territory. Figure 6, Figure 7, Figure 8, Figure 9, Figure 10, Figure 11
The arterial territories represented in our sections are a model of dominant vascularization and cannot account for individual variations. For example, the anterior inferior cerebellar artery can usually replace a hypoplastic posterior inferior cerebellar artery, taking over most of the anterior and inferior part of the cerebellar hemisphere. There are also many individual variations in the relative importance of cerebellar arteries in the vascularization of the brainstem. Some variations are less frequent, such as cerebellar arteries originating from the internal carotid artery. [27] Figure 12, Figure 13, Figure 14
MRI studies have reevaluated the clinical spectrum of posterior circulation stroke. [28] Because the topographic, etiologic, and clinical spectrums vary, large prospective studies, including well documented patients, are of utmost importance. [29,30] Classical syndromes have been revisited and new clinical patterns highlighted, for example, in lower brainstem or mid brain infarcts. [31,32] However, most recent studies are based on various anatomic support and sometimes even lack anatomic reference. In the latter case, MRI is even considered to be an effective means of identifying etiologies according to the location of the infarction. [33,34] In addition, several clinicotopographic MRI studies were based on previous mapping reports in which anatomic support was a compilation of data in the literature. [32,35,36] On the other hand, reports in which the arterial vascular territories are well identified by anatomic studies are scarce. [37] This lack of standardization in both arterial territory localization and the planes used to identify them mar the accuracy of such reports. Figure 15, Figure 16
Our vascular mapping, established for arterial dominant territories, evaluated in a standard plane, and based on anatomic studies, should be the first step toward the achievement of both accurate and reproducible clinicotopographic correlations. to 4.
Acknowledgments
We wish to thank Patrick M. Pullicino, Pierre Amarenco, and Louis R. Caplan for their helpful comments on the first version of this article. We are also indebted to J.L. Vannson, medical illustrator, for his kind assistance. The color publication of this article is possible through an educational grant from Sanofi-Winthrop.
- Copyright 1996 by Advanstar Communications Inc.
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