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Neuroradiology |
1 From the Depts of Neuroradiology (I.Y., T.A.Y.) and Neurology (M.D.), Klinikum Grosshadern, Munich, Germany; Dept of Anatomy, Ludwig-Maximilians Universität, Munich, Germany (B.M.); Neurosurgical Unit, Klinik Im Park, Zürich, Switzerland (U.D.S.); and Depts of Radiology and Neurosurgery, Mount Sinai School of Medicine, New York, NY (T.P.N.). Received Mar 15, 2001; revision requested May 3; revision received Aug 13; accepted Sep 9. Address correspondence to T.A.Y., Lysholm Department of Radiology, National Hospital of Neurology and Neurosurgery, Queen Square, London WC1N 3BG, England (e-mail: T.yousry@ion.ucl.ac.uk).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: In 30 subjects (60 nerves) and in one patient with right superior oblique myokymia (SOM), the anatomy of the trochlear nerve was depicted with three-dimensional (3D) Fourier transformation constructive interference in steady state (CISS) magnetic resonance (MR) imaging, whereas the adjacent vessels were detected with 3D time-of-flight (TOF) MR imaging before and after gadopentetate dimeglumine administration. The images were evaluated with respect to the identification of the trochlear nerve, the distance between the point of exit (PE) and the midline, the visualized length, the vascular relationships, and the distance between the PE and the point of neurovascular contact.
RESULTS: 3D CISS MR imaging depicted the proximal cisternal segment of the trochlear nerve in the transverse, sagittal, and coronal planes in 57 (95%), 51 (85%), and 48 (80%) of 60 nerves, respectively. The distance from the midline to the PE was 3–9 mm, and the maximum visualized length of the trochlear nerve was 1–14 mm. An arterial-trochlear neurovascular contact was seen at the root exit zone (REZ) in eight (14%) nerves and at a mean distance of 3.4 mm distal to the PE in 29 nerves (51%). The patient with SOM had arterial-trochlear neurovascular contact at the REZ.
CONCLUSION: Use of 3D CISS sequences and 3D TOF sequences with or without gadopentetate dimeglumine enables accurate identification of the proximal cisternal segment of the trochlear nerve and its neurovascular relationships.
© RSNA, 2002
Index terms: Brain, anatomy, 10.92, 146.92 • Brain, MR, 146.121411, 146.121412, 146.12142, 146.12143 • Nerves, cranial, 146.92 • Nerves, MR, 146.121411, 146.121412, 146.12142, 146.12143
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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3D CISS (12) is a high-spatial-resolution, refocused gradient-echo MR imaging sequence that is flow compensated (14). The 3D CISS sequence depicts small structures surrounded by cerebrospinal fluid with high contrast and high spatial resolution and is suitable for MR cisternography. Cranial nerves VI (10,15), VII, VIII (16–19), and XII (20) have been visualized successfully on MR images obtained by using the 3D CISS sequence. The anatomic course and neurovascular relationships of the thin abducent nerve are depicted reliably in the transverse, sagittal, and coronal planes with 3D CISS sequences in 94%–96% of cases (15). These high success rates led us to use the same sequence to study the anatomic course and neurovascular relationships of the trochlear nerve.
The specific aims of this study were (a) to assess the anatomic features of the proximal portion of the cisternal segment of the trochlear nerve from the root exit zone (REZ) of the point of exit (PE) of this nerve to the free edge of the tentorium and (b) to assess the vascular relationships of that portion of the trochlear nerve.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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MR Imaging Procedures
All MR imaging examinations were performed with a 1.5-T unit (Magnetom Vision; Siemens, Erlangen, Germany) by using a regular quadrature head coil. The following pulse sequences were used: (a) 3D CISS (12.25/5.90 [repetition time msec/echo time msec], 70° flip angle, 180 x 180-mm [read x phase encode] field of view, 70.0-mm slab thickness, 512 x 262 matrix, 106 3D partitions, one slab, 0.35 x 0.69-mm pixel size, 0.66-mm effective section thickness, one acquisition, imaging time of 11 minutes 4 seconds) and (b) 3D time of flight (TOF) before and 3 minutes after the administration of 0.1 mmol/kg of gadopentetate dimeglumine (31/7, 20° flip angle, 200-mm field of view, 50-mm slab thickness, 512 x 224 matrix, 50 3D partitions, one slab, 0.78 x 0.39-mm pixel size, 1-mm effective section thickness, one acquisition, imaging time of 5 minutes 49 seconds).
Image Analysis Procedures
The data set from each 3D CISS sequence was reconstructed in transverse, sagittal, and coronal planes with a section thickness of 0.66 mm. Image analysis was simplified with use of a multiplanar reconstruction program (Siemens) that correlated the position of any point selected in one plane with the position of that same point in the other two orthogonal planes. This program helped to assess nerve position and any neurovascular contact at each point along the cisternal course of the trochlear nerve. The images were analyzed by two observers (I.Y., T.A.Y.) collaboratively. To exclude the possibility of mistaking the trochlear nerve for a vessel, or vice versa, we compared the structures identified as the trochlear nerve on 3D CISS images with the corresponding structures on 3D TOF images obtained before and after administration of gadopentetate dimeglumine.
Anatomic course and identification of the trochlear nerve.—We analyzed each side of each subject to (a) identify the trochlear nerve in the transverse, sagittal, and coronal planes and confirm its identity as a nerve by means of comparison of the 3D CISS and 3D TOF images, (b) identify the PE of the trochlear nerve from the middle portion of the brain, (c) measure the distance from the PE to the frenulum of the anterior medullary velum, (d) measure the length of the proximal cisternal segment of the trochlear nerve (ie, the distance from the PE to the most distal visible point of the nerve before it becomes covered by the tentorium), and (e) assess the precise course of the proximal trochlear nerve through the cistern—that is, whether it first runs laterally in a coronal plane and then anteriorly in a sagittal plane or follows an oblique anterolateral course through both planes simultaneously.
The reliability of identifying the trochlear nerve was scored on an arbitrary scale of certainty: A score of 2 indicated a positive identification; a score of 1, a highly probable identification; and a score of 0, no identification (15).
Nerve-vessel contact.—Neurovascular contact was defined as the absence of any detectable cerebrospinal fluid layer between the trochlear nerve and an adjacent vessel (15). When the 3D CISS images showed a vessel either in direct contact with or in close relation to the trochlear nerve, we identified the vessel by tracing its branches backward to the proximal parent vessel and comparing the vessel with the corresponding structures depicted with the 3D TOF sequences. Vessels were identified as arteries if they were visualized on 3D TOF images and could be traced to the parent arteries. Vessels were defined as veins if they were hyperintense on contrast-enhanced 3D TOF images but not on unenhanced 3D TOF images and/or if they could be traced to a larger vein. The precise neurovascular relationship in the transverse plane was then recorded at two sites:
1. At the REZ: According to descriptions in the literature, we defined the REZ as the short segment of the trochlear nerve extending from the PE for up to 1.2 mm along the nerve. We determined whether a vessel was in direct contact with the trochlear nerve at the PE or within 1.2 mm of the PE, in which case we measured the distance between the PE and the vessel.
2. Along the cisternal segment of the trochlear nerve: Again, we determined whether a vessel was in direct contact with the trochlear nerve or in close proximity to it and determined the distance between the PE and the point of contact. In addition, we defined the location of the vessel with respect to the trochlear nerve as anterior (ie, superficial), posterior (ie, deep), or complex (ie, the relationship could not be clarified at the point of contact) (15).
Patient evaluation.—The same two observers collaboratively analyzed the images obtained in the patient by using the criteria just described. Specifically, they (a) identified the trochlear nerve in the transverse, sagittal, and coronal planes by using the system described earlier and confirmed its identity as a nerve by comparing structures on the 3D CISS and 3D TOF images; (b) identified the PE of the trochlear nerve from the middle portion of the brain; (c) measured the distance from the PE to the frenulum of the anterior medullary velum; (d) measured the length of the proximal cisternal segment of the trochlear nerve; (e) assessed the precise course of the proximal trochlear nerve through the cistern; (f) determined the neurovascular relationship at the REZ and at the cisternal segment of the trochlear nerve; (g) determined whether a vessel was in direct contact with or in close proximity to the trochlear nerve; and (h) determined the distance between the PE and the point of contact and scored the location of the vessel with respect to the trochlear nerve.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Trochlear Nerve Dimensions
The distance from the midline (anterior medullary velum) to the PE ranged from 3.0 to 9.0 mm (mean, 5.7 mm) (Table 2). The maximum length of the cisternal segment of the trochlear nerve that was visualized between the PE and the free edge of the tentorium ranged from 1.0 to 14.0 mm (mean, 7.5 mm).
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Arteries.—The main trunk or medial branch of the SCA was always identified. Because we could not determine the exact point of the bifurcation of the SCA into its medial and lateral (rostral or caudal [21]) branches, we could not differentiate between the main trunk and the medial branch of the SCA. Therefore, for simplicity, we used the term medial SCA branches to refer to the SCA main trunk or medial branch in the quadrigeminal plate cistern. A total of 59 medial SCA branches were observed to be in relation to 46 (81%) of the 57 nerves identified. In 17 nerves (30%), the arteries were in close relation to the trochlear nerve but not in direct contact with it; the mean distance from the PE was 2.5 mm (range, 1–7 mm). In two of these 17 nerves, two arteries were observed to be in close relation to each nerve. In 29 nerves (51%), medial SCA branches were in direct contact with the trochlear nerve (Figs 2, 3), at a mean distance of 3.4 mm from the PE (range, 1–11 mm). In four of these 29 nerves, multiple points of contact were observed: One nerve had four points of contact, one nerve had three points of contact, and two nerves had two points of contact each. In four additional nerves, two arteries that were in relation to each nerve were detected: One artery was in proximity to but not in direct contact with the trochlear nerve, and the second artery was in direct contact with the trochlear nerve. The medial SCA branches passed posteriorly (ie, deep) to the trochlear nerve in 26 (44%) of the 59 arteries and anteriorly (ie, superficial) to the trochlear nerve in 24 (41%) arteries (Figs 2, 3). In the remaining nine (15%) arteries, the relationship between the arteries and the nerves was complex (Table 3).
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The proximal cisternal segment of four trochlear nerves (7%) had no relation to or contact with an artery or vein. Three other nerves (5%) appeared to have a combination of arterial and venous relationships. One of these three nerves was in close proximity to two veins and in direct contact with one artery. Another nerve was in close proximity to one artery and in direct contact with one vein. The last nerve was in close proximity to one artery and one vein.
Neurovascular Relationships: REZ
Arterial nerve–vessel contacts were detected at the PE in two (4%) of 57 nerves. In six (11%) nerves, medial SCA branches were observed to be in direct contact with the trochlear nerve, at a distance of 1 mm from the PE. Therefore, the SCA branches were in direct contact with the REZ in a total of eight (14%) nerves. In four (7%) additional nerves, medial SCA branches were in relation to but not in direct contact with the nerve; the distance from the PE was 1 mm. Venous nerve–vessel contacts were detected at the PE in three (5%) nerves.
Patient Results
3D CISS MR imaging successfully depicted both the trochlear nerves in the patient with right superior oblique myokymia. The right trochlear nerve was identified (score, 1) in all three planes. The left trochlear nerve was identified with near certainty (score, 2) in the transverse and sagittal planes and identified with high certainty (score, 1) in the coronal plane. On both sides, the cisternal length of the trochlear nerve was 6 mm and the distance from the PE to the superior medullary velum was 5 mm. One medial SCA branch was in direct contact with the trochlear nerve at the PE on the right side (Fig 4). The relationship between the artery and the nerve was complex: It was impossible to identify these structures separately on the 3D CISS image. MR angiographic findings confirmed the presence of an artery at the PE of the trochlear nerve (Fig 4). The fact that the SCA branch and the REZ of the trochlear nerve were inseparable at the PE of the nerve is consistent with a vascular compression of the nerve. On the left side, no arterial or venous contact was depicted at the REZ, but a medial SCA branch was observed to have a complex relation to the trochlear nerve at a distance of 6 mm from the PE on the left side. The final clinical diagnosis was myokymia related to neurovascular compression.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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Trochlear Nerve Anatomy
The first aim of this study was to determine the MR imaging characteristics of the trochlear nerve and the reliability of detecting the nerve with MR imaging. The trochlear nerve can be divided into four segments: central, cisternal, cavernous, and orbital (22).
The central segment of the trochlear nerve extends from the nucleus to the PE of the nerve from the middle portion of the brain (22). The nucleus of the trochlear nerve is in the tegmentum of the middle portion of the brain at the level of the inferior colliculus. Axons leaving the nucleus form a fascicle that courses posteroinferiorly around the aqueduct to decussate within the superior medullary velum (2,23). The trochlear nerve then emerges laterally to the frenulum of the superior medullary velum, beneath the inferior colliculus on the side contralateral to its nucleus of origin (1,2,23,24). The PE is 0.7 mm (range, 0–1 mm) inferior to the lower border of the inferior colliculus and 4.0 mm (range, 3.0–5.5 mm) lateral to the midline (25). At the PE, a variable number of rootlets, usually two (26), unite to form the nerve trunk (3,26).
The cisternal segment of the trochlear nerve extends from the level of the inferior colliculus to the rostrolateral free edge of the tentorium (27). The short initial portion of the cisternal segment is in the quadrigeminal plate cistern. The longer distal portion runs through the caudal portion of the ambient cistern (27). The cisternal segment of the trochlear nerve parallels the courses of the SCA, the posterior cerebral artery, and the basal vein of Rosenthal (2), and it passes between the posterior cerebral artery and the SCA (4). Within the quadrigeminal plate cistern, twigs from the medial branch of the SCA usually surround the nerve. The cisternal segment terminates at the level of the rostrolateral margin of the tentorium (27), where it pierces the dura (28).
The cavernous segment of the trochlear nerve then continues forward through the upper portion of the lateral wall of the cavernous sinus toward the orbit (1).
The orbital segment of the trochlear nerve traverses the superior orbital fissure to supply the superior oblique muscle. The course of the nerve remains external to the tendinous attachments of the extraocular muscles (23,28).
Imaging.—Imaging the cisternal segment of the trochlear nerve may be difficult because of the small diameter of this nerve and the nerve’s proximity to vessels with a similar course and caliber. To our knowledge, only five previously published reports have addressed the MR imaging depiction of the trochlear nerve. Caillet et al (7), by using a T1-weighted SE sequence with 3–5-mm thick sections, identified the trochlear nerve in the transverse and sagittal planes in 30% of cases and identified the nerve in the coronal plane occasionally. Hosoya et al (8) visualized the trochlear nerve in 10% of cases by using a contrast-enhanced 3D spoiled gradient-recalled-echo sequence. Casselman and Dehaene (11) first used the 3D CISS sequence with a section thickness of 0.7 mm to image the cisternal portion of the trochlear nerve. They did not analyze the reliability in detecting the nerve. Yousry et al (12) found the 3D CISS sequence to be superior to the T2-weighted fast spin-echo sequence for identifying the cisternal components of the cranial nerves and detected the trochlear nerve in 47.5% of cases. Results of the study conducted by Held et al (10) confirmed the superiority of the 3D CISS MR imaging sequence over T2-weighted fast spin-echo and magnetization-prepared gradient-echo sequences. By using the 3D CISS sequence, they identified the trochlear nerve "at the inferior colliculus" in 93.4% of cases and in its "circumpeduncular course" in 100% of cases (10).
A major problem in identifying the trochlear nerve is that of distinguishing the nerve from the multiple arteries and veins that surround it. This difficulty seems to be the cause of the lower detection rate achieved previously (12). A high detection rate does not prove the reliability of a technique, however. A high detection rate can also result from mistaking vessels for nerves. To prevent such misinterpretations, a technique that enables one to reliably distinguish vessels from nerves must be applied. TOF MR imaging, which yields high signal intensity of arteries and enhancement of small vessels after gadopentetate dimeglumine administration, represents such a technique. We therefore addressed the problem of mistaking vessels for nerves by adding a 3D TOF sequence both before and after the administration of gadopentetate dimeglumine (15,29). This methodological change, which allowed the reliable depiction of the nerves per se, is presumed to be the main reason for the high detection rate (95%) achieved in this study.
The width of the quadrigeminal plate cistern also can influence the identification of the trochlear nerve. Casselman and Dehaene (11) stated that visualization of the cisternal portion of the trochlear nerve is usually possible in older patients with large cisterns. The mean age of our study subjects was 60 years and suggests that these individuals may have had relatively large cisterns. To date, however, no relationship between the width of the quadrigeminal plate cistern and patient age has been quantified.
The course of the trochlear nerve can be considered classic if the nerve first passes laterally from the inferior colliculus to the free edge of the tentorium in a nearly coronal plane (9,13) and then passes anteriorly in a sagittal plane. We identified such a course in 20 (35%) nerves. More frequently, however, the trochlear nerve was observed to pursue an oblique anterolateral course, advancing in both directions simultaneously (35 [61%] of nerves). This oblique course is more difficult to differentiate from blood vessels and may be a third reason for the smaller trochlear nerve detection rate in other studies (12).
Landmarks.—The superior medullary velum may be used as a landmark to identify the site at which the trochlear nerve leaves the brain stem (9). In all of the cases in which the trochlear nerve could be identified in the study, the nerve emerged just caudally to the inferior colliculus and just laterally to the triangular, or tent-shaped, superior medullary velum. The characteristic shape of the velum therefore serves as the landmark on imaging sections on which the trochlear nerve is sought. When the velum is identified, the PE of the trochlear nerve is then located 6 mm (range, 3–9 mm) lateral to the midline. This 6-mm distance, measured in vivo, approximates the known 4-mm (range, 3.0–5.5 mm) distance measured in fixed anatomic specimens described in the literature (25).
Neurovascular Relationships
The second aim of this study was to determine the normal variations in the neurovascular relationships of the initial cisternal segment of the trochlear nerve. In the ambient cistern, the trochlear nerve is either in close proximity to or in direct contact with the main trunk of the SCA and its branches (ie, accessory SCA, lateral and medial terminal stems, small and large collateral arteries: vermian, paravermian, collicular, and lateral hemispheric branches) (3,27). These vessels may course rostrally, caudally, anteriorly, or posteriorly to the trochlear nerve or, very rarely, penetrate the nerve (27,30). The same artery may cross the trochlear nerve one to three times, with or without direct contact with the nerve (27). Neurovascular contact between the trochlear nerve and the SCA can be detected anatomically in 90% of nerves (3).
The main trunk of the SCA can be divided into proximal (ie, initial) and distal portions. Although the proximal portion is far medial to the trochlear nerve, the distal portion is in close proximity to the trochlear nerve in 73% of cases (27). The proximal, or main trunk, of the SCA usually courses anteromedially to the trochlear nerve, crosses the anterior or posterior surface of the trochlear nerve, and terminates by dividing into lateral and medial terminal stems at any point between the basilar artery and the inferior colliculus (27). The lateral terminal stem of the SCA is in relation to the distal segment of the trochlear nerve (73%) more often than it is in relation to the proximal segment (20%) or entire cisternal segment of the trochlear nerve (6.7%) (27). The medial terminal stem can be located rostrally and/or caudally to the trochlear nerve (27). When the medial stem originates directly from the basilar artery, it is close to or in direct contact with almost the entire cisternal segment of the trochlear nerve (27).
In our study, the vessels that were related to the proximal cisternal segment of the trochlear nerve included the medial branches of the SCA and the veins. In 29 (51%) nerves, the medial SCA branches were in direct contact with the trochlear nerve, at a mean distance of 3.4 mm from the PE. In six (21%) of these 29 nerves, the distance between the point of contact and the PE was 1 mm. In two (4%) additional cases, arterial neurovascular contact at the PE was observed, and in three (5%) additional cases, venous contact at the PE was observed.
The total prevalence of 60% neurovascular contact observed in this imaging study is substantially less than the 90% prevalence reported in the anatomic literature (3). This difference may be explained by the fact that we limited our investigation to the proximal cisternal segment of the trochlear nerve and excluded the subtentorial segment, which also has contact with adjacent vessels. It is generally agreed that abnormalities result from neurovascular contacts only when the site of contact is at or near the REZ, where the individual nerve fibers are covered by central (ie, oligodendrocyte-derived) myelin rather than peripheral myelin (31). The REZ is defined as the "transition zone between central and peripheral myelin" (32). For the trochlear nerve, the REZ is 0–1.0-mm (mean, 0.3-mm) long in histologic preparations (13). Taking into consideration the estimated postfixation shrinkage of up to 20% (33), the measured length of the REZ of the trochlear nerve can be up to 1.2 mm in vivo. Therefore, only neurovascular contacts at and up to 1.2 mm distal to the PE may be relevant to how this mechanism causes abnormality. Defining the REZ as the most proximal 1.2 mm along the cisternal segment of the trochlear nerve, we detected arterial contacts at the REZ in 14% of the nerves and venous contacts at the REZ in 5% of the nerves. Even at the REZ, however, neurovascular contacts can remain asymptomatic, and this is also true for the facial nerve, which is shown to have asymptomatic contacts at the REZ in 21% of nerves (34), and for the trigeminal nerve, which is shown to have asymptomatic contacts at the REZ in 7% of nerves (32).
Superior Oblique Myokymia
The term superior oblique myokymia was coined by Hoyt and Keane (35) in 1970 to refer to a disorder that causes unilateral rotatory nystagmus. It was postulated that the origin of this disorder could be vascular compression of the trochlear nerve, which is a theory that has been supported by the effective microvascular decompression at neurosurgery in two patients (36,37). Investigators in prior neuroimaging studies (36–40) of superior oblique myokymia could not detect neurovascular conflicts affecting the trochlear nerve. In the patient we examined, a medial SCA branch was observed to be in close contact with the right trochlear nerve, directly at the PE of the nerve. Because the patient had a good response to carbamazepine, which is the first line of treatment for superior oblique myokymia, no further therapy was considered to be necessary at the time of the study. If similar MR imaging findings can be confirmed in a series of patients with superior oblique myokymia, further arguments that support the microvascular compression hypothesis of neural dysfunction could be advanced. The ability to visualize neurovascular contact by using MR imaging could help in the decision making and planning of microvascular decompression of the affected nerve.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, I.Y., T.A.Y.; study concepts, I.Y., U.D.S., T.P.N., T.A.Y.; study design, I.Y., T.A.Y., M.D., B.M.; literature research, I.Y., M.D.; clinical studies, M.D., I.Y.; data acquisition, I.Y., B.M., M.D.; data analysis/interpretation, I.Y., M.D., T.A.Y.; statistical analysis, I.Y.; manuscript preparation, I.Y., B.M., T.P.N., U.D.S., T.A.Y.; manuscript definition of intellectual content, I.Y., M.D., T.P.N., T.A.Y.; manuscript editing, revision/review, and final version approval, all authors.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSIONREFERENCES |
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