Author's Accepted Manuscript
Brainstem white matter tracts and the control of eye movements Koji Sakai PhD, Hajime Yokota MD, PhD, Kentaro Akazawa MD, PhD, Kei Yamada MD, PhD
www.elsevier.com/locate/enganabound
PII: DOI: Reference:
S0887-2171(14)00067-5 http://dx.doi.org/10.1053/j.sult.2014.06.009 YSULT597
To appear in: Semin Ultrasound CT MRI
Cite this article as: Koji Sakai PhD, Hajime Yokota MD, PhD, Kentaro Akazawa MD, PhD, Kei Yamada MD, PhD, Brainstem white matter tracts and the control of eye movements, Semin Ultrasound CT MRI , http://dx.doi.org/10.1053/j.sult.2014.06.009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Brainstem white matter tracts and the control of eye movements
Koji Sakai*1 PhD, Hajime Yokota*2, 3 MD, PhD, Kentaro Akazawa2 MD, PhD, Kei Yamada2 MD, PhD
*equal contribution
1. Graduate School of Medicine, Department of Human Health Science, Kyoto University 2. Graduate School of Medical Science, Department of Radiology, Kyoto Prefectural University of Medicine 3. Graduate School of Medicine, Department of Diagnostic Radiology and Radiation Oncology, Chiba University
Contact Adress Shogoin Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, JAPAN TEL: +81-75-751-1625 e-mail: [email protected]
Abbreviations III: oculomotor nucleus IV: trochlear nucleus VI: abducens nucleus 1
VII: facial nucleus ASCT: anterior spinocerebellar tract CPT: corticopontine tract CST: corticospinal tract CTT: central tegmental tract DSCP: decussation of superior cerebellar peduncle ICP: inferior cerebellar peduncle IOP: inferior olivary peduncle MCP: middle cerebellar peduncle ML: medial lemniscus MLF: medial longitudinal fasciculus PCT: pontocerebellar tract PPRF: paramedian pontine reticular formation RN: red nucleus SCP: superior cerebellar peduncle SN: substantia nigra SThT: spinothalamic tract T1WI: T1-weighted MR image T2WI: T2-weighted MR image
Abstract This paper summarizes the anatomy of brainstem tracts and cranial nerves as depicted by magnetic resonance imaging, with special emphasis on the structures that are involved in the control of eye movement. It discusses the 2
anatomical structures that can be observed on conventional magnetic resonance images as well as structures that can only be observed using more advanced imaging techniques such as diffusion tensor imaging and tractography. The basic mechanisms of various kinds of ophthalmoplegia are also discussed.
1. Introduction The brainstem is one of the most important parts of the central nervous system (CNS). In addition to regulating fundamental activities that are vital to human life, the brainstem also controls complex eye movements, and examination of unusual eye movements enables neurologists to estimate the precise location of brainstem lesions. Neuroanatomically, the brainstem is one of the most thoroughly studied regions of the CNS. The brainstem is composed of three parts: the medulla oblongata, the pons, and the midbrain. Although the diencephalon can be also included in the brainstem, we chose to exclude it from this paper for simplicity. The brainstem is comprised of many different nuclei and tracts, each one with a different function. The brainstem includes the control centers for autonomic functions, as well as the circuits that control consciousness. There are also major ascending and descending tracts within the brainstem, some of which will be covered in a different paper in this edition and are thus not included herein. In this article, we summarize the basic anatomy of the brainstem that can be visualized with magnetic resonance (MR) imaging. The MR imaging techniques covered include both conventional and more advanced techniques such as 3
diffusion tensor imaging (DTI) and tractography. We have emphasized the depiction of the cranial nerves (CN) that are important to the control of eye movement.
2. Tracts within the brainstem 2.1. Basic anatomy The basic anatomical architecture of the brainstem is no different to that of the neural tube. The ventral portion is motor related and the dorsal part is sensory related. The corticospinal tract runs ventrally through the brainstem. The dorsal part of the brainstem is composed of fibers that ascend from the spinal cord. The same rule applies to the nuclei of the CN. The motor nuclei are located ventral to the central canal (for example, in the aqueduct and the fourth ventricle) and the sensory nuclei are located slightly dorsal or sometimes lateral to the motor nuclei. In this chapter we focus on the control of eye movement and discuss the fibers that are related to the control of eye movement and that run in close proximity to the CN, including CN III, IV and VI. 2.1.1. Medial longitudinal fasciculus (MLF) Conjugate eye movement is performed by synchronous activity of CN III, IV and VI. Connecting fibers joining the nuclei for these nerves pass through the MLF. Other CN related to eye movements include CN V, VII, VIII, and XI, and these are also connected to the MLF. The MLF itself is continuous with the spinal cord and has descending fibers that control head position and posture. 2.1.2 Medial lemniscus (ML) The ML is the major fiber pathway carrying proprioceptive information. It leads to 4
the thalamus from the dorsal funiculus and passes close to the midline of the brainstem. The ML is horizontally oriented on an axial MR image of the pons, but vertically oriented below and above the pons (Figure 1-4). It can be easily identified, even on sagittal T1-weighted MR images (T1WI), as a line of hypointensity between the pontine base and the tegmentum. The ML can sometimes be helpful in determining which part of an atrophied pons is affected. 2.1.3. Spinothalamic tract The spinothalamic tract carries information regarding pain, temperature, crude touch and firm pressure. It extends from the anterolateral funiculus of the spinal cord to the thalamus and passes through the outer edge of the brainstem. In the midbrain and pons it ascends along with the ML (Figure 1-4). 2.1.4. Central tegmental tract (CTT) The rubro-olivary tracts, which connect the red nucleus and the inferior olivary nucleus, pass through the CTT. The CTT forms part of the extrapyramidal system and is involved in augmenting movement, in conjunction with the dentate nucleus of the cerebellum. The circuit between the red nucleus, the inferior olivary nucleus, and the dentate nucleus is called the Guillan-Mollaret triangle. 2.1.5. Superior cerebellar peduncle (SCP) The SCP primarily comprises efferent fibers. The tracts originate from the dentate nucleus and travel to the contralateral red nucleus and thalamus, crossing at the midbrain, at the point known as the superior cerebellar decussation. The tracts to the contralateral red nucleus form part of the Guillan-Mollaret triangle. The anterior spinocerebellar tract, which includes proprioceptive fibers, is the only afferent tract that passes through the SCP. 5
2.1.6. Middle cerebellar peduncle The middle cerebellar peduncle is the largest white matter structure of the cerebellum and contains only afferent fibers, including the pontocerebellar tract. Fibers from the cerebral cortex reach the contralateral cerebellum via the ventral pontine nuclei. 2.1.7. Inferior cerebellar peduncle The inferior cerebellar peduncle is primarily composed of afferent fibers, including the posterior spinocerebellar and olivocerebellar tracts. This tract should be particularly scrutinized in patients presenting with clinical features of ‘central’ vertigo. The olivocerebellar tract forms the last piece of the Guillan-Mollaret triangle.
2.2 Basic sectional anatomy In this section we use T2-weighted MR images (T2WI) and vector color maps (VCM) to demonstrate the sectional anatomy of the brainstem. VCM depict the crude locations of major fiber pathways. Minor fibers are hidden within these major fiber pathways and thus cannot be directly observed, except for some of the relatively large fiber bundles. The brainstem nuclei are mainly composed of neuronal cells and thus have less anisotropy than neuronal fiber tracts. Therefore, they are not clearly visible on VCM 1. 2.2.1. Anatomy at the level of the CN III nuclei The midbrain including the CN III nuclei is shown in Figure 1. The corticospinal tract is located at the ventral portion of brainstem and is slightly hyperintense on T2WI compared to the surrounding structures. The red nucleus and substantia 6
nigra are the other landmark structures that can be clearly seen as hypointense regions on T2WI due to pigmentation. However, these nuclei are obscured on VCM as many fibers with different orientations pass through these regions. Part of the tract of CN III passing through the tegmentum can be perceived as an anteroposteriorly oriented fiber bundle (shown in green on Figure 1).
2.2.2. Anatomy at the level of the CN IV nuclei The midbrain including the CN IV nuclei is shown in Figure 2. The superior cerebellar decussation can be identified as an area of slight hyperintensity at the midline on T2WI, and is often also hyperintense on diffusion-weighted MR images. However, VCM are much more reliable for identifying internal brainstem structures such as the SCP and the superior cerebellar decussation. The decussation is a transversely oriented fiber bundle at the midline in red color on Figure 2. The SCP that connects to this decussation can also be identified. Smaller longitudinal fibers such as the MLF and CTT are hidden within these fibers on VCM.
2.2.3. Anatomy at the level of the CN VI nuclei The pons including the CN VI nuclei is shown in Figure 3. The ML can be seen as a slightly hyperintense region on T2WI and a slightly hypointense region on T1WI. Its ventral margin forms the border between the pontine tegmentum and the basis pontis. VCM depict major fiber bundles at the pontine base, including longitudinal fibers such as the corticopontine and corticospinal tracts as well as transverse fibers such as the pontocerebellar tract. The transverse fibers of the 7
pontocerebellar tract pass through the middle cerebellar peduncle to reach the cerebellum. The tract of CN V through the brachium pontis, which can be perceived as an anteroposteriorly oriented fiber bundle (shown in green on Figure 3), continues as the trigeminal nerve running through the cerebrospinal fluid (CSF).
2.2.4. Anatomy at the level of the inferior olivary nuclei The medulla oblongata including the inferior olivary nuclei is shown in Figure 4. Major fiber bundles at this level run in a craniocaudal direction, and thus are visualized as blue color fibers on VCM. The inferior olivary nuclei are seen as a pair of oval shaped structures at this level. However, they are somewhat difficult to visualize on VCM due to their low anisotropy.
2.3 Lesions involving brainstem tracts In this section, we briefly discuss brainstem pathologies that are not directly related to eye movements. Certain groups of neurons in the CNS may degenerate after injury to their axons or cell bodies, and this is referred to as Wallerian degeneration. Wallerian degeneration is typically observed on MR images as a hyperintense area on T2WI, and can only be observed from around 4 weeks after onset. Since the advent of DTI and tractography, Wallerian degeneration of several brainstem tracts has been studied. One example is the degeneration of the inferior cerebellar peduncle secondary to an infarct at the lateral
medulla2.
This
Wallerian
degeneration 8
was
depicted
on
diffusion-weighted MR images at 12 days after the event, which is earlier than the time at which changes can be depicted using conventional imaging techniques. Another important area that may show Wallerian degeneration is the CTT. For instance, in Leigh syndrome (subacute necrotizing encephalopathy), symmetric hyperintensity can be often observed along the CTT from the time when the putaminal signal abnormality first appears (Figure 5). This signal change may reflect a secondary effect throughout the extrapyramidal system, as it is inevitably associated with abnormalities in other regions, although primary damage to this tract cannot be completely excluded.
The CTT forms part of the Guillan-Mollaret triangle (Figure 6). Damage to any part of this triangle except for the inferior cerebellar peduncle can cause trans-synaptic degeneration of the inferior olivary nucleus, which is known as hypertrophic olivary degeneration (Figure 7)3. The loss of descending tonic inhibition is thought to account for the increased volume and signal hyperintensity of the olivary nuclei in the subacute phase. DTI and tractography have revealed a decrease in the volume of the CTT in patients with hypertrophic olivary degeneration4.
The ML has been studied using tractography and one study elucidated the direct involvement of the ML in a small dorsal pontine infarction, leading to pseudoathetosis by loss of ipsilateral proprioception5. The curved shape of the 9
ML in the sagittal view depicted by tractography in this study is identical to that evident in sagittal T1WI (Figure 3).
3. CN and CN nuclei related to eye movement 3.1. Basic anatomy The first two CN, the olfactory and optic nerves are the direct extension of the telencephalon and diencephalon, respectively. The remaining 10 pairs of CN originate from the brainstem. In this section, we focus on the three pairs of CN that control eye movements. 3.1.1. The oculomotor nerve The oculomotor nerve (CN III) is shown in Figure 8. The oculomotor nuclei are located in the parasagittal ventral apex of the central gray around the aqueduct, at the level of the superior colliculi, situated medial to the MLF (Figure 1). The motor nuclei of CN III control the majority of extraocular muscles, including the medial, superior, and inferior rectus, as well as the inferior oblique and levator palpebrae. The accessory nuclei of the oculomotor nerve (Edinger-Westphal nucleus), which project visceral efferent fibers, are located superomedial to the main nuclei. The parasympathetic nerve, which originates from these accessory nuclei, is connected with the ciliary ganglion and controls the smooth muscles inside the eyeball, including the musculus ciliaris and sphincter muscle of the pupil. The oculomotor tract through the midbrain runs ventrally along the parasagittal midline, and most of it runs through the medial part of the red 10
nucleus. It then exits the brainstem through the interpeduncular fossa. Within the CSF space, it passes between the posterior cerebral artery and the superior cerebellar arteries, and forms the lateral border of Liliequist’s membrane. It then enters the foramen of the oculomotor nerve to run in the lateral wall of the cavernous sinus.
3.1.2. The trochlear nerve The trochlear nerve (CN IV) is shown in Figure 9. The trochlear nuclei are located caudal to the oculomotor nuclei and are in close proximity with the dorsal part of the MLF. They control the superior oblique muscles. The fiber bundles from the trochlear nuclei initially proceed dorsally, and cross at the superior medullary velum just beneath the level of the inferior colliculi. This is the only CN that controls the contralateral structure. After exiting the brainstem, the trochlear nerves run through the ambient cistern, circling the cerebral peduncles.
3.1.3. The abducens nerve The abducens nerve (CN VI) is shown in Figure 10. The abducens nuclei are located at the parasagittal region of the middle-lower part of pons. They are seated in the area of the facial colliculi, where the facial nerve tracts follow a sharp J-turn around the abducens nuclei. These nuclei control the lateral rectus muscles. The paramedian pontine reticular formation (PPRF) is located ventral to the abducens nuclei and the MLF at the midline location of pons, and is known as the lateral gaze center of brainstem. The abducens tracts head forward and downward within the pons, and pass through the ML and the corticospinal tract. 11
They then leave the brainstem via the pontomedullary groove, ascend within the prepontine cistern and finally enter the foramen of abducens nerve, also known as Dorello’s canal. These foramina are located below the petroclival ligaments.
3.2. Lesions affecting eye movement CN III and VI exit from the ventral aspect of the brainstem and CN IV exits from the dorsal aspect of the midbrain. Lesions that directly involve the nuclei and fibers at the exit zones can cause monoplegia.
Gaze is a much more complex eye movement that is mainly controlled by the combination of CN III, IV and VI. Gaze can be simply classified as lateral, vertical or conjugate. The frontal eye field (Brodmann area 8) and supplementary eye field (Brodmann area 6) are regions of the cerebral cortex that control gaze, and they innervate the contralateral PPRF, which controls lateral gaze. Fibers from the PPRF reach the ipsilateral CN VI nucleus and contralateral CN III nucleus through the contralateral MLF.
Lateral gaze palsies are classified as internuclear ophthalmoplegia, lateral gaze palsy, or one and a half syndrome, and the corresponding lesions are located in the MLF; PPRF; and the MLF and PPRF, respectively (Figure 11)6,
7, 8
. In
internuclear ophthalmoplegia, lesions in the MLF cause ipsilateral eye adduction failure. The contralateral eye can abduct, but with nystagmus. In lateral gaze palsy, lesions in the PPRF cause ipsilateral eye abduction and contralateral eye 12
adduction failure. Lateral gaze to the contralateral side is preserved in these cases. If there are lesions in both the MLF and the PPRF, symptoms of both internuclear ophthalmoplegia and lateral gaze palsy can occur. The symptoms of this ‘one and a half’ syndrome include ipsilateral eye abduction and adduction failure and contralateral eye adduction failure. The contralateral eye can abduct, but with nystagmus. Demyelinating diseases, infarction, hemorrhage and neoplasms are representative causes of horizontal gaze palsy. The most common causes are multiple sclerosis in young patients and brainstem infarction in elderly patients (Figure 12).
The control center for vertical gaze is located at the rostral interstitial nucleus of the MLF, near the CN III nucleus in the midbrain. The Cajal interstitial nucleus also plays a role in the control of vertical gaze. In addition, it has been suggested that a center for convergence is located near CN III nucleus. A lesion in the midbrain, such as tumor, can cause vertical gaze palsy and convergence palsy, and this is known as Parinaud syndrome. Progressive supranuclear palsy is often accompanied by vertical gaze palsy, possibly due to the degeneration that takes place in this part of the midbrain9, 10.
3.4. Lesions affecting the ocular nerves in the subarachnoid space The CNs can be directly affected by various causes, including ischemia, inflammation, infection, autoimmune disease and trauma. The length of some CN within the subarachnoid space is relatively long, rendering them vulnerable 13
to subarachnoid space lesions, including but not limited to aneurysmal compression, dissemination of neoplasm, meningitis, cerebral herniation and CSF hypovolemia.
Aneurysmal compression of CN III may arise from lesions of the carotid siphon or posterior communicating artery origin (Figure 13). The third nerve palsy in such cases is often complete with both oculomotor palsy and papillary dilatation (a so called “surgical IIIrd nerve”). This is in distinction to the partial IIIrd nerve palsy (oculomotor palsy but preserved papillary function) seen in microvascular ischemia due to diabetes mellitus (so called “medical IIIrd nerve palsy). External compressive lesions affect but the parasympathetic fibers which run on the surface/periphery of the nerve as well as the motor fibers deeper within. In cases of microvascular ischemia, there is occlusion of the vasa nervorum running over the surface of the nerve, limiting diffusion of oxygen to the motor fibers deep within the nerve; due to collateralization of blood supply over the surface the parasympathetic fibers are relatively preserved. Of the three CN involved in the control of eye movements, CN III is the only one that has been successfully depicted within the brainstem using tractography11, 12. This probably owes to the relatively larger size of this nerve compared with CN IV and VI. Depiction of CN III in the brainstem allows visualization of the spatial relationship between the midbrain lesions and the internal neural pathway of CN III. There are reports of patients with congenital absence of CNs13. Möbius syndrome is characterized by congenital palsies of CNs VI and VII bilaterally is 14
due to heterogeneous causes, such as brainstem dysgenesis or destructive episodes in fetal stages, such as ischemia. High-resolution imaging sequences have revealed absence of these nerves in such cases (Figure 14).
4. Summary MR imaging allows noninvasive observation of some of the important brainstem structures. CN that run through the CSF space can be more easily visualized than other structures as they can be imaged by high-resolution imaging sequences, typically the heavily-T2-weighted steady state imaging sequences. Imaging the internal structures within the brainstem is more challenging. Although some of the important structures, including the superior cerebellar decussation and the ML at the level of pons, can be seen on conventional images, most structures are much more difficult to image unless they have pathological changes in signal intensity. The newer imaging techniques, including DTI and tractography, are able to clearly show some of the fibers within the brainstem and will aid further observations. However, even with these newer techniques, the majority of the fine structures in the brainstem cannot be directly observed, and an understanding of neuroanatomy is crucial to identify their locations and explain the clinical manifestations of lesions in this part of the brain.
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REFERENCES 1. Nagae-Poetscher LM, Jiang H, Wakana S, et al: High-resolution diffusion tensor imaging of the brain stem at 3 T: AJNR Am J Neuroradiol 25:1325-30, 2004 2. Yamada K, Kizu O, Ito H, et al: Wallerian degeneration of the inferior cerebellar peduncle depicted by diffusion weighted imaging: J Neurol Neurosurg Psychiatry 74:977–978, 2003 3. Kitajima M, Korogi Y, Shimomura O, et al: Hypertrophic olivary degeneration: MR imaging and pathologic findings: Radiology. 192:539-43, 1994 4. Shah R, Markert J, Bag AK, et al: Diffusion Tensor Imaging in Hypertrophic Olivary Degeneration: AJNR Am J Neuroradiol 31:1729–31, 2010 5. Shiga K, Miyagawa M, Yamada K, et al: Pontine pseudoathetosis: lemniscal involvement visualized by axonal tracking method with diffusion tensor imaging: J Neurol 250:511-512, 2003 6. Kataoka S, Hori A, Shirakawa T, et al: Paramedian pontine infarction. Neurological/topographical correlation: Stroke 28:809-15, 1997 7. de Seze J, Lucas C, Leclerc X, et al: One-and-a-half syndrome in pontine infarcts: MRI correlates: Neuroradiology 41:666-9, 1999 8. Wall M, Wray SH: The one-and-a-half syndrome-a unilateral disorder of the pontine tegmentum: a study of 20 cases and review of the literature: Neurology 33:971-80, 1983 9. Yagishita A, Oda M: Progressive supranuclear palsy: MRI and pathological findings: Neuroradiology 38 Suppl 1:S60-66, 1996 10. Oba H, Yagishita A, Terada H, et al: New and reliable MRI diagnosis for 16
progressive supranuclear palsy: Neurology 64:2050-2055, 2005. 11. Yamada K, Shiga K, Kizu O, et al: Oculomotor nerve palsy evaluated by diffusion-tensor tractography: Neuroradiology 48: 434–437, 2006 12. Kwon HG, Kim MS, Kim SH, et al: Injury of the oculomotor nerve in a patient with traumatic brain injury: diffusion tensor tractography study: J Neurol Neurosurg Psychiatry 84:1073–1074, 2013 13. Assaf AA: Congenital innervation dysgenesis syndrome (CID)/congenital cranial dysinnervation disorders (CCDDs): Eye (Lond) 25:1251-61, 2011
Figure legends Figure 1. Anatomy at the level of the midbrain including the CN III nuclei. a) Axial T2 weighted image showing labeled structures, b) Vector color map (VCM) showing labeled structures.
Figure 2. Anatomy at the level of the trochlear (CN IV) nuclei. a) Axial T2 and b) VCM image with labeled structures.
Figure 3. Anatomy at the level of the CN VI nuclei in the pons. a) Axial T2, b) VCM and c) sagittal T1 weighted images showing anatomical labels. The ML in c allows identification of the boundary between the pontine tegmentum (anteriorly) and the basis pontis (posteriorly).
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Figure 4. Anatomy at the level of the medulla oblongata including the inferior olivary nuclei. a) Axial T2 and b) VCM image with anatomical labels.
Figure 5. Leigh’s encephalopathy highlighting the central tegmental tracts. a) and b) axial T2 weighted images in the midbrain showing hyperintense signal in the central tegmental tracts (arrows); c) axial T2 weighted image showing diffuse bilateral lenticular T2 hyperintensity (arrows).
Figure 6. The Guillan-Mollaret triangle. Diagram showing the circuit connecting the dentate nucleus (DN) of the cerebellum of one side with the red nucleus (RN) and the inferior olivary nucleus (ION) of the other side, via the superior cerebellar peduncle and the inferior cerebellar peduncle, and connecting RN with ION via the central tegmental tract.
Figure 7. Hypertrophic olivary degeneration. This is an 45-year-old male with bleeding cavernoma of the pons/midbrain. a) and b) Axial T2 weighted images showing a haemorrhagic cavernoma in the right dorsolateral midbrain. The haematoma compresses the right superior cerebellar peduncle and right central 18
tegmental tract; c) Axial T2 weighted image at the level of the medulla one year later showing bilateral hypertrophic olivary degeneration; involvement of the left olive is likely secondary to the superior cerebellar peduncle involvement whereas involvement of the right side is likely due to CTT damage (Images courtesy of Dr. Mukai, Chiba University Hospital, Japan)
Figure 8. Anatomy of CNIII. a) Axial T2 weighted image through the midbrain showing the location of the III nuclei and the ventral paramedian course; b) Axial T2 weighted steady state image showing the cisternal portions of CN III bilaterally (arrows) emerging from the interpeduncular fossa.
Figure 9. Anatomy of the trochlear (CN IV) nerve. a) Axial T2 and b) T2 weighted steady-state images showing the presumed course of the trochlear nerves bilaterally (dotted lines); the nerves are frequently too small to identify, even with sub-millimetre voxel acquisition.
Figure 10. Anatomy of the abducens (CN VI) nerve. a) Axial T2 weighted image showing the paramedian course of the VIth nerves (yellow dotted lines) and the
19
looping course of the VIIth cranial nerve (orange dashed arrows) around the VIth nerve nuclei; b) axial and c) sagittal T2 weighted steady state sequence showing the cisternal portions (arrows) of the VIth nerve.
Figure 11. Lateral eye movement disorders. a) Diagram showing the clinical features of internuclear ophthalmoplegia due to a lesion of the MLF, the lesion is on the side of adduction failure; b) lateral gaze palsy due to a lesion in the PPRF, the side of the lesion corresponds to the side of lateral gaze failure; c) ‘one and a half’ syndrome due to a lesion affecting both the MLF and PPRF, the side that can still abduct (albeit with nystagmus) is contralateral to the side of the lesion.
Figure 12. Clinical case of INO in a 40 yr old male. a) Axial T2 weighted image showing left paramedian hyperintensity in the dorsal pons; b) Axial DWI shows diffusion restriction; c) VCM demonstrates a small infarct in the longitudinal fibers; d) Axial T2 weighted image showing exotropia (left eye turned out) due to adduction failure from damage to the left MLF. The right eye is in a normal position.
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Figure 13. Aneurysmal compression of CN III and VI in a 60 year old male with ophthalmoplegia. a) Maximum Intensity Projection (MIP) of MR angiography shows aneurysm of the right internal carotid siphon; b) coronal T2 steady state image showing that the right CN III is compressed upward compared to the left side (arrows); c) the right CN III passes along the superior surface of the aneurysm (arrow).(Images courtesy of Dr. Mukai, Chiba University Hospital, Japan)
Figure 14. 6-year-old child with Möbius syndrome. a) and b) Axial T2 steady state image showing absent VIIth nerves (a) and VIth nerves (b) with only the VIIIth nerves visible bilaterally (arrows); c) axial T2 weighted steady state image showing bilateral esotropia (inturned eyes) due to abduction failure; d) axial T2 weighted image showing V-shaped depression in the fourth ventricular floor due to the absence of facial colliculi (arrows).
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Brainstem white matter tracts and the control of eye movements Koji Sakai PhD, Hajime Yokota MD, PhD, Kentaro Akazawa MD, PhD, Kei Yamada MD, PhD
www.elsevier.com/locate/enganabound
PII: DOI: Reference:
S0887-2171(14)00067-5 http://dx.doi.org/10.1053/j.sult.2014.06.009 YSULT597
To appear in: Semin Ultrasound CT MRI
Cite this article as: Koji Sakai PhD, Hajime Yokota MD, PhD, Kentaro Akazawa MD, PhD, Kei Yamada MD, PhD, Brainstem white matter tracts and the control of eye movements, Semin Ultrasound CT MRI , http://dx.doi.org/10.1053/j.sult.2014.06.009 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Brainstem white matter tracts and the control of eye movements
Koji Sakai*1 PhD, Hajime Yokota*2, 3 MD, PhD, Kentaro Akazawa2 MD, PhD, Kei Yamada2 MD, PhD
*equal contribution
1. Graduate School of Medicine, Department of Human Health Science, Kyoto University 2. Graduate School of Medical Science, Department of Radiology, Kyoto Prefectural University of Medicine 3. Graduate School of Medicine, Department of Diagnostic Radiology and Radiation Oncology, Chiba University
Contact Adress Shogoin Kawahara-cho, Sakyo-ku, Kyoto, 606-8507, JAPAN TEL: +81-75-751-1625 e-mail: [email protected]
Abbreviations III: oculomotor nucleus IV: trochlear nucleus VI: abducens nucleus 1
VII: facial nucleus ASCT: anterior spinocerebellar tract CPT: corticopontine tract CST: corticospinal tract CTT: central tegmental tract DSCP: decussation of superior cerebellar peduncle ICP: inferior cerebellar peduncle IOP: inferior olivary peduncle MCP: middle cerebellar peduncle ML: medial lemniscus MLF: medial longitudinal fasciculus PCT: pontocerebellar tract PPRF: paramedian pontine reticular formation RN: red nucleus SCP: superior cerebellar peduncle SN: substantia nigra SThT: spinothalamic tract T1WI: T1-weighted MR image T2WI: T2-weighted MR image
Abstract This paper summarizes the anatomy of brainstem tracts and cranial nerves as depicted by magnetic resonance imaging, with special emphasis on the structures that are involved in the control of eye movement. It discusses the 2
anatomical structures that can be observed on conventional magnetic resonance images as well as structures that can only be observed using more advanced imaging techniques such as diffusion tensor imaging and tractography. The basic mechanisms of various kinds of ophthalmoplegia are also discussed.
1. Introduction The brainstem is one of the most important parts of the central nervous system (CNS). In addition to regulating fundamental activities that are vital to human life, the brainstem also controls complex eye movements, and examination of unusual eye movements enables neurologists to estimate the precise location of brainstem lesions. Neuroanatomically, the brainstem is one of the most thoroughly studied regions of the CNS. The brainstem is composed of three parts: the medulla oblongata, the pons, and the midbrain. Although the diencephalon can be also included in the brainstem, we chose to exclude it from this paper for simplicity. The brainstem is comprised of many different nuclei and tracts, each one with a different function. The brainstem includes the control centers for autonomic functions, as well as the circuits that control consciousness. There are also major ascending and descending tracts within the brainstem, some of which will be covered in a different paper in this edition and are thus not included herein. In this article, we summarize the basic anatomy of the brainstem that can be visualized with magnetic resonance (MR) imaging. The MR imaging techniques covered include both conventional and more advanced techniques such as 3
diffusion tensor imaging (DTI) and tractography. We have emphasized the depiction of the cranial nerves (CN) that are important to the control of eye movement.
2. Tracts within the brainstem 2.1. Basic anatomy The basic anatomical architecture of the brainstem is no different to that of the neural tube. The ventral portion is motor related and the dorsal part is sensory related. The corticospinal tract runs ventrally through the brainstem. The dorsal part of the brainstem is composed of fibers that ascend from the spinal cord. The same rule applies to the nuclei of the CN. The motor nuclei are located ventral to the central canal (for example, in the aqueduct and the fourth ventricle) and the sensory nuclei are located slightly dorsal or sometimes lateral to the motor nuclei. In this chapter we focus on the control of eye movement and discuss the fibers that are related to the control of eye movement and that run in close proximity to the CN, including CN III, IV and VI. 2.1.1. Medial longitudinal fasciculus (MLF) Conjugate eye movement is performed by synchronous activity of CN III, IV and VI. Connecting fibers joining the nuclei for these nerves pass through the MLF. Other CN related to eye movements include CN V, VII, VIII, and XI, and these are also connected to the MLF. The MLF itself is continuous with the spinal cord and has descending fibers that control head position and posture. 2.1.2 Medial lemniscus (ML) The ML is the major fiber pathway carrying proprioceptive information. It leads to 4
the thalamus from the dorsal funiculus and passes close to the midline of the brainstem. The ML is horizontally oriented on an axial MR image of the pons, but vertically oriented below and above the pons (Figure 1-4). It can be easily identified, even on sagittal T1-weighted MR images (T1WI), as a line of hypointensity between the pontine base and the tegmentum. The ML can sometimes be helpful in determining which part of an atrophied pons is affected. 2.1.3. Spinothalamic tract The spinothalamic tract carries information regarding pain, temperature, crude touch and firm pressure. It extends from the anterolateral funiculus of the spinal cord to the thalamus and passes through the outer edge of the brainstem. In the midbrain and pons it ascends along with the ML (Figure 1-4). 2.1.4. Central tegmental tract (CTT) The rubro-olivary tracts, which connect the red nucleus and the inferior olivary nucleus, pass through the CTT. The CTT forms part of the extrapyramidal system and is involved in augmenting movement, in conjunction with the dentate nucleus of the cerebellum. The circuit between the red nucleus, the inferior olivary nucleus, and the dentate nucleus is called the Guillan-Mollaret triangle. 2.1.5. Superior cerebellar peduncle (SCP) The SCP primarily comprises efferent fibers. The tracts originate from the dentate nucleus and travel to the contralateral red nucleus and thalamus, crossing at the midbrain, at the point known as the superior cerebellar decussation. The tracts to the contralateral red nucleus form part of the Guillan-Mollaret triangle. The anterior spinocerebellar tract, which includes proprioceptive fibers, is the only afferent tract that passes through the SCP. 5
2.1.6. Middle cerebellar peduncle The middle cerebellar peduncle is the largest white matter structure of the cerebellum and contains only afferent fibers, including the pontocerebellar tract. Fibers from the cerebral cortex reach the contralateral cerebellum via the ventral pontine nuclei. 2.1.7. Inferior cerebellar peduncle The inferior cerebellar peduncle is primarily composed of afferent fibers, including the posterior spinocerebellar and olivocerebellar tracts. This tract should be particularly scrutinized in patients presenting with clinical features of ‘central’ vertigo. The olivocerebellar tract forms the last piece of the Guillan-Mollaret triangle.
2.2 Basic sectional anatomy In this section we use T2-weighted MR images (T2WI) and vector color maps (VCM) to demonstrate the sectional anatomy of the brainstem. VCM depict the crude locations of major fiber pathways. Minor fibers are hidden within these major fiber pathways and thus cannot be directly observed, except for some of the relatively large fiber bundles. The brainstem nuclei are mainly composed of neuronal cells and thus have less anisotropy than neuronal fiber tracts. Therefore, they are not clearly visible on VCM 1. 2.2.1. Anatomy at the level of the CN III nuclei The midbrain including the CN III nuclei is shown in Figure 1. The corticospinal tract is located at the ventral portion of brainstem and is slightly hyperintense on T2WI compared to the surrounding structures. The red nucleus and substantia 6
nigra are the other landmark structures that can be clearly seen as hypointense regions on T2WI due to pigmentation. However, these nuclei are obscured on VCM as many fibers with different orientations pass through these regions. Part of the tract of CN III passing through the tegmentum can be perceived as an anteroposteriorly oriented fiber bundle (shown in green on Figure 1).
2.2.2. Anatomy at the level of the CN IV nuclei The midbrain including the CN IV nuclei is shown in Figure 2. The superior cerebellar decussation can be identified as an area of slight hyperintensity at the midline on T2WI, and is often also hyperintense on diffusion-weighted MR images. However, VCM are much more reliable for identifying internal brainstem structures such as the SCP and the superior cerebellar decussation. The decussation is a transversely oriented fiber bundle at the midline in red color on Figure 2. The SCP that connects to this decussation can also be identified. Smaller longitudinal fibers such as the MLF and CTT are hidden within these fibers on VCM.
2.2.3. Anatomy at the level of the CN VI nuclei The pons including the CN VI nuclei is shown in Figure 3. The ML can be seen as a slightly hyperintense region on T2WI and a slightly hypointense region on T1WI. Its ventral margin forms the border between the pontine tegmentum and the basis pontis. VCM depict major fiber bundles at the pontine base, including longitudinal fibers such as the corticopontine and corticospinal tracts as well as transverse fibers such as the pontocerebellar tract. The transverse fibers of the 7
pontocerebellar tract pass through the middle cerebellar peduncle to reach the cerebellum. The tract of CN V through the brachium pontis, which can be perceived as an anteroposteriorly oriented fiber bundle (shown in green on Figure 3), continues as the trigeminal nerve running through the cerebrospinal fluid (CSF).
2.2.4. Anatomy at the level of the inferior olivary nuclei The medulla oblongata including the inferior olivary nuclei is shown in Figure 4. Major fiber bundles at this level run in a craniocaudal direction, and thus are visualized as blue color fibers on VCM. The inferior olivary nuclei are seen as a pair of oval shaped structures at this level. However, they are somewhat difficult to visualize on VCM due to their low anisotropy.
2.3 Lesions involving brainstem tracts In this section, we briefly discuss brainstem pathologies that are not directly related to eye movements. Certain groups of neurons in the CNS may degenerate after injury to their axons or cell bodies, and this is referred to as Wallerian degeneration. Wallerian degeneration is typically observed on MR images as a hyperintense area on T2WI, and can only be observed from around 4 weeks after onset. Since the advent of DTI and tractography, Wallerian degeneration of several brainstem tracts has been studied. One example is the degeneration of the inferior cerebellar peduncle secondary to an infarct at the lateral
medulla2.
This
Wallerian
degeneration 8
was
depicted
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diffusion-weighted MR images at 12 days after the event, which is earlier than the time at which changes can be depicted using conventional imaging techniques. Another important area that may show Wallerian degeneration is the CTT. For instance, in Leigh syndrome (subacute necrotizing encephalopathy), symmetric hyperintensity can be often observed along the CTT from the time when the putaminal signal abnormality first appears (Figure 5). This signal change may reflect a secondary effect throughout the extrapyramidal system, as it is inevitably associated with abnormalities in other regions, although primary damage to this tract cannot be completely excluded.
The CTT forms part of the Guillan-Mollaret triangle (Figure 6). Damage to any part of this triangle except for the inferior cerebellar peduncle can cause trans-synaptic degeneration of the inferior olivary nucleus, which is known as hypertrophic olivary degeneration (Figure 7)3. The loss of descending tonic inhibition is thought to account for the increased volume and signal hyperintensity of the olivary nuclei in the subacute phase. DTI and tractography have revealed a decrease in the volume of the CTT in patients with hypertrophic olivary degeneration4.
The ML has been studied using tractography and one study elucidated the direct involvement of the ML in a small dorsal pontine infarction, leading to pseudoathetosis by loss of ipsilateral proprioception5. The curved shape of the 9
ML in the sagittal view depicted by tractography in this study is identical to that evident in sagittal T1WI (Figure 3).
3. CN and CN nuclei related to eye movement 3.1. Basic anatomy The first two CN, the olfactory and optic nerves are the direct extension of the telencephalon and diencephalon, respectively. The remaining 10 pairs of CN originate from the brainstem. In this section, we focus on the three pairs of CN that control eye movements. 3.1.1. The oculomotor nerve The oculomotor nerve (CN III) is shown in Figure 8. The oculomotor nuclei are located in the parasagittal ventral apex of the central gray around the aqueduct, at the level of the superior colliculi, situated medial to the MLF (Figure 1). The motor nuclei of CN III control the majority of extraocular muscles, including the medial, superior, and inferior rectus, as well as the inferior oblique and levator palpebrae. The accessory nuclei of the oculomotor nerve (Edinger-Westphal nucleus), which project visceral efferent fibers, are located superomedial to the main nuclei. The parasympathetic nerve, which originates from these accessory nuclei, is connected with the ciliary ganglion and controls the smooth muscles inside the eyeball, including the musculus ciliaris and sphincter muscle of the pupil. The oculomotor tract through the midbrain runs ventrally along the parasagittal midline, and most of it runs through the medial part of the red 10
nucleus. It then exits the brainstem through the interpeduncular fossa. Within the CSF space, it passes between the posterior cerebral artery and the superior cerebellar arteries, and forms the lateral border of Liliequist’s membrane. It then enters the foramen of the oculomotor nerve to run in the lateral wall of the cavernous sinus.
3.1.2. The trochlear nerve The trochlear nerve (CN IV) is shown in Figure 9. The trochlear nuclei are located caudal to the oculomotor nuclei and are in close proximity with the dorsal part of the MLF. They control the superior oblique muscles. The fiber bundles from the trochlear nuclei initially proceed dorsally, and cross at the superior medullary velum just beneath the level of the inferior colliculi. This is the only CN that controls the contralateral structure. After exiting the brainstem, the trochlear nerves run through the ambient cistern, circling the cerebral peduncles.
3.1.3. The abducens nerve The abducens nerve (CN VI) is shown in Figure 10. The abducens nuclei are located at the parasagittal region of the middle-lower part of pons. They are seated in the area of the facial colliculi, where the facial nerve tracts follow a sharp J-turn around the abducens nuclei. These nuclei control the lateral rectus muscles. The paramedian pontine reticular formation (PPRF) is located ventral to the abducens nuclei and the MLF at the midline location of pons, and is known as the lateral gaze center of brainstem. The abducens tracts head forward and downward within the pons, and pass through the ML and the corticospinal tract. 11
They then leave the brainstem via the pontomedullary groove, ascend within the prepontine cistern and finally enter the foramen of abducens nerve, also known as Dorello’s canal. These foramina are located below the petroclival ligaments.
3.2. Lesions affecting eye movement CN III and VI exit from the ventral aspect of the brainstem and CN IV exits from the dorsal aspect of the midbrain. Lesions that directly involve the nuclei and fibers at the exit zones can cause monoplegia.
Gaze is a much more complex eye movement that is mainly controlled by the combination of CN III, IV and VI. Gaze can be simply classified as lateral, vertical or conjugate. The frontal eye field (Brodmann area 8) and supplementary eye field (Brodmann area 6) are regions of the cerebral cortex that control gaze, and they innervate the contralateral PPRF, which controls lateral gaze. Fibers from the PPRF reach the ipsilateral CN VI nucleus and contralateral CN III nucleus through the contralateral MLF.
Lateral gaze palsies are classified as internuclear ophthalmoplegia, lateral gaze palsy, or one and a half syndrome, and the corresponding lesions are located in the MLF; PPRF; and the MLF and PPRF, respectively (Figure 11)6,
7, 8
. In
internuclear ophthalmoplegia, lesions in the MLF cause ipsilateral eye adduction failure. The contralateral eye can abduct, but with nystagmus. In lateral gaze palsy, lesions in the PPRF cause ipsilateral eye abduction and contralateral eye 12
adduction failure. Lateral gaze to the contralateral side is preserved in these cases. If there are lesions in both the MLF and the PPRF, symptoms of both internuclear ophthalmoplegia and lateral gaze palsy can occur. The symptoms of this ‘one and a half’ syndrome include ipsilateral eye abduction and adduction failure and contralateral eye adduction failure. The contralateral eye can abduct, but with nystagmus. Demyelinating diseases, infarction, hemorrhage and neoplasms are representative causes of horizontal gaze palsy. The most common causes are multiple sclerosis in young patients and brainstem infarction in elderly patients (Figure 12).
The control center for vertical gaze is located at the rostral interstitial nucleus of the MLF, near the CN III nucleus in the midbrain. The Cajal interstitial nucleus also plays a role in the control of vertical gaze. In addition, it has been suggested that a center for convergence is located near CN III nucleus. A lesion in the midbrain, such as tumor, can cause vertical gaze palsy and convergence palsy, and this is known as Parinaud syndrome. Progressive supranuclear palsy is often accompanied by vertical gaze palsy, possibly due to the degeneration that takes place in this part of the midbrain9, 10.
3.4. Lesions affecting the ocular nerves in the subarachnoid space The CNs can be directly affected by various causes, including ischemia, inflammation, infection, autoimmune disease and trauma. The length of some CN within the subarachnoid space is relatively long, rendering them vulnerable 13
to subarachnoid space lesions, including but not limited to aneurysmal compression, dissemination of neoplasm, meningitis, cerebral herniation and CSF hypovolemia.
Aneurysmal compression of CN III may arise from lesions of the carotid siphon or posterior communicating artery origin (Figure 13). The third nerve palsy in such cases is often complete with both oculomotor palsy and papillary dilatation (a so called “surgical IIIrd nerve”). This is in distinction to the partial IIIrd nerve palsy (oculomotor palsy but preserved papillary function) seen in microvascular ischemia due to diabetes mellitus (so called “medical IIIrd nerve palsy). External compressive lesions affect but the parasympathetic fibers which run on the surface/periphery of the nerve as well as the motor fibers deeper within. In cases of microvascular ischemia, there is occlusion of the vasa nervorum running over the surface of the nerve, limiting diffusion of oxygen to the motor fibers deep within the nerve; due to collateralization of blood supply over the surface the parasympathetic fibers are relatively preserved. Of the three CN involved in the control of eye movements, CN III is the only one that has been successfully depicted within the brainstem using tractography11, 12. This probably owes to the relatively larger size of this nerve compared with CN IV and VI. Depiction of CN III in the brainstem allows visualization of the spatial relationship between the midbrain lesions and the internal neural pathway of CN III. There are reports of patients with congenital absence of CNs13. Möbius syndrome is characterized by congenital palsies of CNs VI and VII bilaterally is 14
due to heterogeneous causes, such as brainstem dysgenesis or destructive episodes in fetal stages, such as ischemia. High-resolution imaging sequences have revealed absence of these nerves in such cases (Figure 14).
4. Summary MR imaging allows noninvasive observation of some of the important brainstem structures. CN that run through the CSF space can be more easily visualized than other structures as they can be imaged by high-resolution imaging sequences, typically the heavily-T2-weighted steady state imaging sequences. Imaging the internal structures within the brainstem is more challenging. Although some of the important structures, including the superior cerebellar decussation and the ML at the level of pons, can be seen on conventional images, most structures are much more difficult to image unless they have pathological changes in signal intensity. The newer imaging techniques, including DTI and tractography, are able to clearly show some of the fibers within the brainstem and will aid further observations. However, even with these newer techniques, the majority of the fine structures in the brainstem cannot be directly observed, and an understanding of neuroanatomy is crucial to identify their locations and explain the clinical manifestations of lesions in this part of the brain.
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REFERENCES 1. Nagae-Poetscher LM, Jiang H, Wakana S, et al: High-resolution diffusion tensor imaging of the brain stem at 3 T: AJNR Am J Neuroradiol 25:1325-30, 2004 2. Yamada K, Kizu O, Ito H, et al: Wallerian degeneration of the inferior cerebellar peduncle depicted by diffusion weighted imaging: J Neurol Neurosurg Psychiatry 74:977–978, 2003 3. Kitajima M, Korogi Y, Shimomura O, et al: Hypertrophic olivary degeneration: MR imaging and pathologic findings: Radiology. 192:539-43, 1994 4. Shah R, Markert J, Bag AK, et al: Diffusion Tensor Imaging in Hypertrophic Olivary Degeneration: AJNR Am J Neuroradiol 31:1729–31, 2010 5. Shiga K, Miyagawa M, Yamada K, et al: Pontine pseudoathetosis: lemniscal involvement visualized by axonal tracking method with diffusion tensor imaging: J Neurol 250:511-512, 2003 6. Kataoka S, Hori A, Shirakawa T, et al: Paramedian pontine infarction. Neurological/topographical correlation: Stroke 28:809-15, 1997 7. de Seze J, Lucas C, Leclerc X, et al: One-and-a-half syndrome in pontine infarcts: MRI correlates: Neuroradiology 41:666-9, 1999 8. Wall M, Wray SH: The one-and-a-half syndrome-a unilateral disorder of the pontine tegmentum: a study of 20 cases and review of the literature: Neurology 33:971-80, 1983 9. Yagishita A, Oda M: Progressive supranuclear palsy: MRI and pathological findings: Neuroradiology 38 Suppl 1:S60-66, 1996 10. Oba H, Yagishita A, Terada H, et al: New and reliable MRI diagnosis for 16
progressive supranuclear palsy: Neurology 64:2050-2055, 2005. 11. Yamada K, Shiga K, Kizu O, et al: Oculomotor nerve palsy evaluated by diffusion-tensor tractography: Neuroradiology 48: 434–437, 2006 12. Kwon HG, Kim MS, Kim SH, et al: Injury of the oculomotor nerve in a patient with traumatic brain injury: diffusion tensor tractography study: J Neurol Neurosurg Psychiatry 84:1073–1074, 2013 13. Assaf AA: Congenital innervation dysgenesis syndrome (CID)/congenital cranial dysinnervation disorders (CCDDs): Eye (Lond) 25:1251-61, 2011
Figure legends Figure 1. Anatomy at the level of the midbrain including the CN III nuclei. a) Axial T2 weighted image showing labeled structures, b) Vector color map (VCM) showing labeled structures.
Figure 2. Anatomy at the level of the trochlear (CN IV) nuclei. a) Axial T2 and b) VCM image with labeled structures.
Figure 3. Anatomy at the level of the CN VI nuclei in the pons. a) Axial T2, b) VCM and c) sagittal T1 weighted images showing anatomical labels. The ML in c allows identification of the boundary between the pontine tegmentum (anteriorly) and the basis pontis (posteriorly).
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Figure 4. Anatomy at the level of the medulla oblongata including the inferior olivary nuclei. a) Axial T2 and b) VCM image with anatomical labels.
Figure 5. Leigh’s encephalopathy highlighting the central tegmental tracts. a) and b) axial T2 weighted images in the midbrain showing hyperintense signal in the central tegmental tracts (arrows); c) axial T2 weighted image showing diffuse bilateral lenticular T2 hyperintensity (arrows).
Figure 6. The Guillan-Mollaret triangle. Diagram showing the circuit connecting the dentate nucleus (DN) of the cerebellum of one side with the red nucleus (RN) and the inferior olivary nucleus (ION) of the other side, via the superior cerebellar peduncle and the inferior cerebellar peduncle, and connecting RN with ION via the central tegmental tract.
Figure 7. Hypertrophic olivary degeneration. This is an 45-year-old male with bleeding cavernoma of the pons/midbrain. a) and b) Axial T2 weighted images showing a haemorrhagic cavernoma in the right dorsolateral midbrain. The haematoma compresses the right superior cerebellar peduncle and right central 18
tegmental tract; c) Axial T2 weighted image at the level of the medulla one year later showing bilateral hypertrophic olivary degeneration; involvement of the left olive is likely secondary to the superior cerebellar peduncle involvement whereas involvement of the right side is likely due to CTT damage (Images courtesy of Dr. Mukai, Chiba University Hospital, Japan)
Figure 8. Anatomy of CNIII. a) Axial T2 weighted image through the midbrain showing the location of the III nuclei and the ventral paramedian course; b) Axial T2 weighted steady state image showing the cisternal portions of CN III bilaterally (arrows) emerging from the interpeduncular fossa.
Figure 9. Anatomy of the trochlear (CN IV) nerve. a) Axial T2 and b) T2 weighted steady-state images showing the presumed course of the trochlear nerves bilaterally (dotted lines); the nerves are frequently too small to identify, even with sub-millimetre voxel acquisition.
Figure 10. Anatomy of the abducens (CN VI) nerve. a) Axial T2 weighted image showing the paramedian course of the VIth nerves (yellow dotted lines) and the
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looping course of the VIIth cranial nerve (orange dashed arrows) around the VIth nerve nuclei; b) axial and c) sagittal T2 weighted steady state sequence showing the cisternal portions (arrows) of the VIth nerve.
Figure 11. Lateral eye movement disorders. a) Diagram showing the clinical features of internuclear ophthalmoplegia due to a lesion of the MLF, the lesion is on the side of adduction failure; b) lateral gaze palsy due to a lesion in the PPRF, the side of the lesion corresponds to the side of lateral gaze failure; c) ‘one and a half’ syndrome due to a lesion affecting both the MLF and PPRF, the side that can still abduct (albeit with nystagmus) is contralateral to the side of the lesion.
Figure 12. Clinical case of INO in a 40 yr old male. a) Axial T2 weighted image showing left paramedian hyperintensity in the dorsal pons; b) Axial DWI shows diffusion restriction; c) VCM demonstrates a small infarct in the longitudinal fibers; d) Axial T2 weighted image showing exotropia (left eye turned out) due to adduction failure from damage to the left MLF. The right eye is in a normal position.
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Figure 13. Aneurysmal compression of CN III and VI in a 60 year old male with ophthalmoplegia. a) Maximum Intensity Projection (MIP) of MR angiography shows aneurysm of the right internal carotid siphon; b) coronal T2 steady state image showing that the right CN III is compressed upward compared to the left side (arrows); c) the right CN III passes along the superior surface of the aneurysm (arrow).(Images courtesy of Dr. Mukai, Chiba University Hospital, Japan)
Figure 14. 6-year-old child with Möbius syndrome. a) and b) Axial T2 steady state image showing absent VIIth nerves (a) and VIth nerves (b) with only the VIIIth nerves visible bilaterally (arrows); c) axial T2 weighted steady state image showing bilateral esotropia (inturned eyes) due to abduction failure; d) axial T2 weighted image showing V-shaped depression in the fourth ventricular floor due to the absence of facial colliculi (arrows).
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