Академический Документы
Профессиональный Документы
Культура Документы
ABBREVIATION KEY
CN cranial nerve
MLF medial longitudinal fasciculus
PICA posterior inferior cerebellar
artery
MSA multiple system atrophy
DTI diffusion tensor imaging
ABSTRACT
We present a pictorial review of brain stem anatomy and vasculature at the level of the
midbrain, pons, and medulla by comparing multiple modalities, including MR imaging, dif-
fusion tensor imaging (DTI), color-coded presentation mapping, and diffusion tensor trac-
tography. This side-by-side comparison explored important nuclei and pathways, such as
the pyramidal tracts, transverse pontine fibers, medial longitudinal fasciculus, medial lem-
niscus, lateral lemniscus, and central tegmental tract. In addition, we introduced clinical case
examples, such as congenital anomalies, stroke, neoplasm, neurodegenerative disease, met-
abolic disease, and Wallerian degeneration. These clinical case examples helped solidify our
understanding of brain stem anatomy.
Learning Objectives: List brainstem tracts that can be elucidated with diffusion tractogra-
phy, and document their normal pathways.
anterior portion of the midbrain and gives the midbrain its tery and the posterior cerebral artery as the oculomotor
characteristic shape. Several tracts run in the cerebral pe- nerve or cranial nerve (CN) III. CN III continues through
duncle, including the frontopontine, pyramidal, and oc- the cavernous sinus, superior to the other cavernous CNs,
cipito-temporopontine tracts. The pyramidal tract passes and along the lateral aspect of the cavernous internal ca-
through the central portion of the cerebral peduncle. The rotid artery (ICA). It exits through the superior orbital fis-
frontopontine tract passes medial and the occipito-tem- sure and splits into the superior and inferior divisions.3,4,8,9
poropontine tract lies lateral to the cerebral peduncle. The superior division CN III innervates the superior rectus
Posterior to the cerebral peduncle, the tegmentum con- and levator palpebrae muscles and the inferior division of
tains the bulk of the midbrain nuclei and tracts, such as the the CN III innervates the medial rectus, inferior rectus, in-
substantia nigra, oculomotor nucleus, red nucleus, medial ferior oblique, and sphincter pupillae muscles. Compres-
longitudinal fasciculus (MLF), medial and lateral lemnis- sion of CN III by a posterior communicating artery aneu-
cus, and superior cerebellar peduncle decussation. The tec- rysms typically causes pupil-involving CN III palsy, which
tum, or the quadrigeminal plate, is composed of the supe- presents as diplopia, mydriasis, and ptosis. Microvascular
rior and inferior colliculi, which roughly divide the injury to the CN III leads to pupil-sparing CN III.10,11
midbrain into its upper and lower levels.1-6
Lower Midbrain
Upper Midbrain
Caudally, at the level of the inferior colliculus (Fig 2), the
The red nucleus and substantia nigra dominate the histol-
superior cerebellar peduncle decussation occupies the teg-
ogy as the 2 pigmented nuclei at the level of the superior
mental portion of the midbrain. These crossing fibers are
colliculus (Fig 1). The red nucleus is a round, pigmented
nucleus, which is located centrally within the midbrain teg- depicted in red as transverse fibers on DTI. The superior
mentum. It is an integral part of the Guillain-Mollaret tri- cerebellar peduncles are located posteriorly in the upper
angle and connects to the inferior olivary nucleus by the pons and serve as the main efferent pathway of the cerebel-
central tegmental tract. The substantia nigra is a 2-layer, lum. The superior cerebellar peduncle fibers arise from the
crescent-shaped structure located on each side of the mid- dentate nucleus, decussate in the midbrain at the level of the
brain, immediately posterior to the cerebral peduncle. It is inferior colliculus, and continue to the contralateral red
composed of the substantia nigra pars reticulata and the nucleus in the upper midbrain. Thus, infarctions of the cen-
substantia nigra pars compacta. Currently, these compo- tral midbrain tegmentum cause ataxia and can be seen in
nents of the substantia nigra cannot be differentiated under Claude and Nothnagel syndromes.1,10
conventional imaging techniques.1,3-5 Decreased volume of The trochlear nucleus lies posterior to the superior cere-
the substantia nigra has been associated in Parkinson dis- bellar peduncle decussation, between the periaqueductal
ease, Huntington disease, and multiple system atrophy gray and the MLF. The axons from the trochlear nucleus
(MSA).7 However, some studies contradict this theory that course posteriorly and inferiorly around the cerebral aque-
the substantia nigra decreases in Parkinson disease. duct. Once they cross the midline at the superior medullary
The oculomotor nucleus is located immediately posterior vellum, they exit as the trochlear nerve, or CN IV, along the
to the red nucleus in the midline between the MLF and the dorsal surface of the brain stem, just caudal to the inferior
periaqueductal gray. It is an ovoid structure composed of colliculus. CN IV courses laterally through the ambient
the principal oculomotor nucleus, caudal central oculomo- cistern on gross anatomic specimens. However, its cister-
tor nucleus, nucleus of Perlia, and accessory oculomotor nal course is difficult to identify on imaging due to its
nucleus of Edinger-Westphal.1 The neurons of the oculo- small diameter and the adjacent superior cerebellar ar-
motor nucleus extend their axons anteriorly through or tery and brachial branches of the precentral cerebellar
medial to the red nuclei. They exit the midbrain at the vein. CN IV innervates the superior oblique muscle, and
interpeduncular cistern between the superior cerebellar ar- lesions that involve this nerve may lead to vertical diplo-
Fig 4. Lower pons. (A) Myelin-stained specimen labeled with the major anatomic structures of the lower pons at the level of the middle cerebellar
peduncles, including the pyramidal tract, medial lemniscus, lateral lemniscus, MLF, spinothalamic tract, and central tegmental tract. (B) T2-weighted
MR image at this level, with an overlay of a functional map of the brain stem. (C) DTI at this level, with labeling of important anatomic landmarks.
function, and arousal. The median zone is formed by the addition, CNs VII and VIII exit along the posterolateral
raphe nuclei, a group of serotonergic neurons, which send aspect of the basis pontis and pass through cerebellar pon-
axons to the forebrain and the spinal cord.1,2,4 tine angle and into the internal auditory canal.
The sensory pathways continue their course through the
pons. The medial lemniscus passes anterior to the superior MEDULLA
cerebellar peduncle, and the lateral lemniscus travels lateral The medulla is the caudal portion of the brain stem (Figs 5,
to the superior cerebellar peduncle. In the posterior tegmen- 6), which is separated from the pons by the pontomedullary
tum, the MLF courses posterior to the reticular formation sulcus. On gross examination, the pyramidal tracts are vis-
and the central tegmental tract descends posterolateral to ible along the ventral margins of the upper medulla and
the reticular formation. The central tegmental tract is an decussate in the lower medulla at the bulbospinal level. The
extrapyramidal tract that connects the red nucleus to the inferior olivary nucleus complex is an olive-shaped nucleus
interior olivary nucleus and consists of 3 pathways: pallido- within the anterolateral medulla. It dominates the histo-
olivary, rubro-olivary, and reticulo-olivary fibers.1,13 It is logic landscape of the upper medulla. This undulating com-
one of the first regions to myelinate and demonstrates sen- plex is composed of 3 nuclei, the principal, medial, and
sitivity to severe asphyxiation of infants.15 dorsal nuclei, and plays a vital role in the Guillain-Mollaret
triangle.
Lower Pons: At the Level of the Middle Cerebellar The hypoglossal nucleus is immediately anterior to the
Peduncle fourth ventricle. Multiple rootlets arise from this nucleus
The lower pons (Fig 4) is also divided into the basis pontis and combine to form CN XII. Hypoglossal nerves cross the
and the pontine tegmentum. Posteriorly, the middle cere- lateral cerebellomedullary cistern and exit through the hy-
bellar peduncles form the major afferent pathway between poglossal canal. CN XII innervates the genioglossus, hypo-
the cerebrum, brain stem, and cerebellum. Its fibers origi- glossus, and styloglossus muscles. Lesions in the hypoglos-
nate along the anterolateral border of the basis pontis in the sal nucleus cause deviation of the tongue toward the
upper pons and wrap around the lateral aspect of the lower ipsilateral side.1,5,8
pons. The middle cerebellar peduncle axons run in the an- The vagus nucleus is a complex set of nuclei located
teroposterior direction and are green on the DTI map. In along the posterolateral aspect of the upper medulla, lateral
Fig 6. Medulla at the pyramidal tract decussation. (A) Myelin-stained specimen labeled with the major anatomic structures of the lower medulla at the
level of the pyramidal tract decussation, including the CN/CF (cuneate nucleus/cuneate fasciculus), GN/GF (gracile nucleus/gracile fasciculus),
spinotrigeminal nucleus, and MLF. (B) T2-weighted MR image at this level, with an overlay of a functional map of the brain stem. (C) DTI at this level,
with labeling of important anatomic landmarks.
Neuronal Pathways
Fig 7. Brain stem diffusion tensor tractography. (A, B) Anteroposterior
As we describe in the following section, multiple motor and
and lateral views of diffusion tensor tractography of the brain stem illus-
trate the pyramidal tracts in blue, transverse pontine bers in red, and sensory tracts run through the brain stem. The complex
the middle cerebellar peduncles in green. array of these tracts and their directionality can be visual-
ized with diffusion tractography (Fig 7).
to the CN XII nucleus. The dorsal motor nucleus of the
vagus is located lateral to the hypoglossal nucleus and re- Motor Pathway. The pyramidal tract is one of the main
ceives fibers from the hypothalamus, nucleus of the tractus descending pathways in the brain stem. The cell bodies of
solitarius, and the main sensory nucleus of CN V. Lesions these neurons originate from layer V of the motor cortex or
that involve the dorsal motor nucleus of the vagus cause other nearby cortical areas. They descend through the pos-
swallowing difficulties.1,3,5 terior third of the posterior limb of the internal capsule and
The vestibular nuclei can be found between the vagus enter the brain stem via the central portion of the cerebral
nucleus and the inferior cerebellar peduncle, extending peduncle (Fig 8). From there, the axons pass through the
central portion of the ventral pons to the anterior surface of lamic tract neurons ascend through the caudal medulla,
the medulla and form the medullary pyramids. Approxi- rostral pons, the rostral midbrain, and the ventral postero-
mately 75%90% of these fibers cross at the pyramidal lateral nucleus of the thalamus (Fig 9). At the level of the
decussation to form the lateral cortical spinal tract. Those brain stem, these fibers also give off collateral connections
fibers that do not cross form the anterior cortical spinal to the reticular formation. These spinothalamic tract fibers
tract on both sides of the anterior medial fissure. A very few transmit pain and temperature information. The posterior
numbers of fibers descend in the ipsilateral lateral column-medial lemniscus pathway carries tactile and pro-
column.1-3,5 prioceptive information. Axons from the posterior column
of the spinal cord synapse onto neurons in the gracile and
Pain-Temperature and Tactile-Proprioception. The sen- cuneate nuclei, which are organized somatotopically. Sec-
sory pathway includes the spinothalamic tract and the pos- ondary neurons cross the midline at the caudal aspect of the
terior column-medial lemniscus pathway. The spinotha- dorsal medulla and ascend through the dorsal brain stem as
Fig 13. Medial longitudinal fasciculus syndrome. Axial T2 (A) and dif-
Fig 14. Dysarthria clumsy hand syndrome. Axial T2 (A) and diffusion-
fusion-weighted images (B) through the midbrain illustrate restricted
weighted images (B) through the upper pons depicts restricted diffusion
diffusion and faint T2 hyperintensity in a region of the right MLF.
and T2 hyperintensity in the left ventral pons in the region of the corti-
cospinal tract and transverse pontine bers.
tract are vital components of the triangle of Guillain
and Mollaret, which allows for motor learning. The
Vascular Supply
dentate nucleus (Fig 11) sends information through the
The vertebrobasilar system supplies blood to the brain
superior
stem. The vertebral arteries originate as the first branches of
cerebellar peduncle and superior cerebellar peduncle de-
the right and left subclavian arteries, and may be unequal in
cussation to the contralateral red nucleus. This informa- size as they ascend in the transverse foramina. The intra-
tion then travels downward through the central tegmen- dural segments of the vertebral arteries give off the posterior
tal tract to the inferior olivary nucleus, where inferior cerebellar arteries (PICA). Occasionally, the PICAs
comparisons between the intended and achieved move- can originate from the vertebral artery below the level of the
ments are made. Based on this discrepancy, correcting foramen magnum. At the level of the pontomedullary junc-
movements are made through the climbing cerebellar fi- tion, the right and left vertebral arteries join to form the
bers. Other fibers from the red nucleus end in the ventral basilar artery. The penetrating paramedian and circumfer-
lateral nucleus of the thalamus. Fibers from the inferior ential perforator branches arise from the dorsal aspects of
olivary nucleus cross the midline and pass through the the basilar artery. The superior cerebellar artery and poste-
inferior cerebellar peduncle on their way to the dentate rior cerebral artery are seen at the distal portion of the
nucleus.1,4 basilar artery.1
Fig 17. MSA. (A) DTI images of the lower pons at the level of medial
cerebellar peduncles demonstrate atrophy of the transverse pontine -
bers (red), and middle cerebellar peduncles. (B, C) T2-weighted MR im-
ages of the lower pons at the level of the middle cerebellar peduncles
demonstrate the hot cross bun sign typically seen within the pons. (D)
T2-weighted image at the level of the basal ganglia demonstrates T2
hyperintensity in the left lateral putamen.
At the level of the midbrain (Fig 12A, -B), there are 4 PATHOLOGY
vascular territories, including the anteromedial, anterolat- After a detailed review of brain stem anatomy and vascula-
eral, lateral, and posterior territories. The anteromedial ture, we reviewed a few general cases to illustrate the im-
vascular territory vessels arise from the posterior cerebral portance of functional anatomy and the role that DTI plays.
artery at the interpeduncular fossa. The anterolateral ves-
sels originate from the posterior cerebral artery or the an- Strokes
terior choroidal artery. The lateral territory vessels arise Infarctions of the brain stem typically have good clinical-
from the collicular, choroidal, or PICA. The posterior zone anatomic correlation. For example, an infarction that in-
is supplied by the superior cerebellar, collicular, and the volves the posterior midline midbrain leads to MLF syn-
posteromedial choroidal arteries. drome, characterized by ipsilateral downward gaze and
At the level of the upper pons (Fig 12C), there are 4 vertical eye movement paralysis (Fig 13).13 Dysarthria-
vascular territories, including the anteromedial, anterolat- clumsy hand syndrome occurs when an infarction involves
eral, lateral, and posterior territories. In the lower pons (Fig the cortical spinal tract and ventral transverse pontine fi-
12D), there are 3 vascular territories, including the antero- bers. This lesion leads to mild ipsilateral clumsiness without
medial, anterolateral, and lateral territories. The anterome- frank weakness and contralateral dysmetria, dysrhythmias,
dial region is supplied from the pontine perforating arteries, and dysdiadochokinesia as well as truncal and gait ataxia
which arise from the basilar artery. The anterolateral seg- (Fig 14).
mental arteries arise from the AICA at the pontomedullary Wallenberg syndrome, also known as lateral medullary
sulcus. The lateral zone vessels originate from the lateral syndrome, occurs when an infarction in the posterolateral
pontine perforators, AICA, or the superior cerebellar medulla involves the spinothalamic tract, central tegmental
artery.1 tract, inferior cerebellar peduncle, vestibular nuclei, and
At the level of the medulla oblongata (Fig 12E, -F), there spinotrigeminal nucleus. The symptoms include ataxia, loss
are 4 vascular territories including the anteromedial, an- of pain and temperature sensation (ipsilateral face or con-
tralateral body), vertigo, dysphagia, dysarthria, and nystag- tegmentum, substantia nigra, red nucleus, and globus pal-
mus. In addition, Horner syndrome is found in 91% of lidus. The signs and symptoms include supranuclear verti-
these patients. Wallenberg syndrome is often seen in the cal gaze palsy, pseudobulbar palsy, dystonic rigidity of the
setting of vertebral artery dissections (Fig 15).16 neck and upper extremities as well as frequent falls. As with
Dejerine syndrome, also called medial medullary syn- MSA, progressive supranuclear palsy is clinically difficult to
drome, is a rare infarction in the medial medulla, which differentiate from Parkinson disease and imaging plays a vital
involves the medullary pyramid, medial lemniscus, and hy- role in its diagnosis. On sagittal T1-weighted images, the brain
poglossal nerve. These infarctions are typically due to oc- stem takes on the appearance of a hummingbird due to the
clusion of the anterior spinal artery. The symptoms include reduced number of superior cerebellar peduncle decussation
contralateral upper and lower extremity weakness, vibra- fibers, which decreases the anteroposterior diameter of the
tory and proprioceptive sensory loss, ipsilateral tongue midbrain (Fig 18). Axial T1-weighted images of the upper
weakness, and atrophy (Fig 16).16 pons also demonstrate atrophy of the superior cerebellar pe-
duncles. DTI also clearly shows loss of the superior cerebellar
Neurodegenerative Disorders peduncle decussation in the midbrain.19
MSA is a sporadic, adult-onset, progressive neurodegenera-
tive disease that leads to neuronal loss and gliosis of the Transneuronal Degeneration
inferior olives, pons, cerebellum, substantia nigra, locus Inferior olivary hypertrophy is a form of transneuronal de-
coeruleus, striatum, and intermediolateral column of the generation caused by a lesion in the Guillain-Mollaret tri-
spinal cord. The types of MSA include MSA with parkin- angle. For example, focal hemorrhage in the pontine teg-
sonism, MSA with cerebellar predominant features, and mentum that involves the central tegmental tract leads to T2
Shy-Drager syndrome with autonomic failure. In MSA, ax- hyperintensity in the anterior medulla, which represents
ial T2-weighted images demonstrate the hot cross bun edema and atrophy of the downstream ipsilateral inferior
sign or a cross-shaped hyperintensity in the pons, which is
olivary nucleus (Fig 19). These patients rarely present with
created by selective loss of myelinated transverse pontocer-
palatal myoclonus but are often asymptomatic.20
ebellar fibers in the pontine raphe (Fig 17). In approxi-
mately 80% of cases, it can be difficult to clinically differ-
entiate from Parkinson disease and even respond to Congenital
levodopa during its initial stages. DTI can help discriminate Joubert syndrome is a rare, autosomal, recessive, congenital
between MSA and Parkinson disease based on apparent disorder with symptoms, including hypotonia, ataxia, devel-
diffusion coefficient. In addition, the middle cerebellar pe- opmental delay, mental retardation, irregular breathing, and
duncle width is significantly reduced in patients with MSA ocular motor apraxia. Axial MR images of brain stem dem-
compared with those with Parkinson disease. The hot cross onstrate elongated superior cerebellar peduncles and a deep
bun sign is not specific for MSA, however, and also may be interpeduncular cistern (Fig 20). The DTI sections clearly dem-
seen in patients with spinocerebellar ataxia.17,18 onstrate loss of the corticospinal tract decussation.21
Progressive supranuclear palsy is a rare neurodegenera- Horizontal gaze palsy and progressive scoliosis is a rare,
tive disease characterized by neuronal loss in the midbrain autosomal recessive mutation of the ROBO3 gene, which
CONCLUSION
The brain stem is a complex structure that contains multiple
nuclei and tracts that are vital to our everyday activities but
that are not well understood. A detailed understanding of
Fig 19. Inferior olivary hypertrophy. (A) Axial T2-weighted MR imaging
the brain stem may be attained through a comparison of
at the level of the upper pons demonstrates hemorrhage (*) in the left myelin-stained specimens, MR images, and DTI images.
pontine tegmentum in the region of the left central tegmental tract. (B) This knowledge of functional brain stem anatomy and vas-
Axial T2-weighted image through the upper medulla demonstrates a cular territories plays a critical part in accurately describing
normal inferior olivary nucleus at the time of hemorrhage. (C) The brain stem lesions and in understanding the dysfunction
6-month follow-up T2-weighted MR imaging at the level of the upper
pons demonstrates expected evolution of the blood products. (D) The
that they cause.
6-month follow-up axial T2-weighted MR imaging at the level of the in-
ferior olivary nucleus demonstrates T2 hyperintensity and enlargement REFERENCES
of the left inferior olivary nucleus due to transneuronal degeneration. 1. Naidich TP, Duvernoy HM, Delman BN, et al. Duvernoys
From Ref. 21, reproduced with permission. American Society of
Atlas of the Human Brain Stem and Cerebellum. NY:
Neuroradiology.
Springer-Verlag; 2009
2. Kandel E, Schwartz JH, Jessell T. Principles of Neural Science.
NY: McGraw Hill; 2000
3. Schuenke M, Schulte E, Schumacher U. Thieme Atlas of
Anatomy: Head and Neuroanatomy. Stuttgart, Germany:
Verlag, 2010
4. Nieuwenhuys R, Voogd J, van Huijzen C. The Human Cen-
tral Nervous System. NY: Springer-Verlag; 2008
5. Grossman RI, Yousem DM. Neuroradiology: The Requisites.
St Louis: Mosby; 1994:50 109
6. Haines DE. Neuroanatomy an atlas of structures, sections, and
systems. Baltimore: Lippincott Williams and Wilkins; 2004
Fig 20. Joubert syndrome. (A) Axial T1-weighted MR imaging at the level 7. Oikawa H, Sasaki M, Tamakawa Y, et al. The substantia
of the upper pons demonstrates the elongated superior cerebellar pe- nigra in Parkinson disease: proton density-weighted spin-echo
duncles (SCP), which produce the characteristic molar tooth sign seen in and fast short inversion time inversion-recovery MR findings.
Joubert syndrome. (B) Axial DTI at the level of the pontomesencephalic AJNR Am J Neuroradiol 2002;23:174756
pontomedullary junction demonstrates deepening of the interpeduncu- 8. Sheth S, Branstetter BF IV, Escott EJ. Appearance of normal
lar cistern and elongated, horizontally oriented SCP bers, as indicated cranial nerves on steady-state free precession MR Images.
by the green color.
Radiographics 2009;29:104555. 10.1148/rg.294085743
9. Blake PY, Mark AS, Kattah J, et al. MR of oculomotor nerve
leads to horizontal gaze palsy and progressive scoliosis, as palsy. AJNR Am J Neuroradiol 1995;16:166572
its name implies. Axial and sagittal MR images of the brain 10. Miller MJ, Mark LP, Ho KC, et al. Anatomic relationship of
stem demonstrate flattening of the basis pontis, hypoplasia the oculomotor nuclear complex and medial longitudinal fas-
ciculus in the midbrain. AJNR Am J Neuroradiol 1997;18:
of the pontine tegmentum, and the split pons sign. DTI
11113
demonstrates the absence of midpontine transverse pontine 11. Wakana S, Jiang H, et al. Fiber tract-based atlas of human
fibers and loss of the corticospinal tract decussation.22 white matter anatomy. Radiology 2003;230:77 87
12. Yousry I, Moriggl B, Dieterich M, et al. MR anatomy of the
Neoplasm proximal cisternal segment of the trochlear nerve: neurovascular
Brain stem gliomas are a heterogeneous group of tumors, relationships and landmarks. Radiology 2002;223:3138
most commonly found in children. The most common brain 13. Frohman TC, Galetta S, Fox R, et al. Pearls & Oy-sters: The