Arteries that leave the circle of Willis in the direction of their cortical irrigation zones, give branches to deep brain structures on the way. These branches are the mature result of leptomeningeal branches that penetrate the brain as early intrinsic vessels. When such an artery is occluded by meningitis or embolism for instance, limited (lacunar) infarction affects deep grey matter or juxtaventricular white matter. In the acute stage this presents on cranial ultrasound as a more or less rounded hyperechoic lesion with a clear border, to be differentiated from haemorrhage, abscess, tumor or dysplastic lesions. Such unidentified echobright object (UBO) can be referred to as perforator stroke when the context (often sick neonates with indwelling venous line) and the arterial anatomy templates are compatible with such diagnosis. The lesions remain hyperechoic for weeks and some cavitate, others just seem to shrink. Knowledge of arterial anatomy is essential in understanding UBOs in general and certainly for deep grey matter and the hindbrain.
1 internal carotid artery
2 posterior communicating artery
3 basilar artery
4 tuberothalamic artery (polar a., premammillary a.): to anteromedial and anterolateral thalamus including mammillothalamic tract, TRN
5 paramedian pedicle (thalamic perforator aa.): to posteromedial thalamus and subthalamus
6 thalamogeniculate aa.: to ventrolateral thalamus, lateral mammillary bodies
7 medial posterior choroidal a.: to posterior (pulvinar and geniculates) and anteromedial thalamus (part of anterior nucleus)
8 posterior cerebral artery
9 internal cerebral vein
10 basal vein
11 Heubner’s artery
12 anterior choroidal artery
13 anterior cerebral artery
14 middle cerebral artery
15 lenticulostriate perforator from MCA
Perinatal Perforator Stroke: Graphical Guide
14 Centrum Semi-ovale Stroke
15 Hypothalamic Artery Stroke
Perinatal Perforator Stroke: Branches from the MCA
Perinatal Perforator Stroke: Heubner’s Artery from the ACA
Coronal and parasagittal views — day 2 — <——— Heubner’s recurrent artery
A typical perforator stroke is Heubner’s artery stroke. Heubner’s artery stroke is recognized as a focal lesion in the lateral, anterior caudate head in front of the foramen of Monro. Heubner’s artery, large in the late fetal and perinatal period because of its contribution to matrix perfusion, seems to be a common route for emboli. In children with this type of stroke, contralateral upper limb dystonia has been reported. An important perforator from the anterior communicating artery, the subcallosal artery, perfuses columna fornicis and anterior commissure, leading to basal forebrain amnesia when this territory in infarcted in the adult (no neonatal reports).
The recurrent branch of the ACA, first described by Heubner in 1874, is unique in that it doubles back on its parent vessel. It is the largest branch from the Al or the proximal A2 segment in nearly all brains. It may emerge from the superior surface of A1 at some point between the most medial and lateral portion of the anterior perforated substance, and it may occasionally arise from the ICA at its bifurcation, from the MCA or even from the ACoA. By Perlmutter and Rhoton in 1976 it was found to have its origin from the A2 segment in 78%, from the A1 segment in 14% and at the level of the ACoA in 8%. Most recurrent arteries course anterior to the AI segment but 4/10 course superior to it, under the anterior perforated substance. The recurrent artery enters the brain as a single trunk without branching in around 1/7, it has an average number of branches of 4, but it may have as many as 12 branches. Branches terminate in the anterior perforated substance (4/10), in the Sylvian fissure lateral to the anterior perforated substance (4/10), in inferior surface of the frontal lobe (2/10) and terminated sometimes in descending order of frequency in the inferior frontal area lateral to the olfactory sulcus, the olfactory sulcus and the gyrus rectus. The branches supply the anterior part of the caudate nucleus, the anterior third of the putamen, the tip of the outer segment of the globus pallidus, and the anterior limb of the internal capsule. Constant but few vessels are found in the putamen and anterior hypothalamus but also to a variable degree in the uncinate fasciculus and the olfactory regions. During surgery the medial striate artery of Heubner may be confused with the orbitofrontal artery, which is typically the second major branch of the A2 segment.
Occlusion of Heubner’s artery may cause hemiparesis with brachial predominance due to infarction of the anterior limb of the internal capsule, and aphasia if the artery is on the dominant side. Involvement can cause paralysis of the face, palate and tongue. In the majority these deficits tend to resolve over weeks or months.
A particular variant (and remnant) of Heubner’s artery is the axoid artery: this vessel (remaining a feeder for piriform cortex) arises from the ACA but folllows the M1 MCA to the limen insulae; it has also been called accessory MCA.
32w GA, acceptor in twin anaemia-polycythaemia sequence; striatal arteriopathy plus Heubner’s artery stroke; associated hyperechoic change in germinal matrix in the caudothalamic groove.
Perinatal Perforator Stroke: Medial Posterior Choroidal Artery from the PCA
Tuberothalamic artery (Plets et al. 1970, Percheron 1976 and 1977, Gibo et al. 2001, Cosson et al. 2003, Abels et al. 2006, Kim et al. 2008, ten Donkelaar 2011).
Seven to ten perforating branches arise from the posterior communicating artery. The largest branch is the premammillary artery (anterior thalamoperforating or tuberothalamic artery). These perforating branches vascularize the anterior or tuberothalamic territory: the posterior part of the optic chiasm, the optic tract, the posterior part of the hypothalamus with the mammillary body, and the anterior nucleus, the polar part of the ventral anterior nucleus and the reticular nucleus of the thalamus. Variations of the pre-mamillary artery are rare. The artery rises in the direction of thalamus, has few side branches before it ramifies in the area of anterior thalamus. The tuberothalamic artery is usually a single vessel and less frequently double; it arises almost always from the PCoA, rarely from PCA. Anastomoses involve the extracerebral segment in slightly less than half. In adults isolated tuberothalamic artery infarction is rare and mostly because of small vessel occlusion. Patients with coexisting other infarctions usually have an embolic source.
Unexpected finding at discharge of preterm of 35w PMA: lesion in anterolateral superior thalamus; long straight artery arising from the PCoA
Perinatal Perforator Stroke: Tuberothalamic (Premammillary) Artery from the PCoA
Perinatal Perforator Stroke: Thalamogeniculate Artery from the PCA
Lesion in part ischaemic and haemorrhagic. Preterm of 31 weeks GA, with cardiac tamponnade due to atrial perforation by percutaneous silastic catheter; hypotension and acidosis with bradycardia led to non-cystic leukomalacia and asymmetrical posterior thalamic infarction compatible with occlusion of thalamogeniculate perforators from the PCA; pulvinar is also affected. Straight borders typical of arterial infarction.
Perinatal Perforator Stroke: Anterior Choroidal Artery from the ICA
Newborn girl with shock from E Coli urosepsis on day 4; incidental sonographic finding on day 5; left forearm partial ischaemia (MR in the second week of life). Parasagittal view.
Anterior choroidal artery (Takahashi et al. 1994, Abels et al. 2006, ten Donkelaar 2011).
The inferior choroidal point, the inferior termination of the choroidal fissure, is located immediately behind the uncus, below and slightly anterior to the lateral geniculate body of the thalamus, and it is just anterior to the site where the anterior choroidal artery enters the temporal horn and where the inferior ventricular vein exits the temporal horn to join the basal vein of Rosenthal. After arising from the supraclinoid segment of the internal carotid artery, the anterior choroidal artery initially courses posteriorly, superiorly, and medially in the carotid cistern, and then continues medial to the anteromedial surface of the uncus to reach the optic tract superolateral to the posterior communicating artery; at this point, it diverges from the posterior communicating artery and courses posteriorly, superiorly, and laterally, under the optic tract, to enter the crural cistern between the superior part of the posteromedial surface of the uncus and the crus cerebri; after passing the posterior edge of the intralimbic gyrus, it enters the temporal horn of the lateral ventricle through the choroidal fissure.
Branches:
proximal branches to optic tract, crus posterius capsulae internae and pallidum mediale
distal branches to optic radiation and lateral geniculate
plexus segment for plexus of temporal horn
AChA infarction is reported in the newborn. A hyperechoic lesion is seen between pallidum and thalamus, covering the middle and lower part of the posterior limb of the internal capsule (PLIC). Because lower limb corticospinal fibers course more posteriorly through PLIC, leg monoplegia can be the sequel. Extensive infarction involves pial areas near the optic tract. The consequences of occlusion of the AChA in adults can be contralateral hemiplegia, hemianesthesia and hemianopia (Foix et al. 1925, Abbie 1933 hence Abbie’s syndrome). The contralateral hemiplegia results from infarction in the posterior two thirds of the posterior limb of the internal capsule and the middle third of the cerebral peduncle; the hemianopia from involvement of the optic radiation, the optic tract or part of the lateral geniculate body. The acoustic radiation can also be involved. The visual symptoms of stroke in adults may thus involve pre- and postgeniculate signs. To the classical clinical syndrome of hemimotor, hemisensory and visual field deficit have been added hemiataxia, acute pseudobulbar mutism, pure motor and pure sensory syndromes and disorders of higher cortical function: CT-MRI findings revealed an unexpected superior extension of infarct to include the periventricular caudate nucleus and inferior corona radiata (Helgason 1988). Apparent higher cortical dysfunction may also be consequent to involvement of thalamic nuclei.
Typical AChA stroke areas
Lacunar infarcts in adults are commonly found in the basal ganglia. Microvascular territories of the lenticulostriate arteries, the recurrent artery of Heubner, the anterior choroidal artery, and striate branches of the anterior cerebral and anterior communicating arteries can be examined in perfusion-fixed human brains by simultaneous injection of fluorescent dyes and a radio-opaque substance in 5% gelatin (Feekes et al. 2005). Territories are defined by ultraviolet illumination of dye and high-resolution mammography of radio-opaque substances. Brains are sectioned coplanar with the Talairach proportional grid system. The lenticulostriate artery, recurrent artery of Heubner, and anterior choroidal artery supply distinct territories of the basal ganglia with minimal overlap and sparse anastomoses between major perforators. Individual territories are spatially consistent across brains and match the extent of major/minor infarcts. No significant asymmetries are noted between right and left hemispheres.
The recurrent artery of Heubner (RAH) penetrates at the anterior perforated substance and supplied much of the anterior and ventral portions of the basal ganglia, including the caudate, putamen and internal capsule up to the anterior commissure. With the exception of a few arterioles, Heubner’s artery does not supply the basal forebrain and instead consistently outlines the dorsal and lateral borders of the nucleus accumbens.
The medial and lateral lenticulostriate arteries (LSA) also penetrate the anterior perforated substance but supplied most of the rostrocaudal extent of the basal ganglia, particularly along the lateral and dorsal aspects, forming a fan shaped wedge in both rostrocaudal and mediolateral directions. The lenticulostriate territory extends into the external globus pallidus in addition to the caudate, putamen, and internal capsule.
The anterior choroidal artery (AChA) supplies regions posterior of the anterior commissure, including the internal globus pallidus, tail of the caudate nucleus, and posterior aspects of the basal forebrain, but does not supply much of the basal ganglia. The medial striate branches of the ACA and ACoA do not contribute much to the basal ganglia with the exception of small branches ventromedial to those of Heubner’s artery.
Perinatal Perforator Stroke: History and Variants of the Recurrent Artery of Heubner
Perinatal Perforator Stroke: The Anterior Choroidal Artery
Perinatal Perforator Stroke: The Medial Posterior Choroidal Artery
after ten Donkelaar 2011
Perinatal Perforator Stroke: Perfusion of Thalamus, Arteries and Veins
The thalamus is vascularized by perforating branches of the posterior communicating artery, thalamoperforating and thalamogeniculate branches as well as the posterior choroidal arteries. These perforating branches supply the following structures (with summary of clinical findings in adults in case of stroke):
Seven to ten perforating branches arise from the posterior communicating artery. The largest branch is the premammillary artery (anterior thalamoperforating or tuberothalamic artery). Polar (tuberothalamic) artery syndrome: apathy, amnesia (inability to make new memories).
The thalamoperforating branches (or posteromedial central arteries) arise from the P1 segment and penetrate the posterior perforated substance. They supply the paramedian territory: the medial nuclei, the intralaminar nuclei, part of the dorsomedial nucleus, the posteromedial part of the lateral nuclei and the ventromedial pulvinar of the thalamus. Thalamic-subthalamic syndrome (perforator aa.): hypersomnolence (arousal problems, inertia), disturbed vertical gaze, amnesia, disorientation, abnormal movements like asterixis, tremor or dystonia.
The thalamogeniculate branches usually arise from the distal P2 segment of the PCA. They supply the inferolateral territory: the major part of the lateral side of the caudal thalamus including the rostrolateral part of the pulvinar, the posterior parts of the lateral nuclei and lateral dorsal nucleus, and the ventral posterior and ventral lateral nuclei. Lateral thalamic syndrome (thalamogeniculate aa.): pure hemisensory stroke, hemi-sensorimotor stroke, abnormal movements with hemisyndrome (thalamic syndrome, dystonia like the thalamic hand).
The posterior choroidal artery usually has one or two medial and one to six lateral branches. The medial branch supplies the medial geniculate body and the posterior parts of the medial nucleus and the pulvinar of the thalamus. Posterior choroidal aa. syndrome: visual field defects, mild hemisyndromes, visual hallucinations, dystonic movements, amnesia.
Recognition of these thalamic specific arterial stroke entities is only beginning in the neonatal literature.
Perinatal Perforator Stroke: P1 Median Thalamic Artery from the PCA
Embolism during exchange transfusion, for hyperbilirubinaemia in a term infant, on a venous umbilical catheter: most likely embolus broken down at the top of the basilar artery; this has all characteristics of Percheron artery stroke (PCA P1 perforators occluded on both sides due to branching from a common stem) (Bain et al. 2009).Preterm 34w, umbilical venous catheter only risk factor: right and left medial P1 perforator artery stroke; right superior cerebellar artery stroke; right PCA stroke.
Perinatal Perforator Stroke: Textual Description
PCA perforator stroke: The PCA takes a horizontal course in a wide arc around the crus cerebri, until it reaches the lateral mesencephalic sulcus. Here it turns lateral and posterior to follow the inner border of the hippocampal gyrus, and then it divides into two branches, one following the parieto-occipital and the other the calcarine sulcus. Around the brain stem the PCA gives off a series of side branches subdivided into two groups, branches from the crural part (of interest here), and those from the distal cortical part. The branches from the crural part are deep penetrating vessels (perforating or choroidal).
First, there are the arteriolae retromammillares which are divided in an anteromedial and a posteromedial group.
The anteromedial group supplies the median-posterior part of the mammillary bodies; to them belong the aa. perforantes thalami which vascularize the median anterior part of thalamus, the superior part of nucleus ruber, the median part of subthalamic nucleus, the posterior part of hypothalamus and the superior part of the brachia conjunctiva. The posteromedial group supplies the middle part of the crus cerebri after having perforated the intercrural substantia perforata.
The a. quadrigemina arises close to the origin of the PCA, just medial to the point where the posterior communicating artery joins the latter. It forms a pericrural arc. In the transverse sulcus of the lamina quadrigemina it gives off an anterior branch for the superior colliculus and a posterior branch for the inferior colliculus. Further, during its course it gives off some branches to the anterior part of the lateral side of the crus cerebri.
The thalamogeniculate arteries usually arise just beyond the point where the posterior communicating artery joins the posterior cerebral artery. They are 5 or 6 thin branches penetrating into posterior thalamus, to supply the medial and lateral geniculate bodies, the lower half of the nucleus lateralis thalami, the lateral part of the pulvinar and also the median part of the crus occipitale of the internal capsule.
ACA perforator stroke: The basilar side branches of the anterior cerebral artery (ACA) are the aa. striatae mediales, three or four very thin branches perforating directly the substantia perforata. One of them stands out by a wider caliber: the a. recurrens of Heubner. The level of its origin varies in relation to the anterior communicating artery. This recurrent artery runs in a lateral and dorsal direction, gives off a fine branch for the tuber olfactorium and finally penetrates into the lateral part of the anterior substantia perforata. It perfuses anterior and inferior caudate head, tip of lateral globus pallidus and the medial part of the anterior limb of the internal capsule. A particular variant (and remnant) of Heubner’s artery is the axoid artery: this vessel (remaining a feeder for piriform cortex) arises from the ACA but follows the M1 MCA to the limen insulae; it has also been called accessory MCA. In many cases the anterior communicating artery gives off one or two fine perforating branches, joining the aa. striatae mediales of the ACA. There may be a medial anterior cerebral artery ascending from the ACoA in a direction opposite the perforators.
Anterior choroidal artery branches and stroke:
proximal branches to optic tract, crus posterius capsulae internae and pallidum mediale
distal branches to optic radiation and lateral geniculate
plexus segment for plexus of temporal horn
Templates for perforator stroke (the artery occluded is not a cortical branch but a perforator artery stemming from the proximal parts of the circle of Willis arteries) can mimic templates of haemorrhage from thrombosis in one of the veins drained by the internal cerebral or basal vein. References to ultrasound are in Abels et al. 2006, de Vries et al. 1992 and 1997, van Wezel-Meijler et al. 1999. Descriptions of long-term outcome after neonatal perforator stroke are totally absent.
Centrum semi-ovale stroke: Focal ischaemic infarction is occasionally encountered within the centrum semi-ovale immediately next to the lateral ventricle. Context and imaging are often indicative of an embolic ischaemic lesion. Focal arterial infarction in a terminal lateral striatal MCA branch is a likely possibility. The alternative explanation would be a stroke of one ventriculopetal cortical arterial branch of the ACA, MCA or PCA but with the occlusion away from the surface as it courses in white matter.
PCoA perforator stroke: The posterior communicating artery (PCoA) runs beneath the optic tract and above the oculomotor nerve, and joins the PCA at a small distance from the division of the basilar artery. Five to six small arteries arise from the PoCA, participating in the vascularization of the floor of the third ventricle (hypothalamic nuclei), and of the supero-anterior part of the medial thalamic nuclei. A lateral branch, the premammillary (or tuberothalamic) artery, irrigates the caudal hypothalamus, the medial subthalamus (the substantia nigra, Forel’s field and the zona incerta), and a rostral portion of the thalamus (the ventral part of the anterior group of nuclei, the ventral anterior nucleus, the rostral part of the midline and reticular thalamic nuclei, as well as the rostral part of the mediodorsal nucleus). Finally, peduncular branches nourish the ventromedial part of the rostral crus cerebri.
MCA perforator stroke: Many striate perforators arise from the MCA. A medial group supplies the lateral segment of globus pallidus and the upper and middle part of the caudate head. The lateral striate arteries are often 7-9 fine branches arising from the first part of the M1 segment, also called aa. putamino-capsulo-caudatae: they supply anterior putamen, the anterior part of the internal capsule, the corpus and the upper and lateral part of the caput nuclei caudati.
The posterior choroidal arteries are usually double and originate separately or via a common stem. They also curve around the crus cerebri. The first, the a. choroidea posterior medialis, takes a postero-anterior course towards the pineal body, to which it gives off some small branches; it diminishes in size in the choroid plexus of the third ventricle. The second, the a. choroidea posterior lateralis gives two end branches. One follows the median part of the upper side of the thalamus, the supero-medial part of which it irrigates. The other reaches the choroid plexus of the lateral ventricle opposite the lateral part of the pulvinar. It also vascularizes the posterior part of the caudate nucleus. During their ascending course the posterior choroidal arteries give off small branches entering the median part of the pulvinar.
Pial arterial and venous stroke due to meningitis ——>Term, early onset GBS meningitis (courtesy dr Arnaez-Solis, Burgos)Term infant with early onset GBS meningitis and seizures: bilateral, purely ischaemic (hyperintense on T2 MRI) lesions in the hypothalamic area, more extensive on the right; in sagittal ultrasound section the lesion is underneath the sulcus hypothalamicus (from foramen of Monro to aqueduct), the groove that divides the diencephalon into thalamic and hypothalamic parts; hypothalamic hypothyroidism and diabetes insipidus. The lesions are well demarcated on DWMRI.
Arterial stroke to hypothalamus is exceptional, as it is not a predilection site for embolism. The rare situations where we do encounter such infarcts is due to basal purulent meningitis, typically associated with GBS infection in the newborn.
<—— inflammatory response in the Virchow-Robin spaces of perforator arteriesVentilated term infant, umbilical venous catheter in situ from birth, liver laceration during difficult breech delivery. During routine US a nodular lesion was seen near the left genu of the internal capsule; the circumstances suggested embolic infarction without haemorrhagic conversion (see T1 MRI); the lesion is located between the circular sulcus of the insula and the caudate head, no residual hemisyndrome.Endoscopic laparotomy and indwelling lines; multiple emboli.
Perinatal Perforator Stroke: Centrum Semi-ovale Arteries
Centrum semi-ovale stroke: Focal ischaemic infarction is occasionally encountered within the centrum semi-ovale immediately next to the lateral ventricle. Context and imaging are often indicative of an embolic ischaemic lesion. Focal arterial infarction in a terminal lateral striatal MCA branch is a likely possibility. The alternative explanation would be a stroke of one ventriculopetal cortical arterial branch of the ACA, MCA or PCA but with the occlusion away from the surface as it courses in white matter.
Stroke in centrum semi-ovale; stroke in tubero-thalamic artery
adapted from Paturet 1964
Arteries to hypothalamus come from all parts of the circle of Willis: ACA, PCoA, ICA, PCA P1. A large artery from the PCoA is the premammillary or tuberothalamic artery (TT).