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  • 2020–2021 BCSC Basic and Clinical Science Course™

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    5 Neuro-Ophthalmology

    Chapter 1: Neuro-Ophthalmic Anatomy

    Vascular Anatomy

    Arterial System

    Knowledge of the vascular anatomy of the head is crucial to understanding the potential for ischemic damage to the visual system. Ischemia is among the most common pathophysiologic causes of visual dysfunction (including vision loss and double vision). The common carotid arteries, arising from the innominate artery on the right and directly from the aorta on the left, supply most of the blood to the skull and its contents. The remainder of the blood supply to the skull comes from the 2 vertebral arteries (VAs), which enter the skull through the foramen magnum after traversing foramina in the cervical vertebral segments. Once the VAs penetrate the dura, they join near the pontomedullary junction to form the basilar artery (BA), which ascends along the anterior surface of the pons to terminate in the 2 posterior cerebral arteries (PCAs) at the level of the midbrain.

    The common carotid artery divides into internal and external branches at the angle of the jaw (Fig 1-6). The external carotid artery (ECA) supplies blood to the face through its major branches of the facial artery (FA). The scalp is supplied via branches of the occipital artery posteriorly and the superficial temporal artery anteriorly. The paranasal sinuses receive their blood supply from branches of the maxillary artery (sphenopalatine and infraorbital), which terminates in the pterygopalatine fossa. The coverings of the brain are supplied by branches of the middle meningeal artery (MMA)—a major branch of the maxillary artery—which enters the middle cranial fossa through the foramen spinosum, lateral to the foramen ovale. Branches of the MMA supply the parasellar area, including the lateral wall of the cavernous sinus (containing CNs III, IV, and VI), and terminate in the arteries of the foramen rotundum and ovale. Variable meningeal branches may enter the superior orbital fissure.

    Ophthalmologists are sometimes concerned about encountering branches of CN VII, particularly when performing a temporal artery biopsy or during orbital or lacrimal surgery. Terminal branches of the FA supply the marginal arcades of the eyelids. It is extremely important to understand the extent of the collateral connections between the branches of the ECA and the internal carotid artery (ICA) (Fig 1-7). This point is particularly germane to interventional neuroradiologists, who may inadvertently embolize distal ICA branches—including the central retinal artery (CRA)—while placing particles into the ECA. Embolization is most likely to occur during the treatment of arteriovenous malformations, but it can also occur when skull-base tumors are embolized prior to surgical resection.

    The most important collateral connections between the internal and external circulations traverse the orbit. They include the anterior and posterior ethmoidal arteries in the medial orbit, the infraorbital and supraorbital arteries (including distal connections to the lacrimal artery) anteriorly, and the zygomaticotemporal branch laterally. The FA joins the distal branches of the supratrochlear and infratrochlear arteries around the angular artery in the medial orbit. In addition, variable collateral dural branches traverse the superior and inferior orbital fissures. In rare instances, the ophthalmic artery (OphA) may also arise as a branch of the meningeal system of the ECA.

    The ICA carries the major blood supply to the intracranial contents (Fig 1-8). The ICA enters the skull through the carotid canal. Within the petrous bone, the ICA is near the middle and inner ear, as well as the intrapetrosal portion of CN VII. As the ICA reaches the parasellar area, it turns superiorly just above the foramen lacerum. It then enters the cavernous sinus, where it first gives off the meningohypophyseal trunk and then turns anteriorly to run horizontally parallel to the body of the sphenoid to give off the inferolateral trunk, which forms anastomoses with branches of the MMA. Branches of the meningohypophyseal trunk supply the dura at the back of the cavernous sinus as well as CNs III, IV, V, and VI entering the cavernous sinus. These branches also variably supply the lateral aspect of the sella turcica, including the pituitary capsule and a large portion of the pituitary gland itself.

    Figure 1-6 Arterial supply of the orbit and ocular adnexa. A, Arterial supply of the ocular adnexa and orbit originating from the aortic arch. B, Anterior view of the superficial arterial supply to the eyelids and anterior orbit. C, Sagittal view of the arterial supply to the orbit and globe. ICA = internal carotid artery.

    (Illustrations by Christine Gralapp.)

    At the anterior aspect of the cavernous sinus, the ICA makes a loop to reverse its direction under the anterior clinoid and the optic nerve. This loop passes through 2 dural rings, both close to the anterior clinoid (the terminal portion of the lesser wing of the sphenoid). As the ICA passes through the second ring, it becomes intradural (Fig 1-9). Just after it becomes intradural, the ICA gives off the OphA, which enters the orbit along with the optic nerve through the optic canal.

    Within the orbit, the OphA (see Fig 1-7) may anastomose with recurrent meningeal branches that enter through the superior orbital fissure. The OphA gives off the CRA, which then enters the substance of the optic nerve approximately 10–12 mm posterior to the globe. Within the eye, the CRA divides into superior and inferior arcades. Like the blood–brain barrier, the retinal arteries and arterioles have tight junctions that form a blood–retina barrier. The intraretinal arterioles run within the substance of the nerve fiber layer to supply the inner two-thirds of the retina.

    The lacrimal artery (LA) runs parallel to the lacrimal branch of CN V1 in the superior lateral orbital roof to reach the lacrimal gland. It also gives off the anterior ciliary artery of the lateral rectus muscle and reaches the anterior segment at the muscle’s insertion. The frontal artery runs within the superior orbit, paralleling the frontal branch of CN V1 to separate into and terminate as the supraorbital and supratrochlear arteries, which, along with the LA, supply the eyelid.

    The next branches leaving the OphA are the superior and inferior muscular arteries, which supply the anterior ciliary arteries of the medial and inferior rectus (inferior muscular artery) and the superior rectus and superior oblique (superior muscular branch) muscles. The anterior ciliary arteries are responsible for the majority of blood flow to the ciliary body. The medial and lateral long posterior ciliary arteries variably anastomose with penetrating branches of the anterior ciliary arteries (within the rectus muscles) to form the greater arterial circle near the anterior part of the ciliary body. Branches from this circle extend radially within the iris to form a second anastomotic circle (the lesser arterial circle) near the collarette of the iris.

    Figure 1-7 Internal carotid artery (green) and external carotid artery (orange) collateral anatomy. 1, internal carotid; 2, external carotid; 3, facial; 4, maxillary; 5, superficial temporal; 6, transverse facial; 7, middle meningeal; 8, frontal branch of superficial temporal; 9, ophthalmic; 10, lacrimal; 11, recurrent meningeal; 12, supraorbital; 13, supratrochlear; 14, angular; 15, palpebral; 16, zygomaticotemporal; 17, zygomaticofacial; 18, deep temporal; 19, infraorbital; 20, muscular.

    (Modified with permission from Kline LB. Neuro-Ophthalmology Review Manual. 6th ed. Thorofare, NJ: Slack; 2008:213, by Christine Gralapp.)

    The terminal OphA supplies additional branches that form collaterals with the anterior and posterior ethmoidal arteries and also form the short and long posterior ciliary arteries (Fig 1-10). The short posterior ciliary arteries divide into 10–20 small branches that supply the optic nerve head (ONH) and posterior choroid. Together, these arteries supply blood to the choroid, the retinal pigment epithelium (RPE), and approximately the outer one-third of the retina, including the photoreceptor cells. In approximately 30% of individuals, branches of the posterior ciliary arteries (cilioretinal arteries) directly supply a portion of the inner retina; this blood supply may protect the macula in the case of a CRA occlusion. Approximately 4 short posterior ciliary arteries form a variably complete anastomotic ring (known as the circle of Zinn-Haller) around the ONH, which is also supplied from the peripapillary choroid and the terminal branches of the pial network.

    Figure 1-8 Branches of the ICA. A, Lateral view. B, Anteroposterior view. Proximal ICA branches: ophthalmic artery (OphA) and its branches (anterior and posterior ethmoidal arteries [A&PEthAs] and central retinal artery [CRA]); posterior communicating artery (PCoA); anterior choroidal artery (AChA); anterior communicating artery (ACoA); anterior cerebral artery (ACA) and its branches (callosomarginal artery [CalMargA] and pericallosal artery [PeriCalA]); and middle cerebral artery (MCA) and its branches (lateral lenticulostriate artery [LatLSA] and posterior temporal artery [PTempA]).

    (Illustrations by Rob Flewell, CMI.)

    Figure 1-9 Lateral view of the bend of ICA within the right cavernous sinus. The anterior clinoid process has been resected to show the proximal and distal dural rings. V1 = ophthalmic division of CN V; V2 = maxillary division of CN V; V3 = mandibular division of CN V.

    (Illustration by Dave Peace.)

    Collateral branches from terminal branches of the infraorbital artery and the superficial temporal artery help supply the lower and upper eyelids and may also provide collateral supply to the anterior segment. These collaterals may be interrupted if the conjunctiva and Tenon capsule are removed from the limbus during ocular surgery.

    Figure 1-10 Schematic representation of the vascular supply to the optic nerve and optic nerve head (ONH). Intraocular view (A), lateral view (B), and sagittal view (C) of the ONH. Short posterior ciliary arteries supply centripetal capillary beds of the anterior ONH. The central retinal artery (CRA) contribution is restricted to nerve fiber layer capillaries and capillaries of the anterior intraorbital optic nerve. Capillary beds at all levels drain into the central retinal vein (CRV). A = arachnoid; Ch = choroid; ColBr = collateral branches; D = dura; LC = lamina cribrosa; NFL = surface nerve fiber layer of the ONH; ON = optic nerve; P = pia; PCilA = posterior ciliary artery; R = retina; RA = retinal arteriole; S = sclera; SAS = subarachnoid space.

    (Reproduced from Hayreh SS. The blood supply of the optic nerve head and the evaluation of it—myth and reality. Prog Retin Eye Res. 2001;20(5):563–593.)

    Distal to the origin of the OphA, the intradural supraclinoid ICA gives off the anterior choroidal artery (AChoA) and anastomoses with the proximal posterior cerebral artery (PCA) through the posterior communicating artery (PCoA). The AChoA supplies blood proximally to the optic tract and distally to the lateral geniculate nucleus (LGN) (Fig 1-11). Injury to the AChoA can produce the optic tract syndrome, a disorder consisting of contralateral homonymous hemianopia, contralateral band atrophy of the ONH, and a contralateral relative afferent pupillary defect (see Chapter 4). The ICA gives off the anterior cerebral artery (ACA) and terminates as branches of the middle cerebral artery (MCA). The proximal ACA (the A1 segment) crosses over the optic nerve and joins the opposite ACA via the anterior communicating artery (ACoA). The combination of the ACoA and PCoA makes up the circle of Willis, which permits collateral flow between the carotid and vertebrobasilar systems when there is vascular compromise. Small perforating branches arising from the proximal ACA as well as the ACoA supply the intracranial optic nerves and chiasm. Although the afferent visual pathways are spared with distal ACA occlusion, the premotor areas of the frontal lobes responsible for initiating saccades are supplied by branches of the ACA. Thus, patients with acute occlusion of the ACA may have a transient gaze preference and difficulty initiating saccades to the contralateral side, although this effect is more commonly seen in patients with MCA territory lesions.

    Figure 1-11 Relationship of the lateral geniculate nucleus to nearby structures and its blood supply. AChoA = anterior choroidal artery; BC = brachium conjunctivum; CerePed = cerebral peduncles; ICA = internal carotid artery; LGN = lateral geniculate nucleus; MCA = middle cerebral artery; MGN = medial geniculate nucleus; ON = optic nerve; PCA = posterior cerebral artery; PCoA = posterior communicating artery; PLChA = posterior lateral choroidal artery; Pulv = pulvinar; RN = red nucleus; SC = superior colliculus; SCA = superior cerebellar artery.

    (Illustration by Craig A. Luce.)

    The MCA divides into several branches, which supply the temporal lobe, parietal lobe, and superficial portions of the frontal lobe and occipital lobe. Branches important to the visual pathways include those supplying the optic radiations as they traverse the deep white matter of the parietal and temporal lobes. Terminal branches of the MCA also variably supply the occipital tip representing the macula. This supply is chiefly responsible for the perimetric finding of macular sparing in PCA or calcarine artery occlusion (see Chapter 4, Fig 4-32). In addition to supplying the afferent pathways, the MCA supplies the middle temporal region, which is involved in visually guided pursuit movements. Thus, lack of blood supply can cause problems with ipsilateral pursuit or asymmetry in optokinetic nystagmus when a clinician rotates the OKN drum toward the side of the infarct.

    The posterior circulation begins with the aortic arch. The right and left VAs arise from the subclavian arteries. The innominate artery becomes the right subclavian artery beyond the origin of the common carotid artery (see Fig 1-6A). The VA travels through a series of foramina in the lateral aspects of the cervical vertebral processes. After penetrating the dura at the foramen magnum, the VA gives rise to the posterior inferior cerebellar artery (PICA) before joining the other VA to form the BA (Fig 1-12). The PICA represents the most caudal of the 2 major circumferential arteries that wrap around the brainstem. Proximally, the PICA and BA first give off branches that perforate the medial portion of the brainstem at the medullary level; the paramedian branches that follow supply the lateral aspects of the brainstem. Distally, the PICA supplies the inferior cerebellum, which is intimately involved in eye movements. VA or PICA occlusion is associated with the lateral medullary syndrome (also called Wallenberg syndrome) (see Chapter 2, Fig 2-6). The second circumferential arteries are branches of the anterior inferior cerebellar artery (AICA). The AICA arises from the caudal BA and supplies the pontomedullary junction and distal cerebellum. A large proximal branch of the AICA, the internal auditory artery, supplies the CN VIII complex in the subarachnoid space and follows it into the internal auditory canal. Along the course of the BA, small perforators arise directly to supply portions of the pons and midbrain. The median perforators of the BA supply the medial longitudinal fasciculus, the paramedian pontine reticular formation (PPRF), and the medially located nuclei of CNs III, IV, and VI. Interruption of these branches (which occurs commonly with vertebrobasilar atherosclerotic disease or emboli to these end arteries) often produces variable ophthalmoplegia, internuclear ophthalmoplegia, and skew deviation. Pontine branches of the BA also supply the proximal portions of the CNs (particularly CN V) as they exit the brainstem.

    Figure 1-12 Vertebrobasilar arterial system and major arteries with common variations of the cortical branches of the posterior cerebral artery (PCA). A, Lateral view. B, Anteroposterior view. Vertebral artery (VA) and basilar artery (BA) branches: anterior inferior cerebellar artery (AICA); posterior inferior cerebellar artery (PICA); superior cerebellar artery (SCA). PCA and its branches: calcarine artery (CalcA); parieto-occipital artery (ParOccipA); posterior choroidal artery (PChoA); posterior temporal artery (PTempA); posterior communicating artery (PCoA).

    (Illustration by Rob Flewell, CMI.)

    The distal 2 sets of circumferential arteries consist of the superior cerebellar artery (SCA) followed by the PCA, representing the terminal branches of the BA at the level of the midbrain. Perforators from the proximal SCA partially supply the nucleus of CN III and its fascicles. In addition, small branches often supply the CN V root. CN III exits between the SCA and the PCA, where it may be compressed by an aneurysm.

    Perforators from the proximal PCA (the P1 segment) supply the rostral portion of the midbrain (the portion involved in vertical gaze) and part of the LGN. A large branch, the artery of Percheron, often supplies both sides of the midbrain from one of the PCAs. Because thalamostriate arteries originate from P1, infarcts related to the internal ICA–MCA spare the thalamus. The P1 segment ends with the PCoA, which joins the vertebrobasilar circulation to the carotid circulation anteriorly. The connecting PCoA parallels the course of CN III and then joins the ICA, which explains the occurrence of CN III palsy with PCoA aneurysms (see Chapters 2 and 7). As the distal PCA courses around the brainstem, it gives off a parieto-occipital branch before terminating in the calcarine branch, which supplies the primary visual cortex (Fig 1-13).

    Figure 1-13 The occipital cortex and its blood supply. The primary visual cortex, or striate cortex (V1); the parastriate cortex (V2); and V3 are keyed by color. CalcA = calcarine artery; CC = corpus callosum; MCA = middle cerebral artery; PCA = posterior cerebral artery.

    (Illustration by Craig A. Luce.)

    Excerpted from BCSC 2020-2021 series: Section 5 - Neuro-Ophthalmology. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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