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  • 2020–2021 BCSC Basic and Clinical Science Course™

    Go to Academy Store Learn more and Purchase.

    5 Neuro-Ophthalmology

    Chapter 1: Neuro-Ophthalmic Anatomy

    Efferent Visual System (Ocular Motor Pathways)

    Brainstem

    The supranuclear pathways for saccades and smooth pursuit eventually reach the brainstem neural network (via the SC and BG), which allows for conjugate eye movements. The following list of major anatomical structures and their functions helps set a foundation for discussion of the pathways for coordinating conjugate eye movements (Fig 1-25):

    • riMLF: excitatory burst neurons that generate vertical and torsional saccades

    • interstitial nucleus of Cajal (INC): inhibitory burst neurons for vertical saccades and the neural integrator for vertical and torsional gaze

    • region of riMLF and INC: inhibitory burst neurons for vertical and torsional saccades

    • posterior commissure (PC): projecting axons from the INC to the contralateral nuclei of CNs III, IV, and VI and the INC

    • medial longitudinal fasciculus (MLF): major pathway for relaying signals within the brainstem

    • DLPN: neurons for smooth pursuit

    • nucleus prepositus hypoglossi (NPH): neural integrator for horizontal gaze

    • PPRF: excitatory burst neurons that generate horizontal saccades and inhibitory burst neurons for horizontal saccades

    • CNs III, IV, and VI: neurons that project directly to EOMs

    • vestibular nuclei (CN VIII): neurons that project to saccade generators and ocular motor CNs

    Figure 1-25 Schematic representation of a sagittal section of the brainstem showing the location of the important structures involved in eye movements. The shaded areas indicate the paramedian pontine reticular formation (PPRF). The DLPN are not visible because this illustration is a midsagittal section and the DLPN is laterally located; it is best visualized on an axial view through the rostral pons. INC = interstitial nucleus of Cajal; MLF = medial longitudinal fasciculus; MRF = mesencephalic reticular formation; NPH = nucleus prepositus hypoglossi; PC = posterior commissure; riMLF = rostral interstitial nucleus of MLF.

    (Illustration by Rob Flewell, CMI.)

    In general, the midbrain is responsible for vertical eye movements and the pons for horizontal eye movements. Vertical and torsional saccades are generated from excitatory burst cells of the riMLF within the midbrain. In contrast, the pathways for vertical vestibular and vertical smooth pursuit ascend from the medulla and pons to the midbrain via the MLF. Horizontal saccades are generated from excitatory burst cells within the PPRF, and horizontal smooth-pursuit eye movements arise from the CN VI nucleus, which receives input from the vestibulocerebellum (see the section “Cerebellum,” later in this chapter).

    Vertical gaze is controlled through the midbrain. The primary gaze center is located in the riMLF (Fig 1-26). This area receives input from the medial and superior vestibular nuclei via the MLF and other internuclear connections. Other areas in the rostral midbrain, including the INC, also modulate vertical motility. Burst-cell input may come in part from the PPRF caudally but also locally from within the riMLF. The INC (the neural integrator for vertical and torsional gaze) receives signals from the riMLF and from the vestibular nuclei and projects via the PC to the motoneurons of the CN III and CN IV nuclei. Activity from the vertical gaze center is distributed to the CN III and CN IV nuclei. Information involved in upgaze crosses in the PC. Damage to this pathway results in dorsal midbrain syndrome, a disorder that includes vertical gaze difficulty (most commonly, impaired supraduction), skew deviation, light–near pupillary dissociation, eyelid retraction, and convergence-retraction nystagmus (see Chapter 9 in this volume).

    Figure 1-26 Anatomical schemes for the synthesis of upward and downward movements. From the vertical semicircular canals, primary afferents from CN VIII synapse on the VN and ascend into the medial longitudinal fasciculus (MLF) and brachium conjunctivum (not shown) to contact the CN III and CN IV nuclei and the interstitial nucleus of Cajal (INC). (For clarity, only excitatory vestibular projections are shown.) Excitatory burst neurons in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) project to the motoneurons of CNs III and IV and send axon collaterals to the INC. Each riMLF neuron sends axon collaterals to yoke-pair muscles (Hering’s law). III nucleus = oculomotor nerve (CN III) nucleus; IV nucleus = trochlear nerve (CN IV) nucleus; PC = posterior commissure.

    (Illustration by Rob Flewell, CMI.)

    Horizontal gaze is coordinated through the CN VI nucleus in the dorsal caudal pons (Fig 1-27). This nucleus receives tonic input from the contralateral horizontal semicircular canal through the medial and lateral vestibular nuclei. Burst information is supplied from the PPRF, which is directly adjacent to the CN VI nucleus and the MLF. The burst cells are normally inhibited by omnipause neurons. Saccades are thought to be initiated by supranuclear inhibition of the omnipause cells, which allows burst-cell impulses to activate the horizontal and vertical gaze centers. To produce horizontal movement of both eyes, a signal to increase firing must be distributed to the ipsilateral lateral rectus and the contralateral medial rectus muscles. The lateral rectus muscle is supplied directly through ipsilateral CN VI. The contralateral medial rectus muscle is stimulated by interneurons that cross in the pons and ascend in the contralateral MLF. Therefore, pathology affecting the right MLF will result in a right internuclear ophthalmoplegia—a right (ipsilateral) adduction deficit with attempted left gaze—often accompanied by abducting nystagmus of the left (contralateral) eye and a skew deviation (see Chapter 7, Fig 7-5).

    Figure 1-27 Anatomical scheme for the synthesis of signals for horizontal eye movements. From the horizontal semicircular canal, primary afferents of the vestibular nerve (CN VIII) project mainly to neurons of the vestibular nerve nucleus (CN VIII nucleus), which then send an excitatory connection to the contralateral abducens nucleus (CN VI nucleus). CN VI innervates the ipsilateral lateral rectus muscle and the contralateral oculomotor nerve nucleus (CN III nucleus) via the medial longitudinal fasciculus (MLF). Horizontal saccades are generated in the frontal eye field, which activates the contralateral PPRF. Burst neurons in the PPRF stimulate the ipsilateral abducens nucleus, with the subsequent pathway identical to that subserving horizontal vestibular-generated eye movements. Some neurons in the PPRF project to the nucleus prepositus hypoglossi (NPH) (the neural integrator) and then to the abducens nucleus.

    (Illustration by Rob Flewell, CMI.)

    The distribution of infranuclear (ocular motor cranial nuclei and nerves) as well as supranuclear information requires internuclear communication within the brainstem. The most important of these pathways, the MLF, runs in 2 parallel columns from the spinal cord to an area of the midbrain PC that is located dorsomedial to the red nucleus and rostral to the INC. The bulk of the fibers contributing to the MLF originate in the vestibular nuclei. The projections from the superior vestibular nucleus are ipsilateral, and those from the medial vestibular nucleus are contralateral. The MLF also receives interneurons originating from the contralateral CN VI nucleus.

    To maintain eccentric gaze, additional tonic input must be provided to the yoke muscles that hold the eye in position. This additional input is provided by integrating the velocity signal provided by the burst-neuron activity. For horizontal eye movements, integration takes place in the NPH, located adjacent to the medial vestibular nucleus at the pontomedullary junction, with input from the cerebellum. Neural integration for vertical eye movements involves the INC in addition to the cerebellum. Pathology affecting the neural integrator (often metabolic, associated with alcohol consumption or anticonvulsant medication) results in failure to maintain eccentric gaze, recognized clinically as gaze-evoked nystagmus (see Chapter 9).

    Vestibular-ocular system

    The output of the vestibular nuclei provides both the major supranuclear input into ocular motility and the major tonic input into eye position. This system has one of the shortest arcs in the nervous system, producing a fast response with extremely short latency. The hair cells of the semicircular canals alter their firing in response to relative movement of the endolymph (Fig 1-28). The signal is produced by a change in velocity (head acceleration) in any 1 of 3 axes. The information is then conveyed to the vestibular nuclei (located laterally in the rostral medulla) via the inferior and superior vestibular nerves. Hair cells in the macula acoustica of the utricle and saccule also contribute to the vestibular nerve. Calcium carbonate crystals within the otoliths respond to linear acceleration (most importantly, gravity) to orient the body. The vestibular nerve and the output of the membranous labyrinth (the cochlear nerve) make up the CN VIII complex and exit the petrous bone through the internal auditory meatus. CN VIII traverses the subarachnoid space within the cerebellopontine angle. Within the medulla, the vestibular information synapses in the medial, lateral, and superior vestibular nuclei. Tonic information from the horizontal canal crosses directly to the contralateral gaze center within the CN VI nucleus in the dorsal medial aspect of the caudal pons just under the fourth ventricle. Tonic information from the anterior and posterior canals travels rostrally through several of the important internuclear connections to innervate the vertical gaze center in the rostral midbrain. Medial and inferior vestibular nuclei, as well as the NPH and the inferior olivary nucleus, project to the nodulus (a central nucleus of the cerebellum) and the ventral uvula. This pathway, which projects back to the vestibular nuclei, is responsible for the velocity storage mechanism (ie, the mechanism that maintains the vestibular signal beyond the output of the primary vestibular neurons).

    Figure 1-28 Vestibular system. A, Schematic of the mammalian labyrinth. The crista of the lateral semicircular canal is shown but not labeled (with the canal projecting forward). B,Top: Motion transduction by the vestibular hair cells. At rest, there is a resting rate of action potential discharge in the primary vestibular afferents (center hair cell). Depolarization occurs when the stereocilia are deflected toward the kinocilium (represented by the longest cilium, with a beaded end). Hyperpolarization occurs when the stereocilia are deflected away from the kinocilium. This movement of the stereocilia modulates the discharge rate in the vestibular nerve neuron. Bottom: The action potential generated by the shearing forces on the hair cell. Depolarization (left side of graph) causes an increase in the frequency of the action potential. Hyperpolarization causes a decrease in the frequency of action potential.

    (Reproduced with permission from Leigh RJ, Zee DS. The Neurology of Eye Movements. 4th ed. New York: Oxford University Press; 2006.)

    For information on clinical disorders of vestibular-ocular function, see Chapter 8.

    Cerebellum

    The other major connection in the ocular motor system is to the vestibulocerebellum. The structures in this area, largely through the brachium conjunctivum, are responsible for adjusting the gain of all ocular movements. Gain may be defined as the output divided by the input. For example, keeping the eyes stable in space while the head rotates requires the eyes to move in a direction opposite that of head rotation at the same velocity and distance; this would be considered a gain of 1. The cerebellum is involved in gain adjustment to allow compensation after peripheral lesions (eg, vestibular nerve dysfunction such as vestibular neuritis). Disease processes directly affecting the cerebellum may affect the vestibular-ocular reflex.

    Efference copy information (regarding the position of the eyes) is supplied directly from the ocular motor pathways (possibly through cell groups of the paramedian tracts within the vestibular nuclei), whereas afferent signal error information arrives at the cerebellum via the climbing fibers from the inferior olivary nucleus. Additional cerebellar inputs include mossy fiber input from the vestibular nuclei and the NPH. Purkinje cells within the paraflocculus discharge during smooth pursuit. The dorsal vermis may play a role in initiating pursuit and saccades. The fastigial nucleus is responsible for overcoming a natural imbalance in the input from the vertically oriented semicircular canals. Thus, loss of fastigial function may be associated with development of downbeat nystagmus, as the imbalance in the vertical information causes constant updrift.

    See Chapter 9 in this volume for further discussion of nystagmus and other spontaneous eye movement disorders.

    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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