Oculomotor System George R. Leichnetz, Ph.D.

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1 Oculomotor System George R. Leichnetz, Ph.D. OBJECTIVES After studying the material of this lecture, the student should be able to: 1. Define different types of eye movement and their underlying neural network, including cortical and brainstem structures and pathways related to specific types of eye movement. 2. Identify eye movement deficits associated with specific lesions. I. INTRODUCTION There are several different types of eye movements. Each type of eye movement has a distinctive premotor neural network. Some eye movements are reflexive eye movements that compensate for head movements (VOR vestibuloocular reflex); intended to maintain fixation (on the fovea) during head movement, or those associated with looking at a moving visual scene, e.g., watching telephone poles while on a moving train (optokinetic). Others track or follow a moving object across the visual field (smooth pursuit). Others are rapid, intentional and voluntary, or reflexively, to look at an object, i.e., to put the object image on the fovea (saccades). All of these types of eye movements are initiated to either put the object image on the fovea of the retina, or to maintain fixation during movement of the head (VOR) or moving visual scene (optokinetic). All of these are conjugate, i.e., the eyes move together in the same direction. The last type, vergence eye movements, are disjunctive, i.e., the eyes move in the opposite direction; convergence is part of the near response which also includes pupillary constriction and accommodation (lens thickening). Each of these types of eye movements has a distinctive premotor neural network, ie. a network of connections that precedes projections to the extraocular motor nuclei (the final pathway to the extraocular muscles). Many eye movements involve structures of the visual pathway (seeing the object), visual cortex and parieto-occipto-temporal associational cortex (image features, perception, visual discrimination, attention, memory), frontal eye field (voluntary eye movement initiation), cerebellum (appropriate metrics and velocity of the eye movement), and vestibular complex (sense head and body movements). The pretectum is also involved where pupillary changes are involved. The large number of structures throughout the brain that are involved make the oculomotor system particularly vulnerable in traumatic or vascular lesions of the brain. Lesions within these premotor neural networks lead to distinctive oculomotor deficits, which are valuable in diagnosis of the location of the lesion. For every type of eye movement, however, the final common pathway to extraocular muscles originates from the extraocular motor nuclei: oculomotor, trochlear, and abducens nuclei.

2 It is necessary to know the principal structures or nexuses within each neural subsystem so as to understand the basis of specific oculomotor deficits that accompany lesion of these structures. II. EXTRAOCULAR MOTOR NUCLEI The premotor neural networks for various types of eye movements must ultimately converge with appropriate motor neuron cell groups within specific extraocular motor nuclei (oculomotor, III; trochlear, IV; abducens, VI) to produce the desired movement. Noback

3 In very general terms, certain extraocular muscles work together to perform eye movements in specific directions: Upward - superior rectus, inferior oblique; Downward- inferior rectus, superior oblique Horizontal (adduction) - medial rectus; Horizontal (abduction) - lateral rectus For example, upward eye movements are initiated from motoneurons within superior rectus and inferior oblique subgroups of the oculomotor (III) nucleus, whereas in downward eye movements, the central connections would converge with the inferior rectus cell group of the oculomotor nucleus and superior oblique subgroup of the trochlear (IV) nucleus. A. Oculomotor Complex: two subdivisions 1. Principal Oculomotor Nucleus - the somatic (GSE) division of the oculomotor complex contains motoneurons that innervate the medial rectus, superior rectus, inferior rectus, and inferior oblique muscles, plus the levator palpebrae superioris muscle (for eyelid elevation) 2. Edinger-Westphal Nucleus - the autonomic (GVE) portion of the oculomotor complex is the Edinger-Westphal nucleus, a small cluster of preganglionic parasympathetic neurons that lies above the rostral portion of the oculomotor nucleus. These GVE axons course via the IIIrd nerve to synapse in the ciliary ganglion, with postganglionic fibers distributed to the sphincter pupillae muscle of the iris (for pupillary constriction) and to the ciliary body (for lens thickening, accommodation).

4 From: Haines, Fundamental Neuroscience B. Trochlear Nucleus - innervates superior oblique muscle C. Abducens Nucleus - two populations of neurons 1. Lateral Rectus Motoneurons - 70% of the neurons of the abducens nucleus are motoneurons that innervate the ipsilateral lateral rectus muscle. 2. Internuclear Neurons - The remaining 30% of neurons in the abducens nucleus are internuclear neurons whose axons cross the midline and ascend in the contralateral medial longitudinal fasciculus (MLF), to medial rectus motoneurons in the contralateral oculomotor nucleus. These internuclear fibers form the basis of contraction of the contralateral medial rectus in a conjugate horizontal eye movement. Therefore, lesions of the abducens nucleus not only paralyze the ipsilateral lateral rectus muscle, but also render the contralateral medial rectus muscle dysfunctional during an attempted ipsilateral horizontal eye movement; thus producing an ipsilateral paralysis of horizontal eye movement.

5 III. TYPES OF EYE MOVEMENTS AND THEIR NEURAL NETWORKS A. SACCADES - rapid eye movements; short rapid jerks to put visual target image on the fovea of the retina (foveate) Voluntary saccades or those that might be made to a remembered target have a cognitive component and therefore involve the frontal eye field, whereas reflexive saccades, that are made in response to a novel object that appears in the visual field (or auditory or somatosensory stimulus), are mediated by the superior colliculus. 1. Frontal Eye Field - area 8 - located in the caudal part of the middle frontal gyrus; it is the origin of corticobulbar projections to preoculomotor centers in the brainstem reticular formation; it also projects to the superior colliculus 2. Superior Colliculus The superior colliculi are paired laminated elevations on the dorsal aspect of the rostral midbrain. Each has seven alternating gray and white layers. The superficial layer receives direct visual input from the retina, and has a map of the visual world. The intermediate layer receives input from the frontal and parietal cortical eye fields (corticotectals), cerebellum (cerebellotectals), and substantia nigra, pars reticulata (nigrotectals). The motor map in the deep layers is in registry with the visual map in the superficial layer so that the eye movements generated are amplitude - and direction - specific to target a precise locus in the visual field. Like the FEF, it projects to preoculomotor centers in the brainstem reticular formation. The superior colliculus of a rhesus monkey From Huerta and Harting in Vanegas (eds) Comparative Neurology of the Optic Tectum

6 3. Preoculomotor Centers in the Brainstem Reticular Formation Neither FEF or SC project directly to motor neurons in the extraocular motor nuclei, but instead project to premotor centers in the brainstem reticular formation. From: J. Buttner-Ennever a. Rostral Midbrain Reticular Formation The region of the mesencephalic reticular formation rostral to the oculomotor complex (where it is contiguous with the caudal subthalamic region), contains the rostral interstitial nucleus of the medial longitudinal fasciculus (rostral imlf) related to the control of vertical downward gaze.

7 From: Haines, Fundamental Neuroscience In the mesencephalic reticular formation within the rostral MLF adjacent to the rostral oculomotor complex, the interstitial nucleus of Cajal is related to the control of vertical upward gaze. From: Haines, Fundamental Neuroscience Neurons in these structures also project to the spinal cord, forming the basis for their role in the head movement aspect of vertical gaze. Lesions of the rostral imlf produce paralysis of downward gaze. Lesions of the interstitial nucleus of Cajal or interconnecting fibers in the posterior commissure produce paralysis of upward gaze. Lesions of the posterior commissure also typically produce deficits in the pupillary light reflex as a result of the proximity to the pretectal area (pretectal syndrome, anisocoria). b. Medial Pontine Reticular Formation The paramedian pontine reticular formation (PPRF) in the medial pontine reticular formation (nucleus reticularis pontis caudalis, NRPC) at the level of the abducens nucleus contains the premotor neurons involved in conjugate horizontal gaze. The NRPC (PPRF) contains neurons that project to ipsilateral abducens neurons, as well as to the cervical spinal cord which provide basis for eye movement plus head movement (gaze).

8 The PPRF is known as the center for conjugate horizontal gaze. Lesions of the PPRF result in paralysis of ipsilateral conjugate horizontal gaze, in contrast to lesions of the abducens nucleus which affect only conjugate horizontal eye movement. From: Haines, Fundamental Neuroscience 4. Frontal Eye Field and Superior Colliculus Project to Brainstem Preoculomotor Centers The FEF and SC project to the centers for vertical and horizontal gaze in the brainstem reticular formation.

9 From: Haines, Fundamental Neuroscience B. SMOOTH PURSUIT - slow eye movements; tracking a moving object across the visual field These movements maintain the focus (fixation) of moving targets on the fovea of the retina. The smooth pursuit system matches eye movement velocity to target velocity. This requires perceiving the object and sensing motion of the visual stimulus, and recruitment of the cerebellum to calculate the appropriate size and velocity of the movement. Neural Network: Retina> LGN> Visual Cortex> MT Visual Area (analysis of visual motion) > Dorsolateral basilar pontine nucleus (via corticopontines from MT)> Cerebellar vermis- oculomotor vermis of the posterior lobe and its connections with the fastigial nucleus

10 C. VESTIBULAR Vestibulo-Ocular Reflex (VOR) compensates for head movement Vestibular eye movements are elicited by head movements that activate receptors in the semicircular canals. The vestibulo-ocular reflex (VOR) is a compensatory eye movement that replicates a head movement, but in the opposite direction. The function of the VOR is to maintain fixation and the stability of the visual field while the head moves. For example, rotation of the head to the right (primarily horizontal canals activated) produces a compensatory conjugate eye movement to the left so that images in the visual field remain stationary on the retina. (see vestibular system lecture for illustration) D. OPTOKINETIC EYE MOVEMENTS - moving visual scene (e.g., riding on a train, watching telephone poles); slow phase follows pole, then quick phase, eyes snap back Optokinetic Eye Movements allows an individual to focus on objects in a moving visual scene (eg. looking out the window of a moving train). There is a slow component in the direction of the moving stimulus and a fast component (quick phase) in the opposite direction when the excursion limit of the oculomotor range has been reached. The optokinetic system works synergistically with the vestibular system to stabilize the visual field on the retina during movements of the visual world or the head. Neural Network: Retina>Pretectum> Nuc. Reticularis Tegmenti Pontis (NRTP)> Cerebellar flocculus

11 E. VERGENCE EYE MOVEMENTS - disjunctive (the only disconjugate type of eye movement) Convergence is part of the "near response", which includes convergence, pupillary constriction, and accommodation Vergence eye movements are associated with changing the point of foveal fixation from a distant object to a near object (near response). Vergence movements are disjunctive, since they are produced by bilateral contraction of the medial rectus muscles in both eyes. Vergence eye movements also are associated with changes in the shape of the lens of the eye (accommodation) and constriction of the pupil (miosis) as a part of the near response. Convergence involves disconjugate eye movements; a simultaneous contraction of two medial rectus muscles Near Response, focusing on a near object, requires convergence, accommodation (lens thickening), and pupillary constriction Neural Network: Retina> LGN> Visual Cortex>Pretectum> Edinger-Westphal Nucleus (IIIrd nerve) to ciliary ganglion to constrictor pupillae, or Supraoculomotor PAG to oculomotor nucleus (to medial rectus motoneurons)- convergence (pathway uncertain) Niewenhuys

12 IV. CLINICAL CORRELATIONS/ OCULOMOTOR LESIONS: A. Oculomotor nerve (C.N. III) lesion: ptosis, exotropia, mydriasis Ptosis- drooping eyelid due to paralysis of the levator palpebrae superioris Exotropia- ipsilateral eye abducted due to paralysis of medial rectus (lateral rectus unopposed) Mydriasis- pupillary dilatation due to disruption of innervation of pupillary constrictors (E- W parasympathetics via oculomotor nerve to ciliary ganglion) From Fix, High-Yield Neuroanatomy B. Abducens Nerve (C.N. VI) Lesion: esotropia (eye can not be abducted; internal deviation due to unopposed action of medial rectus) Esotropia- paralysis of lateral rectus (medial rectus unopposed) From Fix, High-Yield Neuroanatomy C. Abducens Nucleus Lesion: paralysis of ipsilateral conjugate horizontal eye movements Damages both lateral rectus motor neurons and internuclear neurons that project to contralateral medial rectus motor neurons (through MLF to contralateral oculomotor nucleus)

13 D. PPRF Lesion: paralysis of ipsilateral horizontal gaze Disrupts projections to ipsilateral abducens nucleus- producing ipsilateral paralysis of conjugate horizontal eye movements Disrupts projections to ipsilateral cervical spinal cord (pontine reticulospinals)- producing paralysis of ipsilateral head movements E. MLF Lesion: internuclear ophthalmoplegia with nystagmus Disrupts internuclear axons to ipsilateral medial rectus motor neurons (that originated in contralateral abducens nucleus)- produces inability to adduct ipsilateral eye; but the medial recti both contract with convergence Nystagmus- disruption of vestibuloocular fibers in MLF

14 From Fix, High-Yield Neuroanatomy F. Frontal Eye Field lesion: paralysis of contralateral conjugate horizontal gaze Disrupts FEF projections to contralateral PPRF From: Haines, Fundamental Neuroscience

15 From Fix, High-Yield Neuroanatomy SAMPLE QUESTIONS Click here for interactive quiz

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