Oculomotor System Dr. G.R. Leichnetz

Why study eye movements? Abnormalities of ocular motility are often a clue to the localization of lesions and diagnosis of CNS disease…. because the neural networks for different types of eye movements involve structures throughout the CNS, which, when lesioned, produce very predictable and specific clinical deficits. For example, if one observes oculomotor deficits in saccades or smooth pursuit, the clinician knows what sub-set of structures belong to that particular neural network which could account for the deficits.

Since our eyes are embedded in our heads, the disturbances that most likely affect our vision are head perturbations. If we did not have eye movements the visual image would “slip” on the retina every time we moved our heads. Some eye movements stabilize our gaze (maintain fixation), while other eye movements allow us to shift our gaze to new objects of interest.

Types of Eye Movements Conjugate Disconjugate Modified from R. J. Leigh & D. S. Zee, The Neurology of Eye Movements All types are conjugate (both eyes move together in the same direction) except vergence, which is disconjugate.

Different types of eye movements have different underlying neural networks, but ultimately connect with specific groups of motor neurons within the extraocular motor nuclei (III, IV, VI), the “final common pathway” to the extraocular muscles, to produce appropriate eye movements . Different Pre-Oculomotor Neural Networks ?

Levator palpebrae (elevates upper lid) Lateral rectus Sup. rectus Levator palpebrae (elevates upper lid) Oculomotor (III): superior rectus inferior rectus medial rectus inferior oblique levator palpebrae Trochlear (IV): superior oblique Abducens (VI): lateral rectus Inf. rectus All the extraocular muscles are innervated by C.N. III, except the lateral rectus (VI) and superior oblique (IV). LR6SO4 Inf. oblique

Paired muscles function together to produce movements in three principal planes. Horizontal eye movements- medial and lateral rectus Upward eye movements- superior rectus and inferior oblique Downward eye movements- inferior rectus & superior oblique

Extraocular Motor Nuclei

The oculomotor nucleus contains separate motor neuron cell groups that innervate specific extraocular muscles: superior and inferior rectus, medial rectus, inferior oblique, and levator palpebrae Oculomotor complex Oculomotor complex Inf. rectus Sup. rectus Haines Inf. oblique Labelled motor neuron cell groups in the oculomotor nucleus after injection of HRP in target extraocular muscles. Medial rectus Haines, Fundamental Neuroscience

The trochlear nucleus, located in the caudal midbrain above the medial longitudinal fasciculus, innervates the superior oblique muscle . Trochlear nucleus MLF MLF Trochlear nucleus Labeled cells bodies of neurons in the trochlear nucleus after an HRP injection of the superior oblique muscle. MLF Haines

The abducens nucleus, located in the caudal pons below the facial colliculus, innervates the lateral rectus muscle. MLF MLF Abducens nucleus Haines The abducens nucleus after HRP injection into the lateral rectus muscle.

The abducens nucleus contains two populations of neurons:. 1 The abducens nucleus contains two populations of neurons: 1. Lateral rectus motor neurons- 70% 2. Internuclear neurons (project via the MLF to the contralateral medial rectus motor neurons)- 30%

Neural Networks for Different Types of Eye Movement

Vestibulo-Ocular System Second-order vestibular fibers that originate in the vestibular complex ascend through the MLF to the extraocular motor nuclei of III, IV, and VI. These vestibulo-ocular projections are canal-specific, and orchestrate reflexive compensatory eye movements to maintain fixation during head movement, the vestibulo-ocular reflex (VOR).

Precise vestibulo-ocular projections to specific motor neuron cell groups in the the oculomotor, trochlear, and abducens nuclei facilitate reflexive eye movements that compensate for head movements (to maintain fixation). Vestibulo-ocular Reflex (VOR) III IV Medial longitudinal fasciculus Vestibular complex VI

Saccadic System Saccades are rapid eye movements that shift gaze to an object (or event) of interest. Voluntary saccadic eye movements are initiated in the frontal eye field. Reflexive saccadic eye movements are initiated in the superior colliculus. Both the FEF and SC project to pre-oculomotor centers in the brainstem reticular formation adjacent to the extraocular motor nuclei.

Saccadic Eye Movements Voluntary saccadic eye movements are initiated in the frontal eye field. Reflexive saccadic eye movements are initiated in the superior colliculus. SC SC

Superior Colliculus S I D The superior colliculus is a laminated structure located in the tectum of the dorsal midbrain, concerned with the coordination of reflex saccades, which can occur in response to visual, auditory, or somatosensory stimuli. It receives direct retinal input which establishes a visual map in its superficial layer. Courtesy, Dr. Robert F. Spencer S I D An injection of tritiated amino acid into the eye labels the retinal input into the superficial layer of the superior colliculus. A map of the visual field is represented in the superficial layer.

The intermediate and deep layers of the SC are in registry with the visual map in the superficial layer. There is a retinotopic map of the visual world on the surface of the SC S I The deep layer is “motor” and is in registry with the visual map in the superficial layer. The intermediate layer is integrative; receives input from the FEF, cerebellum & basal ganglia, affecting motor output in deep layer. D When the SC initiates a reflexive saccade to look at an object, it can precisely target the location of the object in the visual world, so it can initiate an eye movement of appropriate amplitude and direction to bring the image onto the fovea of the retina.

The deep layer of the superior colliculus gives rise to projections to pre-oculomotor brainstem centers for reflexive saccadic eye movements, and tectospinals to cervical spinal cord to coordinate reflex head movements. Deep layers project to brainstem preoculomotor centers and cervical spinal cord Tectospinals descend to cervical cord to terminate on neck muscle motoneurons

Both the FEF and SC project to the pre-oculomotor saccade centers in the brainstem reticular formation near the extraocular motor nuclei. For vertical saccades- rostral iMLF and INC (midbrain) For horizontal saccades- PPRF (pons) Vertical Saccades (riMLF, INC) IV III VI Horizontal Saccades (PPRF) Lesions of either brainstem region are differentiated on the basis of oculomotor deficits in vertical vs. horizontal eye movements.

Center for Vertical Downward Saccades: Rostral Interstitial Nucleus of the Medial Longitudinal Fasciculus For Vertical Saccades: the preoculomotor nuclei, the rostral interstitial nucleus of the MLF (riMLF) and the interstitial nucleus of Cajal (INC) are located in the rostral midbrain reticular formation where it merges with the subthalamic region. riMLF STN SN From Haines, Fundamental Neuroscience riMLF riMLF Haines The rostral iMLF (premotor center for vertical downward saccades) is located in the rostralmost medial midbrain reticular formation where its neurons are interspersed among the rostralmost fibers of the MLF.

Center for Vertical Upward Saccades: Interstitial Nucleus of Cajal From Haines, Fundamental Neuroscience Oculomotor Complex INC Haines The interstitial nucleus of Cajal contains premotor neurons that project to cell groups in the oculomotor nuclei (superior rectus and inferior oblique) for vertical upward eye movements. Like the riMLF, it neurons are interspersed among the fibers of the rostral MLF.

For Horizontal Saccades: the preoculomotor center is located in the caudal medial pontine reticular formation, and is called the paramedian pontine reticular formation (PPRF). Abducens Nucleus PPRF Haines VI PPRF Large neurons in the PPRF have ascending branches to abducens nucleus, and descending projections to cervical spinal cord (for gaze) Haines The center for horizontal saccades (PPRF) contains premotor neurons that project to the abducens nucleus (lateral rectus motor neurons and internuclear neurons). It also projects to the cervical spinal cord for “gaze” (eye movement + head movement).

Horizontal Saccade Connections Frontal eye field Horizontal Saccade Connections Neurons in the PPRF project to the abducens nucleus (affecting ipsilateral lateral rectus motor neurons and internuclear neurons that project to the contralateral medial rectus motor neurons) for conjugate horizontal eye movements. Its large cells also project to the cervical spinal cord affecting head movement, hence “gaze.” Superior colliculus Oculomotor nucleus Abducens nucleus PPRF Modified from Haines To cervical spinal cord

Saccadic System Frontal Eye Field Superior Colliculus The FEF (voluntary saccades) and SC (reflexive saccades) both project to riMLF and INC (vertical saccades) and PPRF (horizontal saccades)

Smooth Pursuit Eye Movements Smooth pursuit eye movements are slow eye movements used to follow (track) a moving object across the visual scene. Pursuit eye movements cannot be produced voluntarily. To maintain fixation, the eyes must move at the same speed as the visual target (eye movement must match target velocity). To do this, the pursuit system involves seeing the object (visual cortex), analyzing visual motion (pre-occipital cortex, area MT), and calculating the appropriate size and velocity of eye movement (cerebellum).

Smooth Pursuit Pathway Visual Cortex to MT Visual Area (V5) to dorsolateral basilar pontine nucleus (DLPN) to “oculomotor part” of the posterior lobe vermis Lesion of these structures can result in pursuit deficits Visual Cortex Oculomotor Vermis Oculomotor vermis DLPN Dorsolateral pontine nucleus Posterior lobe

Optokinetic System When the visual scene is moving (eg. riding on a train) to maintain fixation on an object (following telephone poles) produces oscillating eye movements which consist of a slow component that follows the object and then a fast component where eyes snap back to look at the next pole, ie. eye movements similar to nystagmus, called optokinetic nystagmus, OKN. The neural network for these eye movements involves the pretectum (receives visual input from the retina), which projects to the reticulotegmental nucleus (NRTP) of the pons, which then relays the information to the cerebellum (flocculonodular lobe).

Optokinetic Pathway Retina and/or visual cortex to pretectal area to nucleus reticularis tegmenti pontis (NRTP) to flocculonodular cortex Lesion of these structures can produce OKN deficits. Visual cortex Retina Flocculus

Vergence Eye Movements Vergence eye movements are the only disjunctive type of eye movement. In convergence, both medial rectus muscles contract. The pathway subserving convergence is not well known. But what is known is that the neural pathway reaches the two medial rectus cell groups in the oculomotor nucleus w/o going through the MLF (convergence is preserved in an MLF lesion, ie. INO). Convergence is part of the “near response,” ie. focussing on a near object, involves: convergence accommodation (lens thickening) pupillary constriction

Oculomotor Lesions

Oculomotor (IIIrd) Nerve Palsy, left eye From: Fix, High-Yield Neuroanatomy Ptosis right left Mydriasis Exotropia With lesion of the left oculomotor nerve (C.N. III), the left eye is abducted (due to unopposed action of the lateral rectus). There is ipsilateral ptosis (paralysis of levator palpebrae) and the ipsilateral pupil is dilated (mydriasis; disruption of parasymp. fibers to constrictor pupillae). left left

Abducens (Sixth) Nerve Palsy, right eye left Ipsilateral eye does not abduct From: Fix, High-Yield Neuroanatomy Lesion of the right abducens nerve (C.N. VI) results in paralysis of the right lateral rectus muscle. When looking to the right, the right eye will not abduct. Esotropia. right

Abducens Nucleus Lesion Cannot abduct the ipsilateral eye or adduct the contralateral eye Right Right Left Lesion of abducens nucleus produces ipsilateral paralysis of conjugate horizontal eye movements (cannot abduct ipsilateral eye due to lesion of lateral rectus motoneurons, and cannot adduct contralateral eye due to lesion of internuclear neurons that project to contralateral medial rectus motor neurons)

MLF Lesion: right MLF Ipsilateral eye will not adduct. Right Left Abducens internuclear neurons project thru MLF to contralateral medial rectus motor neurons Lesion of MLF produces internuclear ophthalmoplegia, INO) cannot adduct eye ipsilateral to MLF lesion due to interruption of internuclear axons (but medial rectus will contract with convergence)

MLF Lesion: Internuclear Ophthalmoplegia, right eye Ipsilateral eye does not adduct right left Fix Lesion of the right MLF disrupts axons of internuclear neurons whose cell bodies are located in the abducens nucleus and which project to the right medial rectus cell group of the oculomotor nucleus. On looking to the left, the ipsilateral eye (on the lesioned side) will not adduct on attempted conjugate eye movement to the opposite side.. But since the medial rectus cell group itself is intact, the ophthalmologist can get adduction in convergence. Lesion of the MLF also produces nystagmus (disrupts VOR).

PPRF Lesion A lesion of the paramedian pontine reticular formation produces an ipsilateral paralysis of conjugate horizontal gaze. Ipsilateral conjugate horizontal gaze paralysis

Frontal Eye Field Lesion on right left Fix Lesion of the frontal eye field (area 8) on the right results in a paralysis of conjugate eye movements to the left. The eyes are deviated to the right (toward side of lesion). The FEF lesion disrupts projections to contralateral PPRF, resulting in a contralateral paralysis of conjugate horizontal gaze