First you tell them what your gonna The oculomotor system tell them

• The phenomenology of movements. Or • The anatomy and physiology of the Fear and Loathing at the and . • The supranuclear control of eye Michael E. Goldberg, M.D. movements: motor control and cognitive plans.

The purposes of eye movements The vestibuloocular .

• Keep an object on the fovea • • • The semicircular canals provide a head • Keep the still when the head moves velocity signal. • Vestibulocular reflex • Optokinetic reflex • The vestibuloocular reflex (VOR) • Change what you are looking at ( move the provides an equal and opposite eye fovea from one object to another) velocity signal to keep the eyes still in • space when the head moves. • Change the depth plane of the foveal object • – eyes move in different directions

The vestibular signal habituates, and is supplemented Smooth pursuit matches eye by vision – the velocity to target velocity

1 6 Muscles move the eyes move the fovea to a new position Levator Palpebrae Superior Rectus

Lateral Rectus

Medial Rectus

Superior Oblique

Inferior Oblique

Inferior Rectus

How the single eye moves The obliques are counterintuitive

• Horizontal: • Each oblique inserts • Abduction (away from the nose) behind the equator of the eye. • Adduction (toward the nose). • The superior oblique •Vertical: rotates the eye • Elevation (the moves up) downward and intorts it! • Depression (the pupil moves down) • The inferior oblique rotates the eye upward • Torsional: and extorts it. • Intorsion: the top of the eye moves towards the • Vertical recti tort the nose eye as well as elevate • Extorsion: the top of the eye moves towards the or depress it. ear.

Oblique action depends on orbital 3 Control the Eye

position Levator Palpebrae

Superior Rectus • The superior oblique depresses the eye Inferior Rectus when it is adducted III: (looking at the Oculomotor Medial Rectus nose).

• The superior oblique Inferior Oblique intorts the eye when Nerve IV: it is abducted Trochlear (looking towards the Superior Oblique ear) Nerve VI: Lateral Rectus Abducens

2 Left fourth nerve palsy Listing’s Law • Hyperopia in central . • Worse on right gaze. • Torsion must be constrained or else vertical • Better on left gaze. lines would not remain vertical. • Worse looking down to right • Listing’s law accomplishes this: the axes of • Better looking up to rotation of the eye from any position to any right. other position lie in a single plane, Listing’s • Head tilt to right plane. improves gaze. • This is accomplished by moving the axis of • Head tilt to left worsens rotation half the angle of the gaze.

The pulleys: something new in Pulley Anatomy orbital anatomy and physiology.

• How is Listing’s law accomplished? • Extraocular muscles have two layers • A global layer that inserts on the sclera • An orbital layer that inserts on a collagen-elastin structure between the orbit and globe. This structure serves as a PULLEY through which the global layer moves the eye. • Moving the pulleys accomplish listings law. (Demer).

Horizontal rectus pulleys change The pulleys their position with horizontal gaze.

3 Eye muscle nuclei Oculomotor neurons describe eye position and velocity.

Mesencephalic Eye position – the step Reticular Lateral Medial Formation

Inferior Colliculus

III Abducens neuron Eye velocity – the pulse IV Sp/s Pulse

Step VI Neuron Medial - Lateral Eye Position Eye Pontine Abducens neuron Nuclei

Horizontal saccades are generated in The transformation from muscle the and medulla activation to gaze Thalamus Superior Colliculus • The pulse of velocity and the step of position are generated independently. Medial • For horizontal saccades the pulse is III longitudinal generated in the paramedian pontine reticular IV fasciculus formation. Cerebellum • The step is generated in the medial vestibular Paramedian and the prepositus hypoglossi by a VI neural network that integrates the velocity Pontine Reticular signal to derive the position signal. Formation Vestibular Nuclei and Pontine Nuclei Hypoglossi

Neurons involved in the generation Digression on Neural Integration of a saccade • Intuitively, you move your eyes from position to position (the step). • Higher centers describe a saccadic position error. • The pontine changes the position error to a desired velocity (the pulse). • The vestibulo-ocular reflex also provides the desired velocity. • In order to maintain eye position after the velocity signal has ended, this signal must be mathematically integrated.

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4 Generating the horizontal gaze Left lateral rectus Right medial rectus . signal and Paramedian nerve: motor pontine reticular neurons only • The medial rectus of one eye and the formation (saccade velocity) Medial lateral rectus of the other eye must be longitudinal Abducens fasciculus coordinated. nucleus: motor neurons and • This coordination arises from interneurons. interneurons in the Medial that project to the contralateral medial vestibular nucleus: eye rectus nucleus via the medial position, VOR longitudinal fasciculus. and smooth Nucleus prepositus pursuit velocity hypoglossi (eye position)

Vertical movements and vergence are To reiterate organized in the

• Ocular motor neurons describe eye position and velocity. Mesencephalic • For smooth pursuit and the VOR the major signal is the Reticular Thalamus velocity signal, which comes from the contralateral medial Formation Superior Colliculus vestibular nucleus. • The neural integrator in the medial vestibular nucleus and rIMLF Inferior Colliculus nucleus prepositus hypoglossi converts the velocity signal into a position signal which holds eye position. III • For horizontal saccades the paramedian pontine reticular formation converts the position signal from supranuclear Medial IV Longitudinal centers into a velocity signal. Cerebellum • This signal is also integrated by the medial vestibular nucleus Fasciculus and the nucleus prepositus hypoglossi. Paramedian • Abducens interneurons send the position and velocity signals VI to the oculomotor nucleus via the medial longitudinal Pontine fasciculus. Reticular Formation Pontine Vestibular Nuclei Nuclei

Internuclear ophthalmoplegia Supranuclear control of saccades • The medial longitudinal fasciculus is a vulnerable fiber tract. • The can make a rapid eye • It is often damaged in multiple sclerosis movement all by itself (the quick phase and strokes. of ). • The resultant deficit is internuclear • The supranuclear control of saccades ophthalmoplegia requires controlling the rapid eye • The horizontal version signal cannot movement for cognitive reasons. reach the medial rectus nucleus, but the • In most cases saccades are driven by convergence signal can.

5 Supranuclear control of saccades Humans look at where they attend

Posterior Parietal Cortex

Frontal Eye Field

Caudate Nucleus

Superior Colliculus

Reticular Formation

Supranuclear Control of Saccades The effect of lesions

• Superior colliculus drives the reticular formation to • Monkeys with collicular or frontal eye field lesions make contralateral saccades. make saccades with a slightly longer reaction time. • The and the parietal cortex drive the • Monkeys with combined lesions cannot make colliculus. saccades at all. • The parietal cortex provides an attentional signal and • Humans with parietal lesions neglect visual stimuli, the frontal eye fields a motor signal. and make slightly hypometric saccades with longer • The substantia nigra inhibits the colliculus unless reaction times. Often their saccades are normal: if • It is inhibited by the caudate nucleus they can see it they can make saccades to it. • Which is, in turn, excited by the frontal eye field. • Humans with frontal lesions cannot make antisaccades.

The Antisaccade Task The Antisaccade Task

• Look away from a stimulus. • The parietal cortex has a powerful signal describing the attended stimulus. • The colliculus does not respond to this signal. • The frontal motor signal drives the eyes away from the stimulus. • Patients with frontal lesions cannot ignore the stimulus, but must respond to the parietal signal

6 Antisaccades Supranuclear control of pursuit: pursuit

Supplementary Eye Field matches eye velocity to target velocity Middle temporal and middle Frontal Eye Field superior temporal (MT and MST) Posterior Parietal Cortex provides the trigger provide the velocity signal to start the pursuit. Frontal Eye Field Striate Cortex

Caudate Nucleus

Superior Colliculus Substantia Nigra Pars Reticulata Dorsolateral Cerebellum vermis and Reticular Formation Vestibular nucleus

Smooth pursuit Clinical deficits of smooth pursuit

• Requires cortical areas that compute • Cerebellar and brainstem disease target velocity, the dorsolateral pontine • Specific parietotemporal or frontal nuclei, and the cerebellum. lesions • Utilizes many of the brainstem • Any clinical disease with an attentional structures for the vestibuloocular reflex deficit – Alzheimer’s or any frontal • Requires attention to the target. dementia, schizophrenia

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