The oculomotor system

Or

Fear and Loathing at the Orbit

Michael E. Goldberg, M.D.

First you tell them what your gonna tell them

The phenomenology of eye movements.

The anatomy and physiology of the extraocular muscles and nerves.

The supranuclear control of eye movements: motor control and cognitive plans.

The purposes of eye movements

Keep an object on the fovea

Fixation

Smooth pursuit

Keep the eyes still when the head moves

Vestibulocular reflex

Optokinetic reflex

Change what you are looking at ( move the fovea from one object to another)

Saccade

Change the depth plane of the foveal object

Vergence – eyes move in different directions

The vestibuloocular reflex.

The semicircular canals provide a head velocity signal.

The vestibuloocular reflex (VOR) provides an equal and opposite eye velocity signal to keep the eyes still in space when the head moves.

The vestibular signal habituates, and is supplemented by vision – the optokinetic response

Smooth pursuit matches eye velocity to target velocity

Saccades move the fovea to a new position

6 Muscles move the eyes

How the single eye moves

Horizontal:

Abduction (away from the nose)

Adduction (toward the nose).

Vertical:

Elevation (the pupil moves up)

Depression (the pupil moves down)

Torsional:

Intorsion: the top of the eye moves towards the nose

Extorsion: the top of the eye moves towards the ear.

The obliques are counterintuitive

Each oblique inserts behind the equator of the eye.

The superior oblique rotates the eye downward and intorts it!

The inferior oblique rotates the eye upward and extorts it.

Vertical recti tort the eye as well as elevate or depress it.

Oblique action depends on orbital position

The superior oblique depresses the eye when it is adducted (looking at the nose).

The superior oblique intorts the eye when it is abducted (looking towards the ear)

3 Cranial Nerves Control the Eye

Left fourth nerve palsy

Listing’s Law

Torsion must be constrained or else vertical lines would not remain vertical.

Listing’s law accomplishes this: the axes of rotation of the eye from any position to any other position lie in a single plane, Listing’s plane.

This is accomplished by moving the axis of rotation half the angle of the eye movement

The pulleys: something new in 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).

Pulley Anatomy

The pulleys

Horizontal rectus pulleys change their position with horizontal gaze.

Eye muscle nuclei

Oculomotor neurons describe eye position and velocity.

The transformation from muscle activation to gaze

The pulse of velocity and the step of position are generated independently.

For horizontal saccades the pulse is generated in the paramedian pontine reticular formation.

The step is generated in the medial vestibular nucleus and the prepositus hypoglossi by a neural network that integrates the velocity signal to derive the position signal.

Horizontal saccades are generated in the pons and medulla

Digression on Neural Integration

Intuitively, you move your eyes from position to position (the step).

Higher centers describe a saccadic position error.

The pontine reticular formation 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.

Neurons involved in the generation of a saccade

Generating the horizontal gaze signal

The medial rectus of one eye and the lateral rectus of the other eye must be coordinated.

This coordination arises from interneurons in the abducens nucleus that project to the contralateral medial rectus nucleus via the medial longitudinal fasciculus.

To reiterate

Ocular motor neurons describe eye position and velocity.

For smooth pursuit and the VOR the major signal is the velocity signal, which comes from the contralateral medial vestibular nucleus.

The neural integrator in the medial vestibular nucleus and nucleus prepositus hypoglossi converts the velocity signal into a position signal which holds eye position.

For horizontal saccades the paramedian pontine reticular formation converts the position signal from supranuclear centers into a velocity signal.

This signal is also integrated by the medial vestibular nucleus and the nucleus prepositus hypoglossi.

Abducens interneurons send the position and velocity signals to the oculomotor nucleus via the medial longitudinal fasciculus.

Vertical movements and vergence are organized in the midbrain

Internuclear ophthalmoplegia

The medial longitudinal fasciculus is a vulnerable fiber tract.

It is often damaged in multiple sclerosis and strokes.

The resultant deficit is internuclear ophthalmoplegia

The horizontal version signal cannot reach the medial rectus nucleus, but the convergence signal can.

Supranuclear control of saccades

The brainstem can make a rapid eye movement all by itself (the quick phase of nystagmus).

The supranuclear control of saccades requires controlling the rapid eye movement for cognitive reasons.

In most cases saccades are driven by attention

Humans look at where they attend

Supranuclear control of saccades

Supranuclear Control of Saccades

Superior colliculus drives the reticular formation to make contralateral saccades.

The frontal eye fields and the parietal cortex drive the colliculus.

The parietal cortex provides an attentional signal and the frontal eye fields a motor signal.

The substantia nigra inhibits the colliculus unless

It is inhibited by the caudate nucleus

Which is, in turn, excited by the frontal eye field.

The effect of lesions

Monkeys with collicular or frontal eye field lesions make saccades with a slightly longer reaction time.

Monkeys with combined lesions cannot make saccades at all.

Humans with parietal lesions neglect visual stimuli, and make slightly hypometric saccades with longer reaction times. Often their saccades are normal: if they can see it they can make saccades to it.

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

Antisaccades

Supranuclear control of pursuit: pursuit matches eye velocity to target velocity

Smooth pursuit

Requires cortical areas that compute target velocity, the dorsolateral pontine nuclei, and the cerebellum.

Utilizes many of the brainstem structures for the vestibuloocular reflex

Requires attention to the target.

Clinical deficits of smooth pursuit

Cerebellar and brainstem disease

Specific parietotemporal or frontal lesions

Any clinical disease with an attentional deficit – Alzheimer’s or any frontal dementia, schizophrenia


	The phenomenology of eye movements.
	The anatomy and physiology of the extraocular muscles and nerves.
	The supranuclear control of eye movements: motor control and cognitive plans.


	Keep an object on the fovea
		Fixation
		Smooth pursuit
	Keep the eyes still when the head moves
		Vestibulocular reflex
		Optokinetic reflex
	Change what you are looking at ( move the fovea from one object to another)
		Saccade
	Change the depth plane of the foveal object
		Vergence – eyes move in different directions


	The semicircular canals provide a head velocity signal.
	The vestibuloocular reflex (VOR) provides an equal and opposite eye velocity signal to keep the eyes still in space when the head moves.


	Horizontal:
		Abduction (away from the nose)
		Adduction (toward the nose).
	Vertical:
		Elevation (the pupil moves up)
		Depression (the pupil moves down)
	Torsional:
		Intorsion: the top of the eye moves towards the nose
		Extorsion: the top of the eye moves towards the ear.


	Each oblique inserts behind the equator of the eye.
	The superior oblique rotates the eye downward and intorts it!
	The inferior oblique rotates the eye upward and extorts it.
	Vertical recti tort the eye as well as elevate or depress it.


	The superior oblique depresses the eye when it is adducted (looking at the nose).
	The superior oblique intorts the eye when it is abducted (looking towards the ear)


	Torsion must be constrained or else vertical lines would not remain vertical.
	Listing’s law accomplishes this: the axes of rotation of the eye from any position to any other position lie in a single plane, Listing’s plane.
	This is accomplished by moving the axis of rotation half the angle of the eye movement


	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).


	The pulse of velocity and the step of position are generated independently.
	For horizontal saccades the pulse is generated in the paramedian pontine reticular formation.
	The step is generated in the medial vestibular nucleus and the prepositus hypoglossi by a neural network that integrates the velocity signal to derive the position signal.


	Intuitively, you move your eyes from position to position (the step).
	Higher centers describe a saccadic position error.
	The pontine reticular formation 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.


	The medial rectus of one eye and the lateral rectus of the other eye must be coordinated.
	This coordination arises from interneurons in the abducens nucleus that project to the contralateral medial rectus nucleus via the medial longitudinal fasciculus.


	Ocular motor neurons describe eye position and velocity.
	For smooth pursuit and the VOR the major signal is the velocity signal, which comes from the contralateral medial vestibular nucleus.
	The neural integrator in the medial vestibular nucleus and nucleus prepositus hypoglossi converts the velocity signal into a position signal which holds eye position.
	For horizontal saccades the paramedian pontine reticular formation converts the position signal from supranuclear centers into a velocity signal.
	This signal is also integrated by the medial vestibular nucleus and the nucleus prepositus hypoglossi.
	Abducens interneurons send the position and velocity signals to the oculomotor nucleus via the medial longitudinal fasciculus.


	The medial longitudinal fasciculus is a vulnerable fiber tract.
	It is often damaged in multiple sclerosis and strokes.
	The resultant deficit is internuclear ophthalmoplegia
	The horizontal version signal cannot reach the medial rectus nucleus, but the convergence signal can.


	The brainstem can make a rapid eye movement all by itself (the quick phase of nystagmus).
	The supranuclear control of saccades requires controlling the rapid eye movement for cognitive reasons.
	In most cases saccades are driven by attention


	Superior colliculus drives the reticular formation to make contralateral saccades.
	The frontal eye fields and the parietal cortex drive the colliculus.
	The parietal cortex provides an attentional signal and the frontal eye fields a motor signal.
	The substantia nigra inhibits the colliculus unless
	It is inhibited by the caudate nucleus
	Which is, in turn, excited by the frontal eye field.


	Monkeys with collicular or frontal eye field lesions make saccades with a slightly longer reaction time.
	Monkeys with combined lesions cannot make saccades at all.
	Humans with parietal lesions neglect visual stimuli, and make slightly hypometric saccades with longer reaction times. Often their saccades are normal: if they can see it they can make saccades to it.
	Humans with frontal lesions cannot make antisaccades.


	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


	Requires cortical areas that compute target velocity, the dorsolateral pontine nuclei, and the cerebellum.
	Utilizes many of the brainstem structures for the vestibuloocular reflex
	Requires attention to the target.


	Cerebellar and brainstem disease
	Specific parietotemporal or frontal lesions
	Any clinical disease with an attentional deficit – Alzheimer’s or any frontal dementia, schizophrenia