Eye Movements Rotate the Eye in the Orbit
To a good approximation, the eye is a sphere that sits in a socket, the orbit. Eye movements are simply rotations of the eye in the orbit. The eye's orientation can be defined by three axes of rotation—horizontal, vertical, and torsional—that intersect at the center of the eyeball, and eye movements are described as rotations around these axes. Horizontal and vertical eye movements change the line of sight by redirecting the fovea; torsional eye movements rotate the eye around the line of sight but do not change gaze.
Horizontal rotation of the eye away from the nose is called abduction and rotation toward the nose is adduction. Vertical movements are referred to as elevation (upward rotation) and depression (downward rotation). Finally, torsional movements include intorsion (rotation of the top of the cornea toward the nose) and extorsion (rotation away from the nose).
Except for vergence, most eye movements are conjugate. For example, during gaze to the right the right eye abducts and the left eye adducts. Similarly, if the right eye extorts, the left eye intorts.
The Six Extraocular Muscles Form Three Agonist–Antagonist Pairs
Each eye is rotated by six extraocular muscles arranged in three agonist–antagonist pairs (Figure 39–4). The four rectus muscles (lateral, medial, superior, and inferior) share a common origin, the annulus of Zinn, at the apex of the orbit. They insert on the surface of the eye, or sclera, anterior to the eye's equator. The origin of the inferior oblique muscle is on the medial wall of the orbit; the superior oblique muscle's tendon passes through the trochlea, or pulley, before inserting on the globe, so that its effective origin is also on the medial wall of the orbit. The oblique muscles insert on the posterior globe.
The origins and insertions of the extraocular muscles.
A. Lateral view of the left eye with the orbital wall cut away. Each rectus muscle inserts in front of the equator of the globe so that contraction rotates the cornea toward the muscle. Conversely, the oblique muscles insert behind the equator and contraction rotates the cornea away from the insertion. The superior oblique muscle passes through a bony pulley, the trochlea, before it inserts on the globe. The levator muscle of the upper eyelid raises the lid.
B. Superior view of the left eye with the roof of the orbit and the levator muscle cut away. The superior rectus passes over the superior oblique and inserts in front of it on the globe.
Each muscle has a dual insertion. The part of the muscle farthest from the eye inserts on a soft-tissue pulley through which the rest of the muscle passes on its way to the eye. When the extraocular muscles contract, they not only rotate the eye but also change their pulling directions.
The actions of the extraocular muscles are determined by their geometry and by the position of the eye in the orbit. The medial and lateral recti rotate the eye horizontally; the medial rectus adducts, whereas the lateral rectus abducts. The superior and inferior recti and the obliques rotate the eye both vertically and torsionally. The superior rectus and inferior oblique elevate the eye, and the inferior rectus and superior oblique depress it. The superior rectus and superior oblique intort the eye, whereas the inferior rectus and inferior oblique extort it.
The relative amounts of vertical and torsional rotation produced by the superior and inferior recti and the obliques depend on eye position. The superior and inferior recti exert their maximal vertical action when the eye is abducted, that is, when the line of sight is parallel to the muscles' pulling directions. Conversely, the oblique muscles exert their maximal vertical action when the eye is adducted (Figure 39–5).
Each superior rectus and oblique muscle has both torsional and elevational actions.
How much elevation and torsion each muscle provides depends on the position of the eye. (Adapted, with permission, from von Noorden 1980.)
A. When eye position is in the primary visual axis (the y axis in the diagram) or lateral to it (abduction), elevation is provided by the superior rectus and all of the intorsion is from the superior oblique muscle. When the eye is positioned completely medial to the visual axis (adduction), intorsion comes predominantly from the superior rectus and most of the elevation comes from the inferior oblique.
B. When the eye is positioned 16 degrees or more laterally from the primary visual axis, the superior oblique intorts the eye and depression comes from the inferior rectus. When it is completely medial to the visual axis, the superior oblique rotates the eye vertically downward and all of the intorsion comes from the superior rectus.
Movements of the Two Eyes Are Coordinated
Humans and other animals with eyes in front have binocular vision. This facilitates stereopsis, the ability to perceive a visual scene in three dimensions, as well as depth perception. At the same time, binocular vision requires precise coordination of the movements of the two eyes so that both foveae are always directed at the target of interest. For most eye movements both eyes must move by the same amount and in the same direction. This is accomplished, in large part, through the pairing of eye muscles in the two eyes.
Just as each eye muscle is paired with its antagonist in the same orbit (eg, the medial and lateral recti), it is also paired with the muscle that moves the opposite eye in the same direction. For example, coupling of the left lateral rectus and right medial rectus moves both eyes to the left during a leftward saccade. The orientations of the vertical muscles are such that each pair consists of one rectus muscle and one oblique muscle. For example, the left superior rectus and the right inferior oblique both move the eyes upward in left gaze. The binocular muscle pairs are listed in Table 39–1.
Figure 39–6Vertical Muscle Action in Adduction and Abduction ||Download (.pdf) Figure 39–6 Vertical Muscle Action in Adduction and Abduction
|Muscle ||Action in adduction ||Action in abduction |
|Superior rectus ||Intorsion ||Elevation |
|Inferior rectus ||Extorsion ||Depression |
|Superior oblique ||Depression ||Intorsion |
|Inferior oblique ||Elevation ||Extorsion |
The Extraocular Muscles Are Controlled by Three Cranial Nerves
The extraocular muscles are innervated by groups of motor neurons whose cell bodies are clustered in three nuclei in the brain stem (Figure 39–6). The lateral rectus is innervated by the abducens nerve (cranial nerve VI), whose nucleus lies in the pons in the floor of the fourth ventricle. The superior oblique muscle is innervated by the trochlear nerve (cranial nerve IV), whose nucleus is located in the midbrain at the level of the inferior colliculus. (The trochlear nerve gets its name from the trochlea, the bony pulley through which the superior oblique muscle travels.)
The ocular motor nuclei in the brain stem.
The nuclei are shown in a parasagittal section through the thalamus, pons, midbrain, and cerebellum of a rhesus monkey. The oculomotor nucleus (cranial nerve III) lies in the midbrain at the level of the mesencephalic reticular formation. The trochlear nucleus (nerve IV) is slightly caudal, and the abducens nucleus (nerve VI) lies in the pons at the level of the paramedian pontine reticular formation, adjacent to the fasciculus of the facial nerve (VII). Compare Figure 45–5. (iC, interstitial nucleus of Cajal; iMLF, interstitial nucleus of the medial longitudinal fasciculus; nD, nucleus of Darkshevich; VN, vestibular nuclei.) (Adapted, with permission, from Henn et al. 1984.)
All the other extraocular muscles—the medial, inferior, and superior recti and the inferior oblique—are innervated by the oculomotor nerve (cranial nerve III), whose nucleus lies in the midbrain at the level of the superior colliculus. The oculomotor nerve also contains fibers that innervate the levator muscle of the upper eyelid. Cell bodies of axons innervating both eyelids are located in the central caudal nucleus, a single midline structure within the oculomotor complex. Finally, traveling with the oculomotor nerve are parasympathetic fibers that innervate the iris sphincter muscle, the constrictor of the pupil, and the ciliary muscles that adjust the curvature of the lens to focus the eye during accommodation.
The pupil and eyelid also have sympathetic innervation, which originates in the intermediolateral cell column of the ipsilateral upper thoracic spinal cord. Fibers of these neurons synapse on cells in the superior cervical ganglion in the upper neck. Axons of these postganglionic cells travel along the carotid artery to the carotid sinus and then into the orbit. Sympathetic pupillary fibers innervate the iris dilator muscle, causing the pupil to dilate and thus providing the pupillary component of the so-called "fight or flight" response. Sympathetic fibers also innervate Müller's muscle, a secondary elevator of the upper eyelid. The sympathetic control of pupillary dilatation and lid elevation is responsible for the "wide-eyed" look of excitement and sympathetic overload.
The best way to understand the actions of the extraocular muscles is to consider the eye movements that remain after a lesion of a specific nerve (Box 39–1).
Box 39–1 Extraocular Muscle or Nerve Lesions
Patients with lesions of the extraocular muscles or their nerves complain of double vision (diplopia) because the images of the object of gaze no longer fall on the corresponding retinal locations in both eyes. Lesions of each nerve produce characteristic symptoms that depend on which extraocular muscles are affected. In general, double vision increases when the patient tries to look in the direction of the weak muscle. Abducens Nerve
A lesion of the abducens nerve (VI) causes weakness of the lateral rectus. When the lesion is complete the eye cannot abduct beyond the midline, such that a horizontal diplopia increases when the subject looks in the direction of the affected eye. Trochlear Nerve
A lesion of the trochlear nerve (IV) affects both torsional and vertical eye movements. When the patient looks straight ahead, the affected eye is above the normal eye (Figure 39–7A). The difference increases when the patient looks to the right, adducting the eye with the weak muscle (Figure 39–7B left), and decreases when the patient looks to the left, abducting the eye (Figure 39–7B right), because the superior oblique predominantly depresses the eye in adduction.
The deficit is worse when patients attempt to depress and adduct the eye, but improves when they elevate the adducted eye (Figure 39–7C). Patients with superior oblique paresis often keep their heads tilted away from the affected eye. A tilt of the head to one side, such that one ear is pointed downward, induces a small torsion of the eye in the opposite direction, known as ocular counter-roll.
When the head tilts to the left, the left eye is ordinarily intorted by the left superior rectus and left superior oblique, while the right eye is extorted by the right superior rectus and right inferior oblique. The elevation action of the superior rectus is canceled by the depression action of the superior oblique, so the eye only rotates. When the head tilts to the right, the inferior oblique and inferior rectus extort the left eye and the superior oblique relaxes.
With paresis of the left superior oblique, when the head tilts to the left the elevation of the superior rectus is unopposed and the eye moves upward (Figure 39–7D right). The diplopia can be minimized by tilting the head to the right (Figure 39–7D left). Oculomotor Nerve
A lesion of the oculomotor nerve (III) has complex effects because this nerve innervates multiple muscles. A complete lesion spares only the lateral rectus and superior oblique muscles. Thus the paretic eye is typically deviated downward and abducted at rest, and it cannot move medially or upward from a middle position. Downward movement is partially affected because the inferior rectus muscle is weak but the superior oblique is preserved.
Because the fibers that control lid elevation, accommodation, and pupillary constriction travel in the oculomotor nerve, damage to this nerve also results in drooping of the eyelid (ptosis), blurred vision for near objects, and pupillary dilation (mydriasis). Although sympathetic innervation is still intact with an oculomotor nerve lesion, the ptosis is essentially complete, since Müller's muscle contributes less to elevation of the upper eyelid than does the levator muscle of the upper eyelid. Sympathetic Oculomotor Nerves
Sympathetic fibers innervating the eye arise from the thoracic spinal cord, traverse the apex of the lung, and ascend to the eye on the outside of the carotid artery.
Interruption of the sympathetic pathways to the eye yields Horner syndrome, whose characteristic features are a partial ipsilateral ptosis owing to weakness of Müller's muscle and a relative constriction (miosis) of the ipsilateral pupil. The pupillary asymmetry is most pronounced in low light because the normal pupil is able to dilate but the pupil affected by Horner syndrome is not.
Effect of a left trochlear nerve palsy.
The trochlear nerve innervates the superior oblique muscle, which inserts behind the equator of the eye. It depresses the eye when it is adducted and intorts the eye when it is abducted.
A. Hypertropia occurs when the eye is in the center of the orbit and the left eye is slightly above the right eye.
B. The hypertropia is worse when the eye is adducted because the unopposed inferior oblique pushes the eye higher (left). The condition is improved when the eye is abducted (right) because the superior oblique contributes less to depression than to intorsion.
C. When the patient looks to the right the hypertropia is worse on downward gaze (left) than it is on upward gaze (right).
D. The hypertropia is improved by head tilt to the right (left) and worsened by tilt to the left (right). The ocular counter-rolling reflex induces intorsion of the left eye on leftward head tilt, and extorsion of the eye on rightward head tilt (see Chapter 40). With leftward head tilt, intorsion requires increased activity of the superior rectus, whose elevating activity is unopposed by the weak superior oblique, causing increased hypertropia. With rightward head tilt and extorsion of the left eye, the unopposed superior rectus muscle is less active, and the hypertropia decreases.
Extraocular Motor Neurons Encode Eye Position and Velocity
We can illustrate how the gaze system generates eye movements by considering the activity of an oculomotor neuron during a saccade. To move the eye quickly to a new position in the orbit and keep it there, two passive forces must be overcome: the elastic force of the orbit, which tends to restore the eye to a central position in the orbit, and a velocity-dependent viscous force that opposes rapid movement. Thus the motor signal must include information about tonic position, which opposes the elastic force, and velocity, which overcomes orbital viscosity and moves the eye quickly to a new position.
Information about the position and velocity of the eye is conveyed by the discharge frequency of an oculomotor neuron (Figure 39–8). The firing rate of the neuron rises rapidly as the eye's velocity increases from 0 degrees to 900 degrees per second; this is called the saccadic pulse. The frequency of this pulse determines the speed of the saccade, whereas the duration of the pulse controls the duration of the saccade. The difference in the firing rates before and after the saccade is called the saccadic step. As described below, the pulse and step are generated by different brain stem structures.
Oculomotor neurons signal eye position and velocity.
A. The record is from an abducens neuron of a monkey. When the eye is positioned in the medial side of the orbit the cell is silent (position Θ0) . As the monkey makes a lateral saccade there is a burst of firing (D1), but in the new position (Θ1) the eye is still too far medial for the cell to discharge continually. During the next saccade there is a burst (D2), and at the new position (Θ2) there is a tonic position-related discharge. Before and during the next saccade (D3) there is again a pulse of activity and a higher tonic discharge when the eye is at the new position (Θ4) . When the eye makes a medial movement there is a period of silence during the saccade (D4) even though the eye ends up at a position associated with a tonic discharge. (Adapted, with permission, from A. Fuchs 1970.)
B. Saccades are associated with a step of activity, which signals the change in eye position, and a pulse of activity, which signals eye velocity. The neural activity corresponding to eye position and velocity is illustrated both as a train of individual spikes and as an estimate of the instantaneous firing rate (spikes per second).
Oculomotor neurons differ from skeletal motor neurons in several ways. Although the extraocular muscles are rich in sensors resembling the muscle spindles of skeletal muscles, there are no ocular stretch reflexes. Oculomotor neurons do not have recurrent inhibitory connections. All oculomotor neurons participate equally in all types of eye movements; no motor neurons are specialized for saccades or smooth pursuit.
However, like skeletal motor units, eye motor units are recruited in a fixed sequence (see Chapter 38). Regardless of the type of eye movement, the specific ocular motor neurons recruited depend on the position of the eye in the orbit and the desired eye velocity. For example, as the eye moves laterally the number of active abducens neurons increases, causing more muscle fibers in the lateral rectus to contract.