Chapter 8D - Control of Eye Movements
Types of eye movements
Although the eyes can be moved voluntarily, most eye movements are through reflexes. The principal types of movement include voluntary motion (both vertical and horizontal), tracking (both voluntary and involuntary) and convergence. Additionally, there are pupillary reactions and control of the lens.
Muscles of the eye
Eye position and motion is controlled by six muscles in each eye. All muscles are tonically active to maintain stability of the eyes. Each eye can be adducted, abducted, elevated, depressed, intorted or extorted. Additionally, this motion must be conjugate in order to prevent diplopia. Horizontal eye movements are controlled by the medial and lateral rectus muscles (adduct and abduct the eyes, respectively). Every movement that elevates the eye above or depresses below the horizontal plane requires the participation of at least two muscles because the axis of the orbit and the muscles of the eye are not directly in line with the visual axis. Accordingly, isolated contraction of the superior or inferior rectus muscles or the superior or inferior oblique muscles results in torsion and deviation of the eye during the process of elevation and depression. For this reason, at least two muscles are primarily active whenever the eyes are elevated or depressed. When looking straight up, the superior rectus and inferior oblique act together. Looking straight down employs the inferior rectus and superior oblique. The six positions of gaze are used to simplify analysis of eye muscle weakness (see figure 27).
Extraocular cranial nerves & nuclei
There are three cranial nerves innervating eye muscles. The oculomotor nerve, CNIII, innervates all of the extraocular muscles with the exception of the lateral rectus and superior oblique. It also innervates the elevator of the upper lid. These motor nerve fibers arise from the oculomotor nucleus, located within the midbrain just ventral to the periaqueduct gray. In addition to motor nerve fibers, the oculomotor nerve contains parasympathetic preganglionic nerve fibers. These nerve fibers synapse in the ciliary ganglion with postganglionic fibers going to the constrictor of the pupil and to the ciliary muscle. Contraction of the ciliary muscle results in the lens becoming rounder, to allow for close focus. The parasympathetic nerve fibers in the oculomotor nerve arise from the Edinger-Westphal nucleus, which is located in the midline between the left and right oculomotor nuclei.
The oculomotor nerve leaves the midbrain in the interpeduncular fossa (figure 15), passes between the superior cerebellar artery and the posterior cerebral artery and enters the dura. It passes through the wall of the cavernous sinus to reach the superior orbital fissure of the skull, which is how it enters the orbit. The cavernous sinus is immediately adjacent to the sella turcica at the skull base, which contains the pituitary gland.
The trochlear nerve, CNIV arises from the trochlear nucleus (figure 15), crosses within the brain stem, and exits from the dorsal side of the brain stem at the ponto-mesencephalic junction. As with the oculomotor nerve, the trochlear nerve passes through the superior orbital fissure after traveling within the wall of the cavernous sinus and innervates the superior oblique muscle.
The abducens nerve, CNVI, innervates the lateral rectus muscle. This nerve arises from motor neurons in the abducens nucleus, which is located at the facial colliculus in the floor of the fourth ventricle in the caudal pons. This nerve exits from the pontomedullary junction and follows a long course through the dura (figure 15). The abducens nerve courses through the cavernous sinus in contact with the internal carotid artery and passes into the orbit through the superior orbital fissure.
Neurons in extraocular nuclei have tonic activity. When the nerve or nucleus is damaged, the eye will drift in the direction of pull of the remaining, intact muscles. Abducens palsy (lateral rectus weakenss) will result in medial drift of the eye, while damage to the trochelar nerve (superior oblique weakness) results in extorsion of the eye.
Voluntary eye movements
Voluntary eye movements occur in small jumps called saccades. These rapid movements occur so fast that the eye cannot see during the movement. Frequent small jumps (microsaccades) occur even when the eye is still.
Voluntary horizontal gaze and vertical gaze utilize different neuronal circuitry. Voluntary conjugate horizontal gaze is initiated by neurons in the frontal eye fields of the cerebral cortex (figure 28). Activation of the right frontal eye field will cause the eyes to look to the left and activation of the left frontal eye field will cause the eyes to look to the right. Projections from the frontal eye field go directly and indirectly (via the superior colliculus) to the contralateral paramedian pontine reticular formation (the PPRF). The PPRF, the region of reticular formation immediately ventral to the abducens nucleus, contains neurons that are critical for generating horizontal saccades. Damage to the left PPRF, for example, will completely prevent the movement of either eye to the left. Projections from the PPRF go to the ipsilateral abducens nucleus and, through the medial longitudinal fasciculus, to the contralateral oculomotor nucleus. This results in conjugate eye movement away from the frontal eye field that started the process and towards the side of the PPRF that was involved in the movement. The medial longitudinal fasciculus (MLF) is the link that yokes the medial movement of one eye to lateral movement of the other eye during lateral gaze. Damage to the MLF permits the abducting eye to move, while preventing the adducting eye from following (internuclear ophthalmoplegia).
Voluntary vertical gaze follows a different pathway (figure 29). First of all, there is no single cortical center responsible for vertical gaze. Instead, diffuse areas of the cortex project to the rostral interstitial nucleus of the MLF (Cajal; located in the rostral midbrain). This nucleus projects bilaterally to the oculomotor and trochlear nuclei, with many of these fibers passing through the posterior commissure. Damage to the rostral interstitial nucleus or the posterior commissure can impair voluntary vertical gaze while still permitting reflex vertical movement. This can be seen with pathology of the rostral, dorsal midbrain.
Vestibulo-ocular reflex
The vestibulo-ocular reflex (VOR) (figure 20) produces eye movement in response to changes in head position. This is an extraordinarily accurate reflex that allows the eyes to remain focused on a target when the head moves. This is reflected in a 1:1 "gain" of this reflex (i.e., 3 degrees of head motion should cause an opposing 3 degrees of eye movement). Projections from the vestibular nerve terminate in the vestibular nucleus and cerebellar flocculus. Many neurons in the vestibular nucleus project to the extraocular nuclei and paramedian pontine reticular formation. The medial longitudinal fasciculus carries many of these connections. With abnormal vestibular input, the eyes will drift away from the direction of perceived motion (vertigo). However, if the person is awake, there will be saccades to reacquire the visual image as it begins to drift. This is the substrate for jerk nystagmus.
The VOR is a reflex response that must be adjusted over time. For example, if there is damage to the vestibular apparatus of an ear, there will be diminished input on that side. Nonetheless, the reflex must still maintain a "gain" of 1:1 causing the eyes to move contrary to head movement if vision is to be stabilized.
Tracking/smooth pursuit eye movements
Most of our normal voluntary eye movements are not smooth, but rather occur in saccades. However, we are able to move our eyes smoothly when tracking a moving object (figure 30). Smooth pursuit eye movements utilize some of the vestibulo-ocular reflex pathways and require a visual input to the occipital cortex in order to permit locking of the eyes onto the target. The occipital eye fields are not as well defined as the frontal eye field. They are located in the region near the junction of the occipital lobes with the posterior parietal and temporal lobes (including visual association areas that are involved in detecting motion).
The occipital eye fields project directly and indirectly to the pontine nuclei. Pontocerebellar fibers carry these signals to the flocculus of the cerebellum. As described above, the flocculus is part of the vestibulo-ocular circuitry. The flocculus, in turn, is connected to the vestibular complex and, as described above, the vestibular complex is capable of generating smooth eye movements in all directions via connections to the extraocular nuclei.
There are two reflexes that use the same wiring as smooth pursuit movements (figure 30). These are the fixation reflexes and the optokinetic reflexes. "Fixation reflex" refers to the ability to fixate on a target that is moving. When the head is moving this reflex complements the VOR to stabilize the eyes. The optokinetic reflex (nystagmus; OKN) is an involuntary fixation on objects that are moving in relationship to the head. This is classically observed when looking out of the side of a moving vehicle and has been termed "railway nystagmus". The eyes will have the tendency to track moving objects, especially if they have very starkly contrasting features. They will track for a distance and then subsequently saccade in the opposite direction to reacquire a target. If one visual cortex is damaged, optokinetic nystagmus will be lost when objects move toward the side of the cortex lesion (that is, if they approach an individual from the side of vision impairment).
Vergence
Another type of normal movement is called vergence. This refers to convergence or divergence of the eyes in order to focus on objects that are closer or further away from the individual. Vergence requires that the occipital lobes be intact and the pathway involves the rostral midbrain reticular formation (adjacent to the oculomotor nuclei) where there are neurons that are active during vergence activities. The details of this pathway are less well understood than for some of the other eye movement pathways although it is wired in parallel with accommodation (contraction of the ciliary muscle and pupillary constrictor muscle). This linkage appears to be due to interconnections between midbrain neurons projecting to the Edinger-Wesphal nucleus (for accommodation) and neurons projecting to the oculomotor nucleus to adduct (converge) the eyes.
Pupillary light reflex
The pupillary light reflex is consensual (bilateral) constriction of the pupil in response to light stimuli. Collateral axons from the optic nerve terminate in the pretectal nuclei. Light triggers bilateral projections from the pretectum to the Edinger-Westfall nucleus to produce pupillary constriction via the parasympathetic division of CNIII.
The superior colliculus
The superior colliculus is less important in humans than many other species (where it may be the primary generator of eye movements). Nonetheless it is a center for certain head and neck reflex movements. The superior colliculus receives retinotopic visual input, auditory input (from the inferior colliculus), somatic sensation from the spinal cord as well as input from the cerebral cortex and substantia nigra, pars reticulata. It projects to areas controlling eye movements, such as the PPRF and midbrain reticular formation as well as to the cervical spinal cord. These latter projections are through the tectospinal tract. It is likely that the superior colliculus triggers reflex head and eye movements towards stimuli of interest, such as flashes of light or loud noises.
Summary
In summary, there are several types of eye movements that have distinct anatomy and physiology. Pathways for voluntary horizontal gaze and for voluntary vertical gaze are distinct from one another and can be damaged separately. The vestibulo-ocular reflex is critical for stabilizing the eyes when the head is moving and utilizes many of the same neuronal pathways used by smooth pursuit or tracking eye movements. Vergence and the responses of accommodation for near vision are triggered simultaneously when examining objects nearer than a few meters from the eyes.