DOCUMENTO MÉTODOS ANTICONCEPTIVOS

Key Notes

Eye movements either keep the gaze fixed on an object when the head is turning, or shift the gaze to follow a moving object. Gaze fixation is brought about by the vestibulo-ocular reflex, which relies on signals from the semicircular ducts, and the optokinetic reflex which depends on visual input. Gaze shift can be produced either by saccades (fast), smooth pursuit (slow) or vergence movements. Vergence allows an object to be tracked as it approaches or recedes and requires the eyes to move in opposite directions.

The actions of three pairs of muscles allow the eyes to be rotated about three principal axes. During conjugate eye movements in which both eyes move in the same direction, eye muscle activity in one eye is

complementary to eye muscle activity in the other. The extraocular muscles are controlled by motor neurons in the nuclei of the oculomotor, trochlear and abducens nerves, which in turn are driven by brainstem reticular and medial vestibular nuclei. Firing of eye motor neurons encodes the velocity of the movement and the change in eye position. Rotation of the head, detected by the semicircular ducts, causes a well- matched opposite rotation of the eyes to keep the retinal image

stationary. For large horizontal head rotations, once the eyes have rotated as far as possible they are rapidly reset to frontwards gaze. This causes nystagmus, flickering eye movements with slow phases in which the gaze is fixed and fast phases when gaze is reset. Vestibulo-ocular reflexes adapt in response to alterations in visual input. This is an example of motor learning by the cerebellum.

Slow head rotation causes images to move across the retina. This triggers eye movement in the opposite direction. Nystagmus occurs for large rotations.

Fast movements taking the fovea to a new point in visual space are saccades, produced reflexly by visual, auditory or somatosensory stimuli. Burst cells in brainstem reticular nuclei are directly responsible for the signals to the eye motor neurons, but saccades are produced in response to activity in the superior colliculus and frontal cortex. The superior colliculus generates reflex saccades. Because it has sensory and motor maps, each point in the superior colliculus represents a location in sensory space and specifies the saccades necessary to point the gaze towards it. The size and direction of saccades is actually determined by the average firing of many collicular neurons. The frontal eye fields, located in the frontal cortex, trigger saccades via connections with the superior colliculus and brainstem, and basal ganglia. The frontal cortex is responsible for intentional saccades.

Eye movements Extraocular eye muscle control Vestibulo-ocular reflexes (VORs) Saccades Optokinetic reflexes (OKRs)

Eye movements The purpose of eye movements is either gaze stabilization, in which the eyes remain fixated on an object during rotation of the head, or gaze shifting which allows the central part of the retina, the fovea, to be brought to bear on an object, or track a moving object. Five types of eye movements, each controlled by a distinct neural system, bring about these aims.

Gaze stabilization is controlled by the vestibulo-ocular and optokinetic systems. Rapid head rotation, detected by the semi-circular ducts provides input for vestibulo-ocular reflexes (VOR), whereas optokinetic reflexes depend on visual input to monitor slow head rotations. For both systems their output causes conjugate eye movements in the opposite direction to the head rotation, so that retinal images do not shift.

Three systems organize gaze shift. The saccadic system generates extremely rapid eye movements, saccades, which move the gaze from one point in the visual field to another, bringing new targets onto the fovea. The smooth pursuit system permits gaze to follow a moving target, so that its image remains on the fovea. Finally, for animals with binocular vision, the vergence system allows the eyes to move in opposite directions (disjunctive movements); either both converge or both diverge, so that both eyes can remain directed towards an object as it gets closer or recedes.

The output of all five eye motor systems is via oculomotor neurons in the brainstem, the axons of which run in three pairs of cranial nerves to the skeletal muscles that move the eyes.

Each eye is moved by three pairs of extraocular eye muscles. Two pairs of rectus muscles (superior and inferior, medial and lateral) originate from a common annular tendon attached at the back of the orbit. These muscles insert into the sclera in front of the equator of the eyeball. The third pair is the oblique muscles (superior and inferior) which insert into the sclera behind the equator of the eyeball (Fig. 1).

Working in concert these muscles act to rotate the eye about three principal axes (Fig. 2). The actions of the medial and lateral rectus muscles are simple. They cause the eye to rotate about the vertical axis so that the gaze moves hori- zontally. The medial rectus brings about rotation towards the midline (adduc- tion) while the lateral rectus causes lateral rotation (abduction). The other two pairs of muscles produce rotations that have components along two of the Extraocular eye

muscle control

These are used to voluntarily track an object that is moving in the visual field. The velocity of the object is signaled by the cortex of the visual ‘where’ system to neurons in the pons. These cells convert the velocity signals to smooth pursuit motor commands.

Signals for vergence include blurring of the retinal image or the degree of accommodation and require the visual cortex. Fast vergence movements are made during saccades.

Related topics Balance (F5) Cerebellar function (K6)

Eye and visual pathways (G2) Basal ganglia function (K8)

Cortical control of voluntary movement (K1)

G8 – Oculomotor control 185

Smooth pursuit movements

principal axes, and the components change depending on the horizontal posi- tion of the eye. These actions are summarized in Table 1.

Eye muscles act in complementary fashion in the two eyes during conjugate movements in which the two visual axes move in parallel. Thus, contraction of the lateral rectus in one eye is coupled with contraction of the medial rectus in the other eye for a conjugate horizontal shift in gaze (see Table 1).

The extraocular muscles are innervated by motor neurons in the nuclei of the oculomotor (III), trochlear (IV) or abducens (VI) cranial nerves. These neurons are the final common path for the output of all five eye-movement systems and are driven by brainstem reticular and medial vestibular nuclei axons that run in the medial longitudinal fasciculus. Eye motor neurons fire both statically, in a manner relating to eye position, and dynamically, reflecting eye velocity. To hold the eye steady in a given position requires tonic discharge by a particular set of motor neurons. The set will be different for different positions. Each motor neuron fires with a frequency needed to maintain eye position, so its firing rate is linearly related to position. Activity by a given neuron is not needed for all positions (e.g. sustained leftward gaze requires high firing rates of motor units in the left lateral rectus, but the left medial rectus is an antagonist of this movement so its motor neurons remain silent).

Superior rectus

Superior oblique

Annular ligament

Lateral rectus (cut)

Inferior rectus

Medial rectus Optic nerve (cut)

Maxilla

Inferior oblique Eyeball Trochlea Frontal bone

Fig. 1. The right orbit showing the extraocular muscles.

Adduction/ abduction Horizontal axis Gaze Intorsion/extorsion Elevation/depression Vertical axis Anteroposterior axis

Fig. 2. Principal axis for rotation of the eye, shown for the right eye. In health, torsional movements (rotation about the anteroposterior axis) are small.

Eye movements are brought about by high-frequency pulses of action poten- tials in oculomotor neurons. The discharge rate during a pulse is directly propor- tional to the velocity of the movement. The eye movement will bring the eye to a new position, which needs the generation of a new position signal. This is thought to be achieved by integrating the velocity signal, an operation probably done by the vestibulocerebellum and prepositus nucleus of the brainstem reticular system. Head rotation detected by the semicircular ducts triggers equal and opposite rota- tion of both eyes. For large head rotations the eyes cannot continue to rotate but must be reset to a central position by rapidly moving in the same direction as the head. This gives rise to nystagmus, eye movements characterized by slow phases that stabilize the retinal image, and quick phases that reset the eyes. By conven- tion the direction of the nystagmus is the direction of the quick phase (Fig. 3).

The horizontal semicircular ducts are effectively wired to the medial and lateral rectus muscles to produce the eye movements that counter the head rota- tion (Fig. 4).

The gain of the VOR (the magnitude of the eye rotation divided by the magni- tude of the head rotation) is quite close to one for fast head rotations. This means there is a good match between eye and head movements, which makes for a stable retinal image. The VOR can be modified by visual experience. When human subjects wear magnifying lenses, which means that they should make bigger eye movements to match head rotations, the gain of their vestibulo- ocular reflexes increases appropriately over the next few days. The cerebellum is required for this adaptation to occur, but not for it to be maintained once estab- lished. The instability of the retinal image acts as an error signal which is Vestibulo-ocular

reflexes (VORs)

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Table 1. Actions of extraocular eye muscles. For the muscles moving the eye vertically the action is different depending on whether the eye is also abducted or adducted. For example, the superior rectus elevates the eye if the lateral rectus is active at the same time, but causes intorsion if the eye is adducted by the medial rectus.

Contralateral eye

Muscle Innervation Movement complementary muscle

Lateral rectus Abducens (VI) Abduction Medial rectus Medial rectus Oculomotor (III) Adduction Lateral rectus Superior rectus Oculomotor (III) Elevation and intorsion Inferior oblique Inferior rectus Oculomotor (III) Depression and extorsion Superior oblique Inferior oblique Oculomotor (III) Extorsion and elevation Superior rectus Superior oblique Trochlear (IV) Intorsion and depression Inferior rectus

Eye position Left Right Slow phase Quick phase Time